Melatonin and corticosterone profiles under polar day in a seabird with sexually opposite activity-rhythms

Abstract

The 24 h geophysical light-dark cycle is the main organizer of daily rhythms, scheduling physiology and behavior. This cycle attenuates greatly during the continuous light of summer at polar latitudes, resulting in species-specific and even individual-specific patterns of behavioral rhythmicity, but the physiological mechanisms underlying this variation are poorly understood. To address this knowledge gap and to better understand the roles of the hormones melatonin and corticosterone in rhythmic behavior during polar day, we exploited the behavior of thick-billed murres (Uria lomvia), a charadriiform seabird with sexually opposite ('antiphase') activityrhythms on a 24 h cycle during the continuous light of polar summer. Melatonin concentration in the plasma of inactive males was unexpectedly high around midday and subsequently fell during a sudden decrease in light intensity as the colony became shaded. Corticosterone concentration in plasma did not vary with time of day or activity in either sex. While the reasons for these unusual patterns remain unclear, we propose that a flexible melatonin response and little diel variation of corticosterone may be adaptive in thick-billed murres, and perhaps other polar birds and mammals, by stabilizing glucocorticoids' role of modulating energy storage and mobilization across the diel cycle and facilitating the appropriate reaction to unexpected stimuli experienced across the diel cycle while attending the colony.

The relationship between daily behavior, hormones, and a color dimorphism in a seabird under natural continuous light

“…Blood was drawn from the brachial vein within 3 min after placing the noose around the bird's head, as capture induces corticosterone to elevate above baseline concentration after approximately 3 min due to corticosterone's role in the physiological response to unexpected noxious stimuli ( (Huffeldt et al, 2020;Romero and Reed, 2005); Supplementary Corticosterone Analyses)). Blood samples were centrifuged within 4 h of sampling.…”

“…Melatonin and glucocorticoids are broadly recognized as endogenous elements of the circadian system because they provide physiological signals of biological rhythms that track daily environmental cycles. Though exceptions exist (e.g., (Ashley et al, 2013;Huffeldt et al, 2020;Jessop et al, 2002), melatonin generally tracks the light-dark cycle by elevating during darkness and falling with increasing light intensity (Gwinner et al, 1997;Pandi-Perumal et al, 2006). In addition to its circadian functions, melatonin serves many other roles, including modulation of the immune system and protection of cellular functions (Pandi-Perumal et al, 2006).…”

“…During the extreme photic conditions in polar summer and winter, light intensity still cycles in the general environment, with the highest intensities during "daytime" (Ashley et al, 2013;Huffeldt et al, 2020). Melatonin can either track this diel change in light intensity (birds: (Ashley et al, 2013;Cockrem, 1991;Hau et al, 2002;Huffeldt et al, 2020;Silverin et al, 2009); mammals: (Griffiths et al, 1986;Stokkan and Reiter, 1994)) or be arrhythmic (birds: (Cockrem, 1991;Miché et al, 1991;Reierth et al, 1999;Steiger et al, 2013); mammals: (Eloranta et al, 1992)).…”

“…During the extreme photic conditions in polar summer and winter, light intensity still cycles in the general environment, with the highest intensities during "daytime" (Ashley et al, 2013;Huffeldt et al, 2020). Melatonin can either track this diel change in light intensity (birds: (Ashley et al, 2013;Cockrem, 1991;Hau et al, 2002;Huffeldt et al, 2020;Silverin et al, 2009); mammals: (Griffiths et al, 1986;Stokkan and Reiter, 1994)) or be arrhythmic (birds: (Cockrem, 1991;Miché et al, 1991;Reierth et al, 1999;Steiger et al, 2013); mammals: (Eloranta et al, 1992)). Although glucocorticoids are known to be under the control of the circadian system in mammals (Dickmeis, 2009;Kalsbeek et al, 2012;Son et al, 2011), most studies of glucocorticoids during polar summer describe little to no variation across the diel cycle (birds: (Huffeldt et al, 2020;Steenweg et al, 2015;Vleck and van Hook, 2002) [cf.…”

“…We then hypothesized that melatonin and corticosterone provide physiological signals of time of day despite continuous light. Our hypothesis is based on the observations that in common murres sex-stereotyped foraging and chick-provisioning depends on time of day (Thaxter et al, 2009), that their colony is subjected to diel changes in ambient light intensity (e.g., (Huffeldt et al, 2020)), and that melatonin rises in response to slight changes in light intensity in other bird species (Kumar et al, 2000).…”