The use of leukocyte profiles to measure stress in vertebrates: a review for ecologists

Abstract

Summary 1.A growing number of ecologists are turning to the enumeration of white blood cells from blood smears (leukocyte profiles) to assess stress in animals. There has been some inconsistency and controversy in the ecological literature, however, regarding their interpretation. The inconsistencies may stem partly from a lack of information regarding how stress affects leukocytes in different taxa, and partly from a failure on the part of researchers in one discipline to consult potentially informative literature from another. 2. Here, we seek to address both issues by reviewing the literature on the leukocyte response to stress, spanning the taxa of mammals (including humans), birds, amphibians, reptiles and fish. 3. We show that much of the early literature points to a close link between leukocyte profiles and glucocorticoid levels. Specifically, these hormones act to increase the number and percentage of neutrophils (heterophils in birds and reptiles), while decreasing the number and percentage of lymphocytes. This phenomenon is seen in all five vertebrate taxa in response to either natural stressors or exogenous administration of stress hormones. For the ecologist, therefore, high ratios of heterophils or neutrophils to lymphocytes ('H : L' or 'N : L' ratios) in blood samples reliably indicate high glucocorticoid levels. Furthermore, this close relationship between stress hormones and N : L or H : L ratios needs to be highlighted more prominently in haematological assessments of stress, as it aids the interpretation of results. 4. As with hormone assays, there are challenges to overcome in the use of leukocytes profiles to assess levels of stress; however, there are also advantages to this approach, and we outline each. Given the universal and consistent nature of the haematological response to stress, plus the overwhelming evidence from the veterinary, biomedical and ecological literature reviewed here, we conclude that this method can provide a reliable assessment of stress in all vertebrate taxa.

Spatial variation in haemoglobin concentration of nestling Blue Tits (Cyanistes caeruleus): a long-term perspective

“…Bańbura et al (2013) examined the heterophil-to-lymphocyte ratio (H/L) in Blue Tits at both our study areas and found that nestlings had on average higher level of the H/L in the urban parkland study area than in the forest study area. The H/L is considered as a reliable indicator of chronic stress reaction in birds (Gross and Siegel 1983;Ots et al 1998;Moreno et al 2002;Davis et al 2008).…”

Opposing selective pressures may act on the colony size in a waterbird species

“…Therefore, H/L ratio is known to increase in response to parasite load, infectious diseases, starvation or physiological disturbance (Gross and Siegel 1983), and it was suggested to be a more reliable stress indicator in birds than individual cell numbers or corticosterone level (Maxwell 1993). High validity of H/L ratio as a proxy of physiological stress in vertebrates has been recently confirmed with a comparative analysis (Davis et al 2008).…”

“…We predicted that under such conditions, large colony size was likely to promote better brood survival by providing reduced predation risk, although these benefits might be accrued at the expense of poorer chick condition (from increased parasitism or social stress). To test the latter prediction, we evaluated growth rates of chicks, as well as their physiological condition expressed with blood hemoglobin concentrations and heterophil/lymphocyte (H/L) ratios, which are considered reliable indicators of physiological stress in birds (Davis et al 2008). In order to confirm whether any potential differences in offspring condition were not genetic, but could be directly attributed to different rearing conditions experienced in the colonies of varying size, a cross-fostering experiment was also conducted.…”

Comparative leukocyte morphometric analysis between endemic Anurans from Brazil and the invasive species Lithobates catesbeianus

“…The hematopoietic tissue is particularly sensitive to environmental changes and is an important indicator of physiological response and stress agents, which are quickly reflected in hematologic parameters (ALLENDER; FRY, 2008;DAVIS;MANEY;MAERZ , 2008;SHUTLER;MARCOGLIESE, 2011). Hematologic and biochemical evaluation of amphibians is of great clinical importance, and provides valuable diagnostic information and understanding of the pathogenesis of diseases, their progression, and response to therapy (SCHMID-SCHÖNBEIN et al, 1980;ALLENDER;FRY, 2008;DAVIS;DURSO, 2009;YOUNG et al, 2012).…”