Skip to main content
SpringerLink
Log in

Humoral immune responses and gill antioxidant-related gene expression of common carp (Cyprinus carpio) exposed to lufenuron and flonicamide

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

The aim of this study was to investigate plasma proteins, total immunoglobulin (Ig), lysozyme and complement (ACH50) levels, and gill superoxide dismutase (SOD) and catalase (CAT) gene expression in common carp (Cyprinus carpio), following exposure to lufenuron (LUF) and flonicamide (FL). Fish were distributed in 12 tanks as three quadrupled treatments: control (fish were kept in pesticide-free water), LUF [fish exposed to 10% of LUF LC50 (4.3 mg/L)], and FL [fish exposed to 10% of FL LC50 (0.1 mg/L)]. The plasma parameters were assessed after 7 and 21 days exposure to pesticides, whereas the gene expressions were assessed after 21 days. The results showed that LUF exposure significantly decreased plasma total protein and globulin levels compared to the control group. Both pesticide significantly decreased plasma total Ig levels compared to the control group; however, LUF exhibited a greater effect. There were no significant effects of pesticides or sampling time on plasma ACH50 activity. Pesticides and sampling time interacted to affect plasma lysozyme activity. Seven days after exposure, both pesticides significantly increased lysozyme activity, and the effect of FL was greater than LUF. Nevertheless, there was no significant difference in plasma lysozyme activities among the pesticides, 21 days after the exposure. Both pesticides significantly decreased SOD and CAT gene expression, nevertheless, FL exhibited greater effects than LUF. In conclusion, both pesticides induced immunosuppression in the fish, though such effects were more severe in LUF group, compared to the FL. These pesticides negatively affect expression of gill antioxidant genes, and the FL effects were greater than the LUF.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alak G, Ucar A, Parlak V, Yeltekin AÇ, Taş IH, Ölmez D, Kocaman EM, Yılgın M, Atamanalp M, Yanık T (2017) Assessment of 8-hydroxy-2-deoxyguanosine activity, gene expression and antioxidant enzyme activity on rainbow trout (Oncorhynchus mykiss) tissues exposed to biopesticide. Comp Biochem Physiol C Toxicol Pharmacol 203:51–58

    Article  CAS  Google Scholar 

  • Arkoosh MR, Van Gaest AL, Strickland SA, Hutchinson GP, Krupkin AB, Hicks MBR, Dietrich JP (2018) Dietary exposure to a binary mixture of polybrominated diphenyl ethers alters innate immunity and disease susceptibility in juvenile Chinook salmon (Oncorhynchus tshawytscha). Ecotoxicol Environ Saf 163:96–103

    Article  CAS  Google Scholar 

  • Banaee M, Haghi BN, Ibrahim ATA (2013) Sub-lethal toxicity of chlorpyrifos on common carp, Cyprinus carpio (Linnaeus, 1758): biochemical response. Int J Aquat Biol 1:281–288

    Google Scholar 

  • Ceyhun SB, Şentürk M, Ekinci D, Erdoğan O, Çiltaş A, Kocaman EM (2010) Deltamethrin attenuates antioxidant defense system and induces the expression of heat shock protein 70 in rainbow trout. Comp Biochem Physiol C Toxicol Pharmacol 152:215–223

    Article  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: Stolen JS (ed) Techniques in fish immunology, vol 1. SOS publication, Fair Haven, pp 101–103

    Google Scholar 

  • Galal AA, Reda RM, Mohamed AA-R (2018) Influences of Chlorella vulgaris dietary supplementation on growth performance, hematology, immune response and disease resistance in Oreochromis niloticus exposed to sub-lethal concentrations of penoxsulam herbicide. Fish Shellfish Immunol 77:445–456

    Article  CAS  Google Scholar 

  • Ghelichpour M, Taheri Mirghaed A (2019) Effects of sublethal exposure to new pesticides lufenuron and flonicamid on common carp, Cyprinus carpio, hydromineral balance to further saltwater exposure. Int J Aquat Biol 7:195–201

    Google Scholar 

  • Ghelichpour M, Taheri Mirghaed A, Mirzargar SS, Joshaghani H, Ebrahimzadeh Mousavi H (2017) Plasma proteins, hepatic enzymes, thyroid hormones and liver histopathology of Cyprinus carpio (Linnaeus, 1758) exposed to an oxadiazin pesticide, indoxacarb. Aquac Res 48:5666–5676. https://doi.org/10.1111/are.13390

    Article  CAS  Google Scholar 

  • Ghelichpour M, Mirghaed AT, Mirzargar SS, Joshaghani H, Mousavi HE (2018) Modification of saltwater stress response in Cyprinus carpio (Linnaeus, 1758) pre-exposed to pesticide indoxacarb. Ecotoxicol Environ Saf 147:139–143

    Article  CAS  Google Scholar 

  • Ghelichpour M, Taheri Mirghaed A, Hoseini SM, Perez Jimenez A (2019a) Plasma antioxidant and hepatic enzymes activity, thyroid hormones alterations and health status of liver tissue in common carp (Cyprinus carpio) exposed to lufenuron. Aquaculture in press:734634 doi:https://doi.org/10.1016/j.aquaculture.2019.734634

    Article  Google Scholar 

  • Ghelichpour M, Mirghaed AT, Hoseinifar SH, Khalili M, Yousefi M, Van Doan H, Jimenez AP (2019b) Expression of immune, antioxidant and stress related genes in different organs of common carp exposed to indoxacarb. Aquat Toxicol 208:208–216

    Article  CAS  Google Scholar 

  • Hansen B, Rømma S, Garmo Ø, Olsvik P, Andersen R (2006) Antioxidative stress proteins and their gene expression in brown trout (Salmo trutta) from three rivers with different heavy metal levels. Comp Biochem Physiol C Toxicol Pharmacol 143:263–274

    Article  CAS  Google Scholar 

  • Harabawy AS, Ibrahim ATA (2014) Sublethal toxicity of carbofuran pesticide on the African catfish Clarias gariepinus (Burchell, 1822): hematological, biochemical and cytogenetic response. Ecotoxicol Environ Saf 103:61–67

    Article  CAS  Google Scholar 

  • Haschek WM, Rousseaux CG, Wallig MA (2009) Fundamentals of toxicologic pathology. Academic Press, San Diego

    Google Scholar 

  • Hedayati A, Hoseini SM, Ghelichpour M (2014) Acute toxicity of waterborne manganese to Rutilus caspicus (Yakovlev, 1870)–gill histopathology, immune indices, oxidative condition, and saltwater resistance. Toxicol Environ Chem 96:1535–1545. https://doi.org/10.1080/02772248.2015.1028408

    Article  CAS  Google Scholar 

  • Hoseini SM, Nodeh AJ (2011) Acute toxicity of potassium permanganate to Caspian roach Rutilus rutilus caspicus in two size classes and under different aeration conditions. Toxicol Environ Chem 93:996–1001. https://doi.org/10.1080/02772248.2011.568484

    Article  CAS  Google Scholar 

  • Hoseini SM, Hedayati A, Ghelichpour M (2014) Plasma metabolites, ions and thyroid hormones levels, and hepatic enzymes′ activity in Caspian roach (Rutilus rutilus caspicus) exposed to waterborne manganese. Ecotoxicol Environ Saf 107:84–89. https://doi.org/10.1016/j.ecoenv.2014.05.002

    Article  CAS  PubMed  Google Scholar 

  • Hoseini SM, Hedayati A, Taheri Mirghaed A, Ghelichpour M (2016) Toxic effects of copper sulfate and copper nanoparticles on minerals, enzymes, thyroid hormones and protein fractions of plasma and histopathology in common carp Cyprinus carpio. Exp Toxicol Pathol 68:493–503

    Article  CAS  Google Scholar 

  • Hoseini SM, Yousefi M, Hoseinifar SH, Van Doan H (2019) Cytokines' gene expression, humoral immune and biochemical responses of common carp (Cyprinus carpio, Linnaeus, 1758) to transportation density and recovery in brackish water. Aquaculture 504:13–21

    Article  CAS  Google Scholar 

  • Kavitha P, Rao JV (2007) Oxidative stress and locomotor behaviour response as biomarkers for assessing recovery status of mosquito fish, Gambusia affinis after lethal effect of an organophosphate pesticide, monocrotophos. Pestic Biochem Physiol 87:182–188

    Article  CAS  Google Scholar 

  • Kim J-H, Kang J-C (2015) Oxidative stress, neurotoxicity, and non-specific immune responses in juvenile red sea bream, Pagrus major, exposed to different waterborne selenium concentrations. Chemosphere 135:46–52

    Article  CAS  Google Scholar 

  • Kreutz LC, Barcellos LJG, dos Santos ED, Pivato M, Zanatta R (2012) Innate immune response of silver catfish (Rhamdia quelen) exposed to atrazine. Fish Shellfish Immunol 33:1055–1059

    Article  CAS  Google Scholar 

  • Lee C-S, Lim C, Webster CD (2015) Dietary nutrients, additives, and fish health. Wiley-Blackwell, Hoboken

    Book  Google Scholar 

  • Lerebours A, Gonzalez P, Adam C, Camilleri V, Bourdineaud JP, Garnier-Laplace J (2009) Comparative analysis of gene expression in brain, liver, skeletal muscles, and gills of zebrafish (Danio rerio) exposed to environmentally relevant waterborne uranium concentrations. Environ Toxicol Chem Int J 28:1271–1278

    Article  CAS  Google Scholar 

  • Li X, Liu L, Zhang Y, Fang Q, Li Y, Li Y (2013) Toxic effects of chlorpyrifos on lysozyme activities, the contents of complement C3 and IgM, and IgM and complement C3 expressions in common carp (Cyprinus carpio L.). Chemosphere 93:mm428–mm433. https://doi.org/10.1016/j.chemosphere.2013.05.023

    Article  CAS  Google Scholar 

  • Ma J, Bu Y, Li X (2015) Immunological and histopathological responses of the kidney of common carp (Cyprinus carpio L.) sublethally exposed to glyphosate. Environ Toxicol Pharmacol 39:1–8

    Article  Google Scholar 

  • Morita M, Ueda T, Yoneda T, Koyanagi T, Haga T (2007) Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding. Pest Manag Sci 63:969–973

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Siwicki A, Anderson D (1993) Nonspecific defense mechanisms assay in fish: II. Potential killing activity of neutrophils and macrophages, lysozyme activity in serum and organs and total immunoglobulin level in serum. In: Siwicki A, Anderson D, Waluga J (eds) Fish disease diagnosis and prevention methods. Wydawnictwo Instytutu Rybactwa Srodladowego, Olsztyn, pp 105–112

    Google Scholar 

  • Slaninova A, Smutna M, Modra H, Svobodova Z (2009) REVIEWS oxidative stress in fish induced by pesticides. Neuroendocrinol Lett 30:2

    CAS  PubMed  Google Scholar 

  • Soares PRL, de Andrade ALC, Santos TP, da Silva SCBL, da Silva JF, dos Santos AR, da Silva Souza EHL, da Cunha FM, Teixeira VW, Cadena MRS (2016) Acute and chronic toxicity of the benzoylurea pesticide, lufenuron, in the fish, Colossoma macropomum. Chemosphere 161:412–421

    Article  Google Scholar 

  • Stara A, Machova J, Velisek J (2012) Effect of chronic exposure to simazine on oxidative stress and antioxidant response in common carp (Cyprinus carpio L.). Environ Toxicol Pharmacol 33:334–343

    Article  CAS  Google Scholar 

  • Taheri Mirghaed A, Fayaz S, Hoseini SM (2018a) Dietary 1, 8-cinoele affects serum enzymatic activities and immunological characteristics in common carp (Cyprinus carpio) exposed to ambient ammonia. Aquac Res 50:146–153. https://doi.org/10.1111/are.13877

    Article  CAS  Google Scholar 

  • Taheri Mirghaed A, Hoseini SM, Ghelichpour M (2018b) Effects of dietary 1, 8-cineole supplementation on physiological, immunological and antioxidant responses to crowding stress in rainbow trout (Oncorhynchus mykiss). Fish Shellfish Immunol 81:182–188. https://doi.org/10.1016/j.fsi.2018.07.027

    Article  CAS  PubMed  Google Scholar 

  • Vázquez MP, Vázquez PP, Galera MM, Moreno AU (2014) Comparison of two ionic liquid dispersive liquid–liquid microextraction approaches for the determination of benzoylurea insecticides in wastewater using liquid chromatography–quadrupole-linear ion trap–mass spectrometry: evaluation of green parameters. J Chromatogr A 1356:1–9

    Article  Google Scholar 

  • Velasques RR, Sandrini JZ, da Rosa CE (2016) Roundup® in zebrafish: effects on oxidative status and gene expression. Zebrafish 13:432–441

    Article  CAS  Google Scholar 

  • Wang T, Long X, Liu Z, Cheng Y, Yan S (2015) Effect of copper nanoparticles and copper sulphate on oxidation stress, cell apoptosis and immune responses in the intestines of juvenile Epinephelus coioides. Fish Shellfish Immunol 44:674–682. https://doi.org/10.1016/j.fsi.2015.03.030

    Article  CAS  PubMed  Google Scholar 

  • Yano T (1992) Assays of hemolytic complement activity. In: Stolen JS (ed) Techniques in fish immunology, vol 2. SOS publication, Fair Haven, pp 131–141

    Google Scholar 

  • Yousefi M, Paktinat M, Mahmoudi N, Pérez-Jiménez A, Hoseini SM (2016) Serum biochemical and non-specific immune responses of rainbow trout (Oncorhynchus mykiss) to dietary nucleotide and chronic stress. Fish Physiol Biochem 42:1417–1425

    Article  CAS  Google Scholar 

  • Yousefi M, Hoseini SM, Vatnikov YA, Kulikov EV, Drukovsky SG (2019) Rosemary leaf powder improved growth performance, immune and antioxidant parameters, and crowding stress responses in common carp (Cyprinus carpio) fingerlings. Aquaculture 505:473–480

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Aquatic Animal Health, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran

    Ali Taheri Mirghaed & Melika Baes

  2. Inland Waters Aquatic Resources Research Center, Iranian Fisheries Science Research Institute, Agricultural Research, Education and Extension Organization, Gorgan, Iran

    Seyyed Morteza Hoseini

Authors
  1. Ali Taheri Mirghaed
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melika Baes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Seyyed Morteza Hoseini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ali Taheri Mirghaed.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taheri Mirghaed, A., Baes, M. & Hoseini, S.M. Humoral immune responses and gill antioxidant-related gene expression of common carp (Cyprinus carpio) exposed to lufenuron and flonicamide. Fish Physiol Biochem 46, 739–746 (2020). https://doi.org/10.1007/s10695-019-00747-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00747-x

Keywords

Search

Navigation