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Effects of ammonium sulfate on stress physiology and innate immunity of Western mosquitofish (Gambusia affinis)

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Abstract

Fertilizers increase yield of crops but may have unintended negative effects on fish as a byproduct of runoff into bodies of freshwater. The objective of this study was to determine if environmentally relevant concentrations of an ammonium fertilizer impacts stress and innate immunity in Western mosquitofish (Gambusia affinis). The mosquitofish were exposed to different concentrations of ammonium sulfate fertilizer: 0 ppm, 40 ppm, and 80 ppm. To test the effects of ammonium sulfate on stress physiology, cortisol released into water by individual fish was collected after 1 week of exposure and again after 2 weeks of exposure and quantified with an enzyme immunoassay. Cortisol levels in the 0-ppm group were not significantly different over the course of the study, but we found a significant increase in cortisol levels in the fish exposed to 40 ppm and 80 ppm. We found reduced survival in fish from the 40 ppm and 80 ppm of ammonium sulfate groups compared with the 0-ppm group. We also used blood samples to complete a lysozyme assay as a measure of innate immune defense. Higher concentrations of ammonium sulfate correlated with significantly lower lysozyme activity in the fish. Overall, our results suggest that relatively low amounts of ammonium sulfate runoff into bodies of water are likely to have negative sublethal and lethal effects on small fishes.

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References

  • Aertz J, Metz JR, Ampe B, Decostere A, Filk G, Saeger SD (2015) Scales tell a story on the stress history of fish. PLoS One 10:e0123411

    Google Scholar 

  • Alexander JB, Ingram GA (1992) Noncellular nonspecific defence mechanisms of fish. Annu Rev Fish Dis 2:249–279

    Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Google Scholar 

  • Breckels RD, Neff BD (2010) Pollution-induced behavioural effects in the brown bullhead (Ameiurus nebulosus). Ecotoxicology 19:1337–1346

    CAS  PubMed  Google Scholar 

  • Brown JA (1993) Endocrine responses to environmental pollutants. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman and Hall Fish and Fisheries Series, vol 9. Springer, Dordrecht

    Google Scholar 

  • Buonocore F, Randelli E, Trisolino P, Facchiano A, de Pascale D, Scapigliati G (2014) Molecular characterization, gene structure and antibacterial activity of a g-type lysozyme from the European sea bass (Dicentrarchus labrax L.). Mol Immunol 82:10–18

    Google Scholar 

  • Callewaert L, Michiels CW (2010) Lysozymes in the animal kingdom. J Biosci 35:127–160

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chien SH, Gearhart M, Villagarcia S (2011) Comparison of ammonium sulfate with other nitrogen and sulfur fertilizers in increasing crop production and minimizing environmental impact: a review. Soil Sci 176:327–335

    CAS  Google Scholar 

  • Constable M, Charlton M, Jensen F, McDonald K, Craig G, Taylor KW (2003) An ecological risk assessment of ammonia in the aquatic environment. Hum Ecol Risk Assess 9:527–548

    CAS  Google Scholar 

  • Dunier M, Siwicki AK (1993) Effects of pesticides and other organic pollutants in the aquatic environment on immunity of fish: a review. Fish Shellfish Immunol 3:423–438

    Google Scholar 

  • Eddy FB, Williams EM (1987) Nitrite and freshwater fish. Chem Ecol 3:1–38

    CAS  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: Stolen JS, Fletcher DP, Anderson BS et al (eds) Techniques in fish immunology. SOS Publications, Fair Haven, pp 101–103

    Google Scholar 

  • Ellis T, James JD, Stewart C, Scott AP (2004) A non-invasive stress assay based upon measurement of free cortisol released into the water by rainbow trout. J Fish Biol 65:1233–1252

    CAS  Google Scholar 

  • Fageria NK, Santos AB, Moraes MF (2010) Influence of urea and ammonium sulfate on soil acidity indices in lowland rice production. Commun Soil Sci Plant Anal 41:1565–1575

    CAS  Google Scholar 

  • Fast MD, Hosoya S, Johnson SC, Afonso LOB (2008) Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short- and long-term stress. Fish Shellfish Immunol 24:194–204

    CAS  PubMed  Google Scholar 

  • Fromm PO (1980) A review of some physiological and toxicological responses of freshwater fish to acid stress. Environ Biol Fish 5:79–93

    CAS  Google Scholar 

  • Gao FY, Qu L, Yu SG, Ye X, Tian YY, Zhang LL, Bai JJ, Lu M (2012) Identification and expression of three c-type lysozymes in Oreochromis aureus. Fish Shellfish Immunol 32:779–788

    CAS  PubMed  Google Scholar 

  • Grindley J (1946) Toxicity to rainbow trout and minnows of some substances known to be present in waste water discharge to rivers. Ann Appl Biol 33:103–112

    CAS  PubMed  Google Scholar 

  • Harper C, Wolf JC (2009) Morphologic effects of the stress response in fish. ILAR 50:387–396

    CAS  Google Scholar 

  • Havas M, Rosseland BO (1995) Response of zooplankton, benthos, and fish to acidification: an overview. Water Air Soil Pollut 85:51–62

    CAS  Google Scholar 

  • Hikima J, Hiorono I, Aoki T (2003) The lysozyme gene in fish. In: Shimizu N, Aoki T, Hirono I, Takashima F (eds) Aquatic Genomics. Springer, Tokyo, pp 301–309

    Google Scholar 

  • Hontela A, Rasmussen JB, Audet C, Chevalier G (1992) Impaired cortisol stress response in fish from environments polluted by PAHs, PCBs, and mercury. Arch Environ Contam Toxicol 22:278–283

    CAS  PubMed  Google Scholar 

  • Jensen FB (2003) Nitrite disrupts multiple physiological functions in aquatic animals. Comp Biochem Physiol 135:9–24

    Google Scholar 

  • Kültz D (2015) Physiological mechanisms used by fish to cope with salinity stress. J Exp Biol 218:1907–1914

    PubMed  Google Scholar 

  • Lewis WM, Morris DP (1986) Toxicity of nitrite to fish: a review. Trans Am Fish Soc 115:183–195

    CAS  Google Scholar 

  • Lie Ø, Evensen Ø, Sorensen A, Froysadal E (1989) Study on lysozyme activity in some fish species. Dis Aquat Org 6:1–5

    CAS  Google Scholar 

  • Little AG, Seebacher F (2015) Temperature determines toxicity: bisphenol A reduces thermal tolerance in fish. Environ Pollut 197:84–89

    CAS  PubMed  Google Scholar 

  • Magnadottir B (2006) Innate immunity of fish (overview). Fish Shellfish Immunol 20:137–151

    CAS  PubMed  Google Scholar 

  • Mazeaud MM, Mazeaud F, Donaldson EM (1977) Primary and secondary effects of stress in fish: some new data and a general review. Trans Am Fish Soc 106:201–212

    CAS  Google Scholar 

  • Mock A, Peters G (1990) Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handling, transport and water pollution. J Fish Biol 37:873–885

    Google Scholar 

  • Mulla MS (1966) Toxicity of new organic insecticides to mosquito fish and some other aquatic organisms. Mosquito News 1:87–91

    Google Scholar 

  • Pascual P, Pedrajas JR, Toribio F, Lopez-Barea J, Peinado J (2003) Effects of food deprivation on oxidative stress biomarkers in fish (Sparus aurata). Chemico-Biol Interact 145:191–199

    CAS  Google Scholar 

  • Philips S, Laanbroek HJ, Verstraete W (2002) Origin, causes and effects of increased nitrite concentrations in aquatic environments. Rev Environ Sci Biotechnol 1:115–141

    CAS  Google Scholar 

  • Pickering AD, Pottinger TD, Christie PJ (1982) Recovery of the brown trout Salmo trutta from acute handling stress: a time course study. J Fish Biol 20:229–244

    Google Scholar 

  • Pickering AD, Pottinger TD, Sumpter JP, Carragher JF, Le Bail PY (1991) Effects of acute and chronic stress on the levels of circulating growth hormone in the rainbow trout Oncorynchus mykiss. Gen Comp Endocrinol 83:86–93

    CAS  PubMed  Google Scholar 

  • Pyke GG (2008) Plague minnow or mosquito fish? A review of the biology and impacts of introduced Gambusia species. Annu Rev Ecol Evol Syst 39:171–191

    Google Scholar 

  • Rakers S, Gebert M, Uppalapati S, Meyer W, Maderson P, Sell AF, Kruse C, Paus R (2011) ‘Fish matters’: the relevance of fish skin biology to investigate dermatology. Exp Dermatol 10:1600–1625

    Google Scholar 

  • Ram RN, Sathyanesan AG (1986) Inclusion bodies: formation and degeneration of the oocytes in the fish Channa punctatus (Bloch) in response to ammonium sulfate treatment. Ecotoxicol Environ Saf 11:272–276

    CAS  PubMed  Google Scholar 

  • Ram RN, Sathyanesan AG (1987) Histopathological changes in liver and thyroid of the teleost fish, Channa punctatus (Bloch), in response to ammonium sulfate fertilizer treatment. Ecotoxicol Environ Saf 13:185–190

    CAS  PubMed  Google Scholar 

  • Ram RN, Singh SK (1988) Long-term effect of ammonium sulfate fertilizer on histophysiology of adrenal in the teleost, Channa punctatus (Bloch). Bull Environ Contam Toxicol 41:880–887

    CAS  PubMed  Google Scholar 

  • Richardson J (1997) Acute ammonia toxicity for eight New Zealand indigenous freshwater species. N Z J Mar Freshw Res 31:185–190

    CAS  Google Scholar 

  • Roche H, Boge G (1996) Fish blood parameters as a potential tool for identification of stress caused by environmental factors and chemical intoxication. Mar Envioron Res 41:27–43

    CAS  Google Scholar 

  • Russo RC (1985) Ammonia, nitrite and nitrate. In: Rand GM, Petrocelli SR (eds) Fundamentals of aquatic toxicology. Hemisphere Publishing Corporation, Washington, pp 455–471

    Google Scholar 

  • Ryan JA, Hightower LE (1994) Evaluation of heavy-metal ion toxicity in fish cells using a combined stress protein and cytotoxicity assay. Environ Toxicol Chem 13:1231–1240

    CAS  Google Scholar 

  • Saurabh S, Sahoo PK (2008) Lysozyme: an important defense molecule of fish innate immune system. Aquac Res 39:223–239

    CAS  Google Scholar 

  • Savci S (2012) An agricultural pollutant: chemical fertilizer. International Journal of Environmental Science and Development. https://doi.org/10.7763/IJESD.2012.V3.191

  • Schram E, Roques JAC, Abbink W, Spanings T, de Vries P, Bierman S, van de Vis H, Flik G (2010) The impact of elevated water ammonia concentration on physiology, growth and feed intake of African catfish (Clarias gareipinus). Aquaculture 306:108–115

    CAS  Google Scholar 

  • Schreck CB (2009) Stress and fish reproduction: The roles of allostasis and hormesis. Gen Comp Endocrinol 165:549–556

    PubMed  Google Scholar 

  • Schulte PM (2014) What is environmental stress? Insights from fish living in a variable environment. J Exp Biol 217:23–34

    PubMed  Google Scholar 

  • Segner H (1987) Response of fed and starved roach, Rutilus rutilus, to sublethal copper contamination. J Fish Biol 30:423–437

    CAS  Google Scholar 

  • Small BC, Bilodeau AL (2005) Effects of cortisol and stress on channel catfish (Ictalurus punctatus) pathogen susceptibility and lysozyme activity following exposure to Edwardsiella ictaluri. Gen Comp Endocrinol 142:256–262

    CAS  PubMed  Google Scholar 

  • Subramanian S, MacKinnon SL, Ross NW (2007) A comparative study on innate immune parameters in the epidermal mucus of various fish species. Comp Biochem Physiol B 148:256–263

    PubMed  Google Scholar 

  • Surace M, Geoffery S (2016) Female body size and reproduction in western mosquitofish (Gambusia affinis) from two ponds in central Ohio. Northeast Nat 23:1–10

    Google Scholar 

  • Swenton DM, Kodric-Brown A (2012) Habitat and life history differences between two species of Gambusia. Environ Biol Fish 94:669–680

    Google Scholar 

  • Takahara T, Yamanaka H, Suzuki AA, Honjo MN, Minamoto T, Yonekura R, Itayama T, Kohmatsu Y, Ito T, Kawabata Z (2011) Stress response to daily temperature fluctuations in common carp, Cyprinus carpio L. Hydrobiologia 675:65–73

    Google Scholar 

  • Tomasso JR, Davis KB, Simco BA (1981) Plasma corticosteroid dynamics in channel catfish (Ictalurus punctatus) exposed to ammonia and nitrite. Can J Fish Aquat Sci 38:1106–1112

    CAS  Google Scholar 

  • Tort L (2011) Stress and immune modulation in fish. Dev Comp Immunol 35:1366–1375

    CAS  PubMed  Google Scholar 

  • Vijayan MM, Ballantyne JS, Leatherland JF (1991) Cortisol induced changes in some aspects of intermediary metabolism of Salvelinus fontinalis. Gen Comp Endcrinol 82:476–486

    CAS  Google Scholar 

  • Wallen IE, Greer WC, Lasater R (1957) Toxicity to “Gambusia affinis” of certain pure chemicals in turbid waters. Sewage Indust Waste 29:695–711

    CAS  Google Scholar 

  • Wendelaar Bonga SE (1997) The stress response in fish. Physiol Rev 77:591–625

    CAS  PubMed  Google Scholar 

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Funding

This study was funded by an Undergraduate Student Research Grant from the Illinois State Academy of Science to E. Schnabel and by the Millikin University Biology Department.

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Correspondence to Travis E. Wilcoxen.

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All methods were approved by the Millikin University Institutional Animal Care and Use Committee (Protocol 17-012).

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Schnabel, E., Wilcoxen, T.E. Effects of ammonium sulfate on stress physiology and innate immunity of Western mosquitofish (Gambusia affinis). Fish Physiol Biochem 46, 2027–2035 (2020). https://doi.org/10.1007/s10695-020-00855-z

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