If you've been reading the tables in the previous pages and noticed that for some well-studied species, the percentage of lymphocytes and neutrophils differ greatly between studies, it's likely because of the stress levels of the animals being studied. The effects of stress on circulating white blood cell distributions has been experimentally studied in a number of animal species over several decades (reviewed in Davis et al. 2008). Below is a table that summarizes this literature (at least the papers the author knows of). In most of these studies, animals were injected with stress hormones - corticosterone, cortisol, dexamethasone or ACTH (which induces cort production) to mimic a stress response, though some involved manipulation of endogenous stress hormones, by way of physical restraint, transport, amputation (newts), temperature extremes, or simply capturing wild animals, which they perceive as stressful.
Last Updated Dec 30 2011
*Neutrophilia = increase in circulating neutrophils, Lymphopenia = decrease in circulating lymphocytes
** The Gross and Siegel (1983) paper is widely-recognized as the first publication on the subject of stress and leukocytes in birds, and deserves further comment here. Gross was from the College of Veterinary Medicine at Virginia Tech, while Siegel was at the USDA Southeast Poultry Research Lab in Athens, GA. Their paper described for the first time the tight relationship between stress hormones and H/L ratios in birds (chickens). They conducted a suite of experiments, stressing birds in various ways, then measuring H/L ratios. The most important experiment was also the simplest and most elegant; they mixed corticosterone into the chicken's feed for one day at varying doses and compared H/L ratios, and plasma levels of corticosterone at the end of the day. They found that birds fed corticosterone had a significantly higher H/L ratio than control birds, but more importantly there was a positive, linear relationship between the cort dose administered and mean H/L ratios per cage (each cage had 10 birds). Interestingly, the relationship between initial dose and plasma levels of corticosterone was much weaker (right graph).
Below are graphs of the data presented by Gross and Siegel (Table 2 in the paper). Each point is the mean of 10 birds.
The authors concluded that H/L ratios represent a reliable indicator of long-term stress, while plasma levels of corticosterone could be considered better-suited for indexing short-term stress.
Complete Reference List for Citations in Table
Aengwanich, W., and O. Chinrasri. 2003. Effect of dexamethasone on differential white blood cell counts and heterophil/lymphocyte ratio in Japanese quails (Coturnix coturnix japonica). Songklanakarin J. Sci. Technol. 25: 183-189.
Aguirre, A. A., G. H. Balazs, T. R. Spraker, and T. S. Gross. 1995. Adrenal and hematological responses to stress in juvenile green turtles (Chelonia mydas) with and without fibropapillomas. Physiological Zoology 68: 831-854.
Altan, O., A. Altan, M. Cabuk, and H. Bayraktar. 2000. Effects of heat stress on some blood parameters in broilers. Turkish Journal of Veterinary Animal Science 24: 145-148.
Anderson, B.H., D.L. Watson, and I.G. Colditz. 1999. The effect of dexamethasone on some immunological parameters in cattle. Veterinary Research Communications 23: 399-413.
Balabanova, L. V., D. V. Mikryakov, and V. R. Mikryakov. 2009. Response of common carp (Cyprinus carpio L.) leucocytes to hormone-induced stress. Inland Water Biology 2: 86-88.
Bedáňová, I., E. Voslářová, V. Večerek, V. Pištěková, and P. Chloupek. 2007. Haematological profile of broiler chickens under acute stress due to shackling. Acta Veterinaria Brno 76: 129-135.
Bennett, M.F. 1986. Stress and changes in the blood of newts, Notophthalmus viridescens, during early regeneration. Journal of Comparative Physiology A 159: 823-826.
Bennett, M.F., and J.K. Alspaugh. 1964. Some changes in the blood of frogs following administration of hydrocortisone. The Virginia Journal of Science 15: 76-79.
Bennett, M.F., and N.C. Newell. 1965. A further study of the effects of hydrocortisone on the blood of frogs. The Virginia Journal of Science 16: 128-130.
Bennett, M.F., and J.A. Harbottle. 1968. The effects of hydrocortisone on the blood of tadpoles and frogs, Rana catesbeiana. Biological Bulletin 135: 92-95.
Bennett, M.F., and A.O. Johnson. 1973. Osmotic stress, ACTH and the white blood cell picture in newts, Notophthalmus viridescens. Journal of Comparative Physiology A 82: 333-338.
Bennett, M.F., and L.E. Reap. 1978. Photoperiod, stress and the distribution of leukocytes in the peripheral blood of Notophthalmus viridescens. Journal of Comparative Physiology A 125: 205-207.
Bennett, M.F., and K.R. Daigle. 1983. Temperature, stress and the distribution of leukocytes in red-spotted newts, Notophthalmus viridescens. Journal of Comparative Physiology A 153: 81-83.
Bennett, M.F., C. Reed, and R.L. Roden. 1974. Circadian changes in responses of newts, Notophthalmus viridescens, to ACTH. Journal of Comparative Physiology A 89: 287-291.
Bennett, M.F., C.A. Gaudio, A.O. Johnson, and J.H. Spisso. 1972. Changes in the blood of newts, Notophthalmus viridescens, following administration of hydrocortisone. Journal of Comparative Physiology A 80: 233-237.
Bilandžič, N., M. Žurič, M. Lojkič, B. Šimič, D. Milić, and I. Barač. 2006. Cortisol and immune measures in boars exposed to three-day administration of exogenous adrenocorticotropic hormone. Veterinary Research Communications 30: 433-444.
Burguez, P.N., J. Ousey, R.S.G. Cash, and P.D. Rossdale. 1983. Changes in blood neutrophil and lymphocyte counts following administration of cortisol to horses and foals. Equine Veterinary Journal 15: 58-60.
Davis, A.K. and J.C. Maerz. 2010. Effects of exogenous corticosterone on circulating leukocytes of a salamander (Ambystoma talpoideum) with unusually abundant eosinophils. International Journal of Zoology. DOI:10.1155/2010/735937
Davis, A. K. & Maerz, J. C. 2011 Assessing stress levels of captive-reared amphibians with hematological data: implications for conservation initiatives. Journal of Herpetology 45, 40-44.
Dhabhar, F.S., A.H. Miller, M. Stein, B.S. McEwen, and R.L. Spencer. 1994. Diurnal and acute stress-induced changes in distribution of peripheral blood leukocyte subpopulations. Brain Behavior and Immunity 8: 66-79.
Frank, D., A. Gauthier, and R. Bergeron. 2006. Placebo-controlled double-blind clomipramine trial for the treatment of anxiety or fear in beagles during ground transport. Canadian Veterinary Journal-Revue Veterinaire Canadienne 47: 1102-1108.
Gross, W.B., and H.S. Siegel. 1983. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Diseases 27: 972-979.
Johansson-Sjobeck, M. L., et al. (1978). Hematological effects of cortisol in european eel, anguilla anguilla l. Comparative Biochemistry and Physiology a-Physiology, 60: 165-168.
Kock, R.A., S.R.O. Mihok, J. Wambua, J. Mwanzia, and K. Saigawa. 1999. Effects of translocation on hematologic parameters of free-ranging black rhinoceros (Diceros bicornis michaeli) in Kenya. Journal of Zoo and Wildlife Medicine 30: 389-396.
Kranendonk, G., H. Hopster, F. van Eerdenburg, K. van Reenen, M. Fillerup, J. de Groot, M. Korte, and M. Taverne. 2005. Evaluation of oral administration of cortisol as a model for prenatal stress in pregnant sows. American Journal of Veterinary Research 66: 780-790.
Lance, V.A., and R.M. Elsey. 1999. Plasma catecholamines and plasma corticosterone following restraint stress in juvenile alligators. Journal of Experimental Zoology 283: 559-565.
López-Olvera, J.R., I. Marco, J. Montané, E. Casas-Díaz, and S. Lavín. 2007. Effects of acepromazine on the stress response in Southern chamois (Rupicapra pyrenaica) captured by means of drive-nets. Canadian Journal of Veterinary Research 71: 41-51.
Maxwell, M.H. 1993. Avian blood leukocyte responses to stress. Worlds Poultry Science Journal 49: 34-43.
McFarlane, J.M., S.E. Curtis, J. Simon, and O.A. Izquierdo. 1989. Multiple concurrent stressors in chicks 2. Effects on hematologic, body composition, and pathologic traits. Poultry Science 68: 510-521.
McGlone, J.J., J.L. Salak, E.A. Lumpkin, R.I. Nicholson, M. Gibson, and R.L. Norman. 1993. Shipping stress and social-status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. Journal of Animal Science 71: 888-896.
McLaren, G. W., D. W. Macdonald, C. Georgiou, F. Mathews, C. Newman, and R. Mian. 2003. Leukocyte coping capacity: a novel technique for measuring the stress response in vertebrates. Experimental Physiology 88: 541-546.
Montane, J., I. Marco, J. Lopez-Olvera, D. Perpinan, X. Manteca, and S. Lavin. 2003. Effects of acepromazine on capture stress in roe deer (Capreolus capreolus). Journal of Wildlife Diseases 39: 375-386.
Morici, L.A., R.M. Elsey, and V.A. Lance. 1997. Effects of long-term corticosterone implants on growth and immune function in juvenile alligators, Alligator mississippiensis. Journal of Experimental Zoology 279: 156-162.
Morrow-Tesch, J.L., J.J. McGlone, and R.L. Norman. 1993. Consequences of restraint stress on natural killer cell activity, behavior, and hormone levels in Rhesus Macaques (Macaca mulatta). Psychoneuroendocrinology 18: 383-395.
Narayan, E., and J. M. Hero. 2011. Urinary corticosterone responses and haematological stress indicators in the endangered Fijian ground frog (Platymantis vitiana) during transportation and captivity. Australian Journal of Zoology 59: 79-85.
Reed, C., and M.F. Bennett. 1973. Circadian effects of hydrocortisone on the blood of the newt, Notophthalmus viridescens. Journal of Comparative Physiology A 86: 59-63.
Reidarson, T.H., and J.F. McBain. 1999. Hematologic, biochemical, and endocrine effects of dexamethasone on bottlenose dolphins (Tursiops truncatus). Journal of Zoo and Wildlife Medicine 30: 310-312.
Rossdale, P.D., P.N. Burguez, and R.S.G. Cash. 1982. Changes in blood neutrophil/lymphocyte ratio related to adrenocortical function in the horse. Equine Veterinary Journal 14: 293-298.
Salak-Johnson, J.L., J.J. McGlone, and R.L. Norman. 1996. In vivo glucocorticoid effects on procine natural killer cell activity and circulating leukocytes. Journal of Animal Science 74: 584-592.
Trottier, M.D., M.M. Newsted, L.E. King, and P.J. Fraker. 2008. Natural glucocorticoids induce expansion of all developmental stages of murine bone marrow granulocytes without inhibiting function. Proceedings of the National Academy of Sciences of the United States of America 105: 2028-2033.Zulkifli, I., M.T.C. Norma, C.H. Chong, and T.C. Loh. 1999. Heterophil to lymphocyte ratio and tonic immobility reactions to preslaughter handling in broiler chickens treated with acorbic acid. Poultry Science 79: 402-406.