The relationship between daily behavior, hormones, and a color dimorphism in a seabird under natural continuous light
Introduction
The cycling between the dark of night and the light of day regulates many ecological interactions and is a major selective force for optimizing behavior and physiology (Kronfeld-Schor and Dayan, 2003; Pittendrigh, 1993; Schwartz and Daan, 2017). This selection has resulted in anticipatory mechanisms in most organisms in the form of biological rhythms, such as circadian rhythms (Pittendrigh, 1993; Schwartz and Daan, 2017). Above the polar circles, however, the 24-h light-dark cycle is greatly attenuated during summer and winter, and investigating the behavior and physiology of polar residents during these seasons is paramount for understanding which mechanisms are the most important for tracking the diel cycle in the wild.
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). Diel patterns of glucocorticoids track circadian rhythms and food intake (Dickmeis, 2009; Kalsbeek et al., 2012; Quillfeldt et al., 2007; Son et al., 2011; Woodley et al., 2003) and commonly link to activity (Jessop et al., 2002; Landys et al., 2006). Glucocorticoids also provide important immunomodulatory and energetic functions, among others (Landys et al., 2006; Sapolsky et al., 2000). In birds, the primary glucocorticoid is corticosterone. The diel pattern of corticosterone in birds is low during the active phase and high during the inactive phase (Breuner et al., 1999; Landys et al., 2006; Romero and Remage-Healey, 2000; Tarlow et al., 2003). Thus, melatonin and corticosterone can act as redundant physiological signals that entrain internal rhythms to environmental rhythms, which, in the example of a diurnal bird, may ultimately be dictated by obtaining food during the day and conserving energy and avoiding predators at night.
During the extreme photic conditions in polar summer and winter, light intensity still cycles in the general environment, with the highest intensities during “daytime” when the angle of the sun above the horizon (“sun angle”) is widest (Ashley et al., 2013; Gabler et al., 2008; 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. Scheiber et al., 2017; mammals: Barrell and Montgomery, 1989). To gain better insight into the functional role of melatonin and corticosterone during the continuous light of polar summer, we studied these hormones in a seabird, the common murre (Uria aalge).
The common murre is a colonial Charadriiform whose range extends from approximately 37°N to well above the northern polar circle (Gaston and Jones, 1998). In common murres, ecological interactions and colony attendance can depend on time of day. Colony attendance by common murres generally follows a diel pattern (Birkhead, 1978; Thayer et al., 1999; Zador and Piatt, 1999), with most foraging occurring outside of nighttime (Regular et al., 2010). Females are more likely to incubate their egg overnight and males are more likely to incubate their egg during midday (Wanless and Harris, 1986), while the amount of time spent attending the colony not incubating or brooding depends on foraging conditions (Zador and Piatt, 1999). Males and females provision their chick diurnally at subpolar latitude, with males spending more time away from the chick during night hours (Thaxter et al., 2009), and murres will also forage with a crepuscular pattern at some colonies (Regular et al., 2010). Above the polar circle at Hornøya (Norway), the same colony where our study was conducted, diel provisioning of the chick is specific to certain times of day in each sex (Holmøy, 2019). Thick-billed murres (U. lomvia), the sister species to common murres, maintain robust and sex-stereotyped rhythms of incubating and brooding under both subpolar and polar conditions (Elliott et al., 2010; Huffeldt and Merkel, 2016; Paredes et al., 2006). All this considered, we expect that common murres keep time during the polar summer to schedule their behavior and physiology according to the diel cycle.
Despite the several sex-stereotyped behaviors described in common and thick-billed murres, lack of information on colony attendance of the sexes during polar day for common murres required us to first test the assumption that they have a sex-stereotyped, diel pattern in their incubating and brooding behavior during polar summer. We predicted that males attending the colony would be incubating their egg or brooding their chick (“on-duty”) during “daytime” and females attending the colony would be on-duty during “nighttime” (Thaxter et al., 2009; Wanless and Harris, 1986).
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). We predicted that circulating melatonin will be elevated in birds attending the colony during “night” hours compared to “day” hours (e.g., Ashley et al., 2013; Hau et al., 2002; Silverin et al., 2009) and that corticosterone will have a typical diel pattern for a diurnal bird, with the lowest concentration during daytime (Scheiber et al., 2017). The alternative hypotheses were that in common murres the continuous light abolishes, directly or indirectly, any diel variation in melatonin, corticosterone, or both.
Furthermore, in the Atlantic Ocean, the common murre displays a plumage color dimorphism, with a bridled morph having a white ring around the eye that extends down the auricular grove and an unbridled morph with a completely dark chocolate-brown head. The frequency of the dimorphism and survival of the two morphs are correlated with sea surface temperature, suggesting that bridled and unbridled birds have different thermal adaptations (Birkhead, 1984; Reiertsen et al., 2012). The dimorphism is associated also with differences in parental investment, with mixed-morph pairs raising heavier chicks compared to single-morph pairs (Kristensen et al., 2014), and morph is linked to genes involved in metabolism and circadian rhythms (Tigano et al., 2018). Given that the plumage color dimorphism in common murres is associated with these different traits and that plumage differences can associate with distinct physiology and behavior in birds (Almasi et al., 2008; Ducrest et al., 2008; Scriba et al., 2017), we also tested whether morph could predict colony attendance and concentrations of melatonin and corticosterone.
Section snippets
Sample collection
One-hundred adult breeding common murres (N = 55 females, 45 males) were captured on Hornøya, Norway (70.39°N, 31.15°E) from the 13th to the 26th of June and from the 1st to the 10th of July 2014. The captured murres were mainly incubating their egg in June (32 of 48 murres; 2 murres nest content unknown) and brooding their chick in July (45 of 50 murres). The study was conducted under the continuous light of polar summer: the sun never went below the horizon (range of sun angle1
Colony attendance behavior
Information on morph was not available for one individual, which was excluded from further analysis (N = 99). Morph was the best predictor of whether a bird attending the colony was on- or off-duty (Table 1), and, given our data, the model including only morph was 2.29 times more likely to predict whether a bird attending the colony was on- or off-duty than the null model (Table 1a). Unbridled individuals were on-duty more often than bridled individuals (Fig. 1). The interaction between sex and
Discussion
Contrary to expectations, the common murres did not schedule their incubating and brooding (on-duty attendance) by time of day and sex, highlighting the importance of testing assumptions based on other populations or species. During the continuous light of polar summer, common murres maintained diel variation in melatonin (Fig. 2b; Table 2), supporting our hypothesis that common murres can use melatonin to signal time of day physiologically. Corticosterone, on the other hand, only had a
Conclusions
We found that common murres maintain a diel profile in melatonin under the continuous light of polar day and that they probably modulate their melatonin concentration behaviorally. Additionally, we found that circulating corticosterone is unlikely to signal time of day physiologically, which adds to the mounting evidence that glucocorticoids either play a minor role, require a very low-amplitude rhythm, or require modulation by other mechanisms to satisfy their physiological duties at polar
CRediT authorship contribution statement
N.P.H. conceived the study, conducted fieldwork under the supervision of K.E.E. and T.K.R., conducted statistical analyses, and drafted the manuscript with input from A.T. W.G. assayed melatonin. S.J.-E. assayed corticosterone. T.M. performed genetic sex-identification. All authors reviewed and revised the manuscript critically.
Declaration of competing interest
None.
Acknowledgements
We thank Manuel Ballesteros for assistance in the field; Vigdis Edvardsen for assistance with DNA extractions and the molecular identification of sex; Monika Trappschuh for assistance with the melatonin assay; and Juanita Olano Marin for assistance with the corticosterone assay. We also thank the anonymous referees for comments that improved the manuscript.
Funding
Field- and lab-work were partially supported by Vecellio Grants for Graduate Research, Wake Forest University, USA to N.P.H. and SEAPOP (seapop.no) to K.E.E. and T.K.R. The funding sources did not have any role in study design; in the collection, analysis, and interpretation of data; in the writing of the manuscript; or in the decision to submit the article for publication.
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