Abstract
Animals in the temperate zones face seasonal variations in environments and hence their immune responses change seasonally. In the current study, seasonal changes in hematological parameters and cytokines in striped hamsters (Cricetulus barabensis) were examined to test the winter immunoenhancement hypothesis, which states that immune function tends to increase in fall and winter compared with other seasons. Male and female hamsters were captured from the wild in the fall and winter of 2014 and in the spring and summer of 2015. Maximum body mass in both sexes and relative fatness in female hamsters occurred in the summer, indicating that body condition was the best during this season. All hematological parameters were not different between male and female hamsters, and were also not affected by the interaction of season and sex except neutrophil granulocytes (GRAN). Red blood cells (RBC) and haematocrit (PCV) were higher in the fall and winter, and hemoglobin concentration (HGB) was the highest in winter in hamsters compared with the spring and summer, implying that their oxygen-carrying capacity and oxygen affinity of the blood increased during these seasons. Compared with other seasons, the number of white blood cells (WBC) was higher in winter than in summer, intermediate granulocytes (MID), the percent of MID (MID%), GRAN and the percent of GRAN (GRAN%) were the highest in winter, which all supported the winter immunoenhancement hypothesis. However, the count of lymphocytes (LYMF) was the highest in spring, being inconsistent with this hypothesis. IL-2 levels, but not TNF-α, were influenced by seasons, sex and their interaction in hamsters. Regardless of sex, IL-4 titres were higher in spring and summer than in fall and winter in hamsters. INF-γ titres in male hamsters did not differ between the spring and summer, while its titres in female hamsters was lower in spring in contrast with winter and summer. Higher IL-2 and IL-4 levels during the breeding seasons might be crucial in controlling the increased possibilities of infections in these seasons. In summary, season and sex had disparate effects on different hematological profiles and the levels of cytokines in hamsters.
Similar content being viewed by others
References
Abdelatif AM, Ibrahim YM, Hassan MY (2009) Seasonal variation in erythrocytic and leukocytic indices and serum proteins of female Nubian goats. Middle East J Sci Res 4:168–174
Ahima RS, Flier JS (2000) Adipose tissue as an endocrine organ. Trends Endocrinol Metab 11:327–332
Al-Busaidi R, Johnson EH, Mahgoub O (2008) Seasonal variations of phagocytic response, immunoglobulin G (IgG) and plasma cortisol levels in Dhofari goats. Small Rumin Res 79:118–123
Aras M, Bayir A, Sirkecioglu AN, Polat H, Bayir M (2010) Seasonal variations in serum lipids, lipoproteins and some haematological parameters of chub (Leuciscus cephalus). Ital J Anim Sci 7:439–448
Babamale OA, Abdulkareem AO, Opeyemi OA, Ugbomoiko US (2017) Alterations in T-helper cell type 1 and blood cell parameters in malaria-infected patients. Egypt J Basic Appl Sci 4:185–189
Bilbo SD, Dhabhar FS, Viswanathan K, Saul A, Yellon SM, Nelson RJ (2002) Short day lengths augment stress-induced leukocyte trafficking and stress-induced enhancement of skin immune function. Proc Natl Acad Sci 99:4067–4072
Brainard GC, Knobler RI, Podolin PL, Lavasa M, Lubin FD (1987) Neuroimmunology: modulation of the hamster immune system by photoperiod. Life Sci 40:1319–1326
Bubenik GA, Brownlee L (1987) Assessing health of male white-tailed deer by white blood cell counts. J Wildl Manag 51:57–58
Bush M, Smith EE, Custer RS (1981) Hematology and serum chemistry values for captive Dorcas gazelles: variations with sex, age and health status. J Wildl Dis 17:135–143
Calder PC, Kew S (2002) The immune system: a target for functional foods? Br J Nutr 88:S165–S176
Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ (2005) A review of the multiple actions of melatonin on the immune system. Endocrine 27:189–200
Casella S, Scianò S, Zumbo A, Monteverde V, Fazio F, Piccione G (2013) Effect of seasonal variations in mediterranean area on haematological profile in dairy cow. Comp Clin Pathol 22:691–695
Chaudhary UB (2015) Seasonal variations in physio-biochemical profiles of indian goats in the paradigm of hot and cold climate. Biol Rhythm Res 46:221–236
Chi QS, Wang DH (2011) Thermal physiology and energetics in male desert hamsters (Phodopus roborovskii) during cold acclimation. J Comp Physiol B 181:91–103
Demas GE (2004) The energetics of immunity: a neuroendocrine link between energy balance and immune function. Horm Behav 45:173–180
Demas GE, Nelson RJ (1998) Short-day enhancement of immune function is independent of steroid hormones in deer mice (Peromyscus maniculatus). J Comp Physiol B 168:419–426
Dobrowolska A, Adamczewska-Andrzejewska KA (1991) Seasonal and long term changes in serum gamma globulin levels in comparing the physiology and population density of the common vole, Microtus arvalis Pall. 1779. J Interdis Cycle Res 22:1–19
Dobrowolska A, Rewkiewicz-Dziarska A, Szarska I, Gill J (1974) Seasonal changes in haematological parameters, level of serum p roteinsand glycop roteins, activity of the thyroid gland, sup rarenal and kidneys in the common vole (Microtus arvalis Pall.). J Interdis Cycle Res 5:347–354
Drazen DL, Kriegsfeld LJ, Schneider JE, Nelson RJ (2000) Leptin, but not immune function, is linked to reproductive responsiveness to photoperiod. Am J Physiol Regul Integr Comp Physiol 278:R1401–R1407
Drazen DL, Jasnow AM, Nelson RJ, Demas GE (2002) Exposure to short days, but not short-term melatonin, enhances humoral immunity of male Syrian hamsters (Mesocricetus auratus). J Pineal Res 33:118–124
Dudzinski ML, Hesterman ER, Mykytowicz R (1962) Some haematological data from an experimental colony of rabbits, Oryctolagus cuniculus L. Aust J Zool 10:587–596
Fair J, Whitaker S, Pearson B (2007) Sources of variation in haematocrit in birds. Ibis 149:535–552
Fazio F, Giangrosso G, Marafioti S, Zanghì E, Arfuso F, Piccione G (2016) Blood haemogram in Ovis aries and Capra hyrcus: effect of storage time. Can J Anim Sci 96:32–36
Flier JS (1998) Lowered leptin slims immune response. Nat Med 4:1124–1125
Franco M, Contreras C, Nespolo RF (2013) Profound changes in blood parameters during torpor in a South American marsupial. Com Biochem Physiol A 166:338–342
Franco M, Contreras C, Place NJ, Bozinovic F, Nespolo RF (2017) Leptin levels, seasonality and thermal acclimation in the Microbiotherid marsupial Dromiciops gliroides: does photoperiod play a role? Comp Biochem Physiol A 203:233–240
Ghosh S, Singh AK, Haldar C (2014) Seasonal modulation of immunity by melatonin and gonadal steroids in a short day breeder goat Capra hircus. Theriogenology 82:1121–1130
Goetz FW, Planas JV, MacKenzie S (2004) Tumor necrosis factors. Dev Comp Immunol 28:487–497
Habibu B, Kawu M, Makun H, Aluwong T, Yaqub L, Dzenda T, Buhari H (2017) Influences of breed, sex and age on seasonal changes in haematological variables of tropical goat kids. Arch Anim Breed 60:33–42
Hangalapura BN, Kaiser MG, Poel JJ, Parmentier HK, Lamont SJ (2006) Cold stress equally enhances in vivo pro-inflammatory cytokine gene expression in chicken lines divergently selected for antibody responses. Dev Comp Immunol 30:500–511
Harikrishnan R, Kim MC, Kim JS, Balasundaram C, Heo MS (2011) Protective effect of herbal and probiotics enriched diet on haematological and immunity status of Oplegnathus fasciatus (Temminck & Schlegel) against Edwardsiella tarda. Fish Shell Immunol 30:886–893
Hotchkiss AK, Nelson RJ (2002) Melatonin and immune function: hype or hypothesis? Crit Rev Immunol 22:351–371
Kim JH, Kang JC (2016) Changes in hematological parameters, plasma cortisol, and acetylcholinesterase of juvenile rockfish, Sebastes schlegelii supplemented with the dietary ascorbic acid. Aquac Rep 4:80–85
Krams I, Cirule D, Krama T, Vrublevska J (2011) Extremely low ambient temperature affects haematological parameters and body condition in wintering Great Tits (Parus major). J Ornithol 152:889–895
Krause JS, Németh Z, Pérez JH, Chmura HE, Ramenofsky M, Wingfield JC (2016) Annual hematocrit profiles in two subspecies of white-crowned sparrow: a migrant and a resident comparison. Physiol Biochem Zool 89:51–60
Krishnamoorthy RV, Shakunthala N (1974) Increased RBC count and pulmonary respiration in cold-adapted frogs. J Exp Biol 61:285–291
Lam QLK, Lu LW (2007) Role of leptin in immunity. Cell Mol Immunol 4:1–13
Li XS, Wang DH (2005) Regulation of body weight and thermogenesis in seasonally acclimatized Brandt’s voles (Microtus brandti). Horm Behav 48:321–328
Li QF, Sun RY, Huang CX, Wang ZK, Liu XT, Hou JJ, Liu JS, Cai LQ, Li N, Zhang SZ, Wang Y (2001) Cold adaptive thermogenesis in small mammals from different geographical zones of China. Comp Biochem Physiol A 129:949–961
Liu JS, Yang M, Sun RY, Wang DH (2009) Adaptive thermogenesis in Brandt’s vole (Lasiopodomys brandti) during cold and warm acclimation. J Therm Biol 34:60–69
Lochmiller RL, Vesty MR, McMurray ST (1994) Temporal variation in humoral and cell-mediated immune responses in a Sigmodon hispidus population. Ecology 75:236–245
Lombardi G, Ricci C, Banfi G (2011) Effect of winter swimming on haematological parameters. Biochem Med 21:71–78
Lord GM, Matarese G, Howard JK, Baker RJ, Bloom SR, Lechler RI (1998) Leptin modulates the T-cell immune response and reverses starvation-induced immunosuppression. Nature 394:897–901
Lu HQ, Li YC, Zhang XD (1987) Age determination, age structure and population dynamics of striped hamster. Acta Theriol Sin 7:28–34 (in Chinese with English subtract)
Mann DR, Akinbami MA, Gould KG, Ansari AA (2000) Seasonal variations in cytokine expression and cell-mediated immunity in male rhesus monkeys. Cell Immunol 200:105–115
Marketon JIW, Glaser R (2008) Stress hormones and immune function. Cell Immunol 252:16–26
Martin LB, Weil ZM, Nelson RJ (2007) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Philol Trans R Soc B 363:1–19
McMurry ST, Lochmiller RL, McBee K, Qualls JCW (1999) Indicators of immunotoxicity in populations of cotton rats (Sigmodon hispidus) inhabiting an abandoned oil refinery. Ecotoxicol Environ Saf 42:223–235
Monroy FP, Banerjee SK, Duong T, Aviles H (1999) Cold stress-induced modulation of inflammatory responses and intracerebral cytokine mRNA expression in acute murine toxoplasmosis. J Parasitol 85:878–886
Moshkin MP, Dobrotvorsky AK, Mak VV, Panov VV, Dobrotvorskaya EA (1998) Variability of immune response to heterologous erythrocytes during population cycles of red (Clethrionomys rutilus) and bank (C. glareolus) voles. Oikos 82:131–138
Myrianthefs P, Karatzas S, Venetsanou K, Grouzi E, Evagelopoulou P, Boutzouka E, Fildissis G, Spiliotopoulou I, Baltopoulos G (2003) Seasonal variation in whole blood cytokine production after LPS stimulation in normal individuals. Cytokine 24:286–292
Nelson RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25:187–192
Nelson RJ, Demas GE (1996) Seasonal changes in immune function. Q Rev Biol 71:511–548
Newson J (1962) Seasonal differences in reticulocyte count, hemoglobin levels and spleen weight in wild voles. Br J Haematol 8:296–302
Norte AC, Ramos JA, Sousa JP, Sheldon BC (2009) Variation of adult Great Tit Parus major body condition and blood parameters in relation to sex, age, year and season. J Ornithol 150:651–660
Owens IPF, Wilson K (1999) Immunocompetence: a neglected life history trait or conspicuous red herring? Trends Ecol Evol 14:170–172
Palenske NM, Saunders DK (2003) Blood viscosity and hematology of American bullfrogs (Rana catesbeiana) at low temperature. J Therm Biol 28:271–277
Pascoli F, Lanzano GS, Negrato E, Poltronieri C, Trocino A, Radaelli G (2011) Seasonal effects on hematological and innate immune parameters in sea bass Dicentrarchus labrax. Fish Shell Immunol 31:1081–1087
Prendergast BJ, Kampf-Lassin A, Yee JR, Galang J, McMaster N, Kay LM (2007) Winter day lengths enhance T lymphocyte phenotypes, inhibit cytokine responses, and attenuate behavioral symptoms of infection in laboratory rats. Brain Behav Immun 21:1096–1108
Pyter LM, Samuelsson AR, Quan N, Nelson RJ (2005) Photoperiod alters hypothalamic cytokine gene expression and sickness responses following immune challenge in female Siberian hamsters (Phodopus sungorus). Neuroscience 131:779–784
Quispe R, Villavicencio CP, Addis E, Wingfield JC, Vasquez RA (2014) Seasonal variations of basal cortisol and high stress response to captivity in Octodon degus, a mammalian model species. Gen Comp Endocr 197:65–72
Rabinovitch A, Suarez-Pinzon WL, Sorensen O, Rajotte RV, Power RF (1997) TNF-α down-regulates type 1 cytokines and prolongs survival of syngeneic islet grafts in nonobese diabetic mice. J Immunol 159(6298):6392
Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89
Schradin C (2008) Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent. Horm Behav 53:573–579
Sealandje RA (1966) Seasonal variations in hemoglobin and hematocrit values in the northern red-backed mouse, Clethrionomys rutilus dawsoni (Merriam), in interior Alaska. Can J Zool 44:213–224
Shapira L, Houri-Haddad Y, Frolov I, Halabi A, Ben-Nathan D (1999) The effect of stress on the inflammatory response to Porphyromonas gingivalis in a mouse subcutaneous chamber model. J Periodontol 70:289–293
Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317–321
Sinclair JA, Lochmiller RL (2000) The winter immunoenhancement hypothesis: associations among immunity, density, and survival in Prairie vole (Microtus ochrogaster) populations. Can J Zool 78:254–264
Song ZG, Wang DH (2003) Metabolism and thermoregulation in the striped hamster Cricetulus barabensis. J Therm Biol 28:509–514
Steiner AA, Romanovsky AA (2007) Leptin: at the crossroads of energy balance and systemic inflammation. Prog Lipid Res 46:89–107
Stevenson TJ, Prendergast BJ (2015) Photoperiodic time measurement and seasonal immunological plasticity. Front Neuroendocr 37:76–88
Valentine GL, Kirkpatrick RL (1970) Seasonal changes in reproductive and related organs in the pine vole, Microtus pinetorum, in south-western Virginia. J Mammal 51:553–560
Walton JC, Weil ZM, Nelson RJ (2011) Influence of photoperiod on hormones, behavior, and immune function. Front Neuroendocr 32:303–319
Wang JM, Zhang YM, Wang DH (2006) Seasonal thermogenesis and body mass regulation in plateau pikas (Ochotona curzoniae). Oecologia 149:373–382
Weber DK, Danielson K, Wright S, Foley JE (2002) Hematology and serum biochemistry values of dusky-footed wood rat (Neotoma fuscipes). J Wildl Dis 38:576–582
Weil ZM, Borniger JC, Cisse YM, Salloum BA, Nelson RJ (2015) Neuroendocrine control of photoperiodic changes in immune function. Front Neuroendocr 37:108–118
Wells RMG, Jones A, Clout MN, Sarre SD, Anderson RK (2000) Seasonal effects on the haematology and blood chemistry of wild brushtail possums, Trichosurus vulpecula (Marsupialia: Phalangeridae) in New Zealand. Comp Haematol Int 10:68–73
Wen JC, Prendergast BJ (2007) Photoperiodic regulation of behavioral responsiveness to proinflammatory cytokines. Physiol Behav 90:717–725
Xu DL, Hu XK (2017) Photoperiod and temperature differently affect immune function in striped hamsters (Cricetulus barabensis). Comp Biochem Physiol A 204:211–218
Xu DL, Hu XK, Tian YF (2017) Effect of temperature and food restriction on immune function in striped hamsters (Cricetulus barabensis). J Exp Biol 220:2187–2195
Xu DL, Hu XK, Tian YF (2018) Seasonal variations in cellular and humoral immunity in male striped hamsters (Cricetulus barabensis). Biol Open 7:1–8
Yang YP, Zhou YL, Zhang PL, Hou XX, Dong WH (1996) A study on the growth and development of striped hamster. Acta Theriol Sin. 16:309–311
Yellon SM (2007) Melatonin mediates photoperiod control of endocrine adaptations and humoral immunity in male Siberian hamsters. J Pineal Res 43:109–114
Yellon SM, Fagoaga OR, Nehlsen-Cannarella SL (1999) Influence of photoperiod on immune cell functions in the male Siberian hamster. Am J Physiol 276:R97–R102
Zhang ZB, Wang ZW (1998) Ecology and management of rodent pests in agriculture. Ocean Publishing House, Beijing
Zhang ZQ, Wang DH (2006) Seasonal changes in immune function, body fat mass and organ mass in Mongolian gerbils (Meriones unguiculatus). Acta Theriol Sin 26:338–345 (in Chinese with English Summary)
Zhang ZQ, Wang DH (2007) Seasonal changes in thermogenesis and body mass in wild Mongolia gerbils (Meriones unguiculatus). Comp Biochem Physiol A 148:346–353
Zhang Z, Chen B, Yuan L, Niu C (2015) Acute cold stress improved the transcription of pro-inflammatory cytokines of Chinese soft-shelled turtle against Aeromonas hydrophila. Dev Comp Immunol 49:127–137
Zhao ZJ (2011) Serum leptin, energy budget and thermogenesis in striped hamsters exposed to consecutive decrease in ambient temperatures. Physiol Biochem Zool 84:560–572
Zhao ZJ, Cao J, Meng XL, Li YB (2010) Seasonal variations in metabolism and thermoregulation in the striped hamster (Cricetulus barabensis). J Therm Biol 35:52–57
Zhao ZJ, Chi QS, Liu QS, Zheng WH, Liu JS, Wang DH (2014) The shift of thermoneutral zone in striped hamster acclimated to different temperatures. PLoS One 9:e84396
Zhou YL, Hou XX, Dong WH, Yang YP (1992) A study of the relative fatness of striped hamster. Acta Theriol Sin 12:207–212
Zimmerman LM, Bowden RM, Vogel LA (2014) A vertebrate cytokine primer for eco-immunologists. Funct Ecol 28:1061–1073
Zou J, Secombes CJ (2011) Teleost fish interferons and their role in immunity. Dev Comp Immunol 35:1376–1387
Acknowledgements
We are grateful for the detailed comments and suggestions provided by the anonymous reviewers. The present study was supported by grants from the National Natural Science Foundation of China (31770444; 31370427) and the State Key Laboratory of Integrated Management of Pest Insects and Rodents (Grant no. IPM1906).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Noga Kronfeld-Schor.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Xu, DL., Hu, XK. Season and sex have different effects on hematology and cytokines in striped hamsters (Cricetulus barabensis). J Comp Physiol B 190, 87–100 (2020). https://doi.org/10.1007/s00360-019-01246-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-019-01246-4