Carotenoids, Birdsong and Oxidative Status: Administration of Dietary Lutein Is Associated with an Increase in Song Rate and Circulating Antioxidants (Albumin and Cholesterol) and a Decrease in Oxidative Damage

Abstract

Despite the appealing hypothesis that carotenoid-based colouration signals oxidative status, evidence supporting the antioxidant function of these pigments is scarce. Recent studies have shown that lutein, the most common carotenoid used by birds, can enhance the expression of non-visual traits, such as birdsong. Nevertheless, the underlying physiological mechanisms remain unclear. In this study we hypothesized that male European starlings (Sturnus vulgaris) fed extra lutein increase their song rate as a consequence of an improved oxidative status. Although birdsong may be especially sensitive to the redox status, this has, to the best of our knowledge, never been tested. Together with the determination of circulating oxidative damage (ROMs, reactive oxygen metabolites), we quantified uric acid, albumin, total proteins, cholesterol, and testosterone, which are physiological parameters potentially sensitive to oxidation and/or related to both carotenoid functions and birdsong expression. We found that the birds fed extra lutein sang more frequently than control birds and showed an increase of albumin and cholesterol together with a decrease of oxidative damage. Moreover, we could show that song rate was associated with high levels of albumin and cholesterol and low levels of oxidative damage, independently from testosterone levels. Our study shows for the first time that song rate honestly signals the oxidative status of males and that dietary lutein is associated with the circulation of albumin and cholesterol in birds, providing a novel insight to the theoretical framework related to the honest signalling of carotenoid-based traits.

Honest Signaling and Oxidative Stress: The Special Case of Avian Acoustic Communication

“…In the last decades several studies have investigated the role of the redox state in mediating the expression of visual secondary sexual traits (Alonso-Alvarez et al, 2007;McGraw, 2008;Svensson and Wong, 2011;Garratt and Brooks, 2012;Hill and Johnson, 2012;Simons et al, 2012), but until now only few of them focused on birdsong (Van Hout et al, 2011;Casagrande et al, 2014Casagrande et al, , 2015Baldo et al, 2015;Costantini et al, 2015; Table 1). Studies carried out in captive male European starlings (Sturnus vulgaris) to investigate whether song activity can honestly convey information about the redox state, reported that the administration of dietary lutein through the diet was associated with an increase in song rate (Van Hout et al, 2011;Casagrande et al, 2014Casagrande et al, , 2015.…”

“…Studies carried out in captive male European starlings (Sturnus vulgaris) to investigate whether song activity can honestly convey information about the redox state, reported that the administration of dietary lutein through the diet was associated with an increase in song rate (Van Hout et al, 2011;Casagrande et al, 2014Casagrande et al, , 2015. Lutein is a hydroxycarotenoid synthetized by autotrophic organisms as an essential photosynthetic pigment.…”

“…Furthermore, captive male starlings undergoing an experimentally induced inflammation were able to maintain song activity when being provided with dietary lutein, while controls birds without access to extra antioxidants significantly decreased their song activity . The first physiological evidence explaining the positive effect of lutein on song indicated that non-reproducing male starlings supplied with dietary lutein had increased endogenous thiols and decreased circulating pro-oxidants (ROMs), suggesting that an amelioration of the redox state was associated with an increase in song activity (Casagrande et al, 2014). The latter study also demonstrated a negative relationship between oxidative damage and the rate of directed and undirected song, suggesting that the song rate of male starlings may be constrained by oxidative status.…”

“…The negative correlation between reactive oxygen metabolites (biomarkers of ongoing oxidative damage to lipids, proteins, and nucleic acids) or protein carbonyls (irreversible damage to proteins) and song rate in captive starlings (Casagrande et al, 2014;Costantini et al, 2015) may suggest that singing activity is not a source of oxidative stress per se and thus does not seem to support the hypothesis that singing performance must entangle costs to be honest, as postulated by the principle of handicap (Zahavi, 1975). However, the seminal paper by Van Noordwijk and de Jong (1986) has nicely demonstrated that heterogeneity in individual quality, and in particular variation in acquisition and allocation of resources, can mask trade-offs.…”

“…Birdsong is also the consequence of a careful synchronization of well-defined brain nuclei that can be vulnerable to oxidative damage (von Schantz et al, 1999;Hill, 2011). Although, a role of the redox state in assuring the honesty of birdsong has been proposed 17 years ago (von Schantz et al, 1999), it has only been investigated recently and in a few studies (Van Hout et al, 2011;Casagrande et al, 2014;Baldo et al, 2015;Costantini et al, 2015). This strongly contrasts with the extensive literature on the mediation of visual signal by oxidative status (reviewed e.g., Blount et al, 2001;McGraw, 2008;Svensson and Wong, 2011;Hill and Johnson, 2012).…”