Abstract
Annual rhythms are observed in many physiological processes and are an important approach to cope with seasonal stressors. The use of lower vertebrates as an experimental model is crucial to understand the evolution of this biological clock. This study aims to characterize the seasonal variability in the leukocyte immune responses in Channa punctatus. Leukocytes were harvested from peripheral blood and respiratory burst activity, leukocyte phagocytosis, and nitrite production were assessed to study innate immunity. Peripheral blood lymphocytes were segregated by centrifugation (density gradient) and proliferative responses of lymphocytes, in the presence of mitogens, were used to study cell-mediated immunity. Annual rhythms were validated in superoxide anion production, nitrite release and phagocytosis. Cosinor analysis revealed a differential pattern of lymphocyte proliferation which was dependent upon season and mitogen used. It was concluded that seasonal variation in immune activity might be associated with annual adaptation against diseases and the optimum immune status of seasonal breeders like fish helps them fight seasonal changes.
Similar content being viewed by others
References
Ahmad R, Haldar C (2008) Photoperiod-Testicular-Immune interaction in a seasonal breeder Indian palm squirrel Funambulus pennanti during the reproductively inactive and active phases. J Neuroendocrinol 21:2–9
Berger J, Slapnickova M (2003) Circadian structure of rat neutrophil phagocytosis. Comp Clin Pathol 12:84–89
Berridge MV, Herst PM, Tan AS (2005) Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction. Biotechnol Ann Rev. https://doi.org/10.1016/S1387-2656(05)11004-7
Bowden TJ, Butler R, Bricknell IR (2004) Seasonal variation of serum lysozyme levels in Atlantic halibut (Hippoglossus hippoglossus L). Fish Shellfish Immunol 17(2):129–135
Bowden TJ, Thompson KD, Morgan AL, Gratacap RML, Nikoskelainen S (2007) Seasonal variation and the immune response: a fish perspective. Fish Shellfish Immunol 22:695–706
Bromage N, Porter M, Randall C (2001) The environmental regulation of maturation in farmed finfish with special reference to the role of photoperiod and melatonin. Aquaculture 197:63–98
Buchtikova S, Simkova A, Rohlenova K, Flajshnas M, Lojek A, Lilius EM, Hyrsl P (2011) The seasonal changes in innate immunity of the common carp (Cyprinus carpio). Aquaculture 318:169–175
Cheng AC, Cheng SA, Chen YY, Chen JC (2009) Effects of temperature change on the innate cellular and humoral immune responses of orange-spotted grouper Epinephelus coioides and its susceptibility to Vibrio alginolyticus. Fish Shellfish Immunol 26(5):768–772
Collazos ME, Barriga C, Rincon EO (1996) Seasonal variations in the immune system of the tench, Tinca tinca (Cyprinidae): proliferative response of lymphocytes induced by mitogens. J Comp Physiol B 165(7):592–595
Cuesta A, Cerezuela R, Esteban MA, Meseguer J (2008) In vivo actions of melatonin on the innate immune parameters in the teleost fish gilthead seabream. J Pineal Res 45(1):70–78
Das A, Jena JK, Sahoo PK (2012) Haematological and innate immune responses in Puntius sarana: normal range and seasonal variation. Cent Eur J Biol 7:460–469
Ding AH, Nathan CF, Stuehr DJ (1988) Release of reactive nitrogen intermediated and Release of reactive nitrogen intermediated and reactive oxygen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production. J Immunol 141:2407–2412
Dunlap JC, Loros JJ, DeCoursey PJ (2004) Chronobiology: biological timekeeping. Sinauer Associates, Sunderland
Fallah FJ, Khara H, Roobi JD, Boorani MS (2014) Hematological parameters of Esox lucius in relation to different ages and seasons. Comp Clin Pathol 23:949–953
Fontaine P, Wang N, Hermelink B (2015) Broodstock management and control of the reproductive cycle. In: Kestemont P, Dabrowski K, Summerfelt RC (eds) Biology and culture of Percid fishes. Springer, Dordrecht, pp 61–100
Haldar C, Singh R, Guchhait P (2001) Relationship between the annual rhythms in melatonin and immune system status in the tropical palm squirrel Funambulus Pennanti,. Chronobiol Int 18(1):61–69
Hotchkiss AK, Nelson RJ (2002) Melatonin and immune function: hype or hypothesis? Crit Rev Immunol 22(5–6):351–371
Jorens PG, Matthys KE, Bult H (1995) Modulation of nitric oxide synthase activity in macrophages. Mediators Inflamm 4:75–89
Kaattari S, Ottinger C (2000) Seasonality of trout leukocytic sensitivity to toxicity: implications for immunotoxic biomonitoring. Mar Environ Res 50:465
Keller JM, McClellan-Green PD, Lee AM, Arendt MD, Maire PP, Segars AL, Whitaker JD, Keil DE, Peden-Adams MM (2005) Mitogen induced lymphocyte proliferation in Loggerhead Sea Turtles: comparison of methods and effects of gender, plasma testosterone concentration, and body condition on immunity. Vet Immunol Immunopathol 103:269–281
Kohanestani ZM, Hajimoradloo A, Ghorbani R, Yulghi S, Hoseini A, Molaee M (2013) Seasonal variations in haematological parameters of Alburnoise Eichwald in Zaringol Stream-Golestan Province Iran. World J Fish Marine Sci 5:121–126
Kondera E, Witeska M, Lugowska K (2019) Annual changes in hematological parameters of common carp juveniles under laboratory conditions. Animal Sci 58:143
Kumari J et al (2006) Seasonal variation in the innate immune parameters of the Asian catfish Clarias batrachus. Aquaculture 252:121–127
Lamkova K, Simkova A, Palikova M, Jurajda P, Lojek A (2007) Seasonal changes in immunocompetence and parasitism in chub (Leuciscus cephalus), a freshwater cyprinid fish. Parasitol Res 101:775–789
Leonardi MO, Klempau AE (2003) Artificial photoperiod influence on the immune system of juvenile rainbow trout (Oncorhynchus mykiss) in the Southern Hemisphere. Aquaculture 221:581–591
Lillehaug A, Lunestad BT, Grave K (2003) Epidemiology of bacterial diseases in Norwegian aquaculture e a description based on antibiotic prescription data for the ten-year period 1991–2000. Dis Aquat Org 53:115–125
Morgan AL, Thompson KD, Auchinachie NA, Migaud H (2008) The effect of seasonality on normal haematological and innate immune parameters of rainbow trout Oncorhynchus mykiss L. Fish Shellfish Immunol 25:791–799
Morgan, AL, Thompson, KD, Porter, MJR, Burrells, C and Bromage, NR, Effect of seasonality on the immune response of rainbow trout, In: European Association of Fish Pathologists Conference, Malta, 2003.
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
Ndong D, Chen YY, Lin YH, Vaseeharan B, Chen JC (2007) The immune response of tilapia Oreochromis mossambicus and its susceptibility to Streptococcus iniae under stress in low and high temperatures. Fish Shellfish Immunol 22(6):686–694
Nelson RJ, Demas GE (1997) Role of melatonin in mediating seasonal energetic and immunologic adaptations. Brain Res Bull 44:423–430
Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ (2002) Seasonal patterns of stress, immune function and disease. Cambridge University Press, Cambridge
Nelson RJ (1996) Interactions between motor commands and somatic perception in sensorimotor cortex. Curr Opin Neurobiol 6(6):801–810
Nelson RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25(4):187–192
Neumann NF, Barreda DR, Belosevic M (2000) Generation and functional analysis of distinct macrophage subpopulations from goldfish (Carassius auratus L.) kidney leukocyte cultures. Fish Shellfish Immunol 10(1):1–20
Nikoskelainen S, Bylund G, Lilius EM (2004) Effect of environmental temperature on rainbow trout (Oncorhynchus mykiss) innate immunity. Dev Comp Immunol 28(6):581–592
Ondrackova M, Reichard M, Jurajda P, Gelnar M (2004) Seasonal dynamics of Posthodiplostomum cuticola (Digenea, Diplostomatidae) metacercariae and parasite-enhanced growth of juvenile host fish. Parasitol Res 93:131–136
Pascoli F et al (2011) Seasonal effects on hematological and innate immune parameters in sea bass Dicentrarchus labrax. Fish Shellfish Immunol 31:1081–1087
Revie CW, Gettinby G, Treasurer JW, Rae GH, Clark N (2002) Temporal, environmental and management factors influencing the epidemiological patterns of sea lice (Lepeophtheirus salmonis) infestations on farmed Atlantic salmon (Salmo salar) in Scotland. Pest Manag Sci 58:576–584
Rieger AM, Hall BE, Barreda DR (2010) Macrophage activation differentially modulates particle binding, phagocytosis and downstream antimicrobial mechanisms. Dev Comp Immunol 34(11):1144–1159
Rowley AF, Hunt TC, Page M, Mainwaring G (1988) Fish. In: Rowley AF, Ratchife NA (eds) Vertebrate blood cells. Cambridge University Press, Cambridge, pp 19–127
Sahoo PK, Mukherjee SC, Sahoo SK (1998) Aeromonas hydrophila versus Edwardsiella tarda: a pathoanatomical study in Clarias batrachus. J Aquac 6:57–66
Sahoo PK, Kumari J, Mishra BK (2005) Non-specific immune responses in juveniles of Indian major carps. J Appl Ichthyol 21(2):151–155
Santos AA, Egami MI, Ranzani-Paiva MJT, Juliano Y (2009) Hematological parameters and phagocytic activity in fat snook (Centropomus parallelus): seasonal variation, sex and gonadal maturation. Aquaculture 296:359–366
Seriani R, De Souza Abessa DM, Pereira CDS, Kirschbaum AA, Assuncao A, Ranzani-Paiva MJT (2013) Influence of seasonality and pollution on the hematological parameters of the estuarine fish Centropomus parallelus. Braz J Oceanogr 61:105–111
Scott AL, Rogers WA, Klesius PH (1985) Chemiluminescence by peripheral blood phagocytes from channel catfish: Function of opson in and temperature. Dev Comp Immunol 9(2):241–250
Sohnle PG, Chusid MJ (1983) The effect of temperature on the chemiluminescence response of neutrophils from rainbow trout and man. J Comp Pathol 93(4):493–497
Srivastava S, Choudhary SK (2010) Effect of artificial photoperiod on the blood cell indices of the catfish Clarias Batrachus. J Stress Physiol BiOchem 6:22–32
Swain P, Mukherjee SC, Sahoo PK, Das BK, Pattnaik P, Murjani G, Nayak SK (2001) Dot-enzyme-linked immunosorbent assay (Dot-ELISA) for the diagnosis of Edwardsiella tarda infection in fish. Asian Fish Sci 14(1):89–94
Valero Y, Garc A, Cuesta A, Chaves-pozo E (2014) Seasonal variations of the humoral immune parameters of European sea bass (Dicentrarchus labrax L.). Fish Shellfish Immunol 39:185–187
Zapata AG, Varas A, Torroba M (1992) Seasonal variations in the immune system of lower vertebrates. Immunol Today 13:142–147
Acknowledgements
Funding (Grant Number F.30-96/2015 (BSR) dated 30/03/2015) from University Grants Commission, India to Dr. Manish Kumar Tripathi is thankfully acknowledged. The authors are grateful to www.meteoblue.com for providing weather data.
Funding
University Grants Commission—South Eastern Regional Office, F.30-96/2015 (BSR) dated 30/03/2015, Manish Kumar Tripathi.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Ethical approval
The research work on the fish Channa punctatus was approved by Institutional Animal Ethics Committee of the University (Approval Number: 994/GO/Re/S/06CPCSEA). All the experiments were carried out following the guidelines of the committee for the purpose of control and supervision of experiments on animals (CPCSEA), Ministry of Statistics & Programme Implementation, were abided by in maintenance of animals. All the authors have consented for the publication. The data pertaining to the results are available in the manuscript. Further queries may be addressed to the corresponding author. AKB and RKC have performed the experiment, AKP has done the Cosinor analysis of the data and MKT has designed the research, wrote the manuscript and analyzed the data.
Additional information
Communicated by H.V. Carey.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bhardwaj, A.K., Chandra, R.K., Pati, A.K. et al. Seasonal immune rhythm of leukocytes in the freshwater snakehead fish, Channa punctatus. J Comp Physiol B 192, 727–736 (2022). https://doi.org/10.1007/s00360-022-01460-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-022-01460-7