The Oxidative Cost of Acoustic Signals: Examining Steroid Versus Aerobic Activity Hypotheses in a Wild Bird

Abstract

Vertebrate vocalizations are widespread secondary sexual signals used for mate attraction and territory defence, and variation in signal quality is often condition dependent and impacts reproductive outcomes. Although vocal signal performance is known to reflect various aspects of male quality, few studies have examined the underlying mechanisms mediating its costs and hence its honesty. Using a population of Arctic-breeding snow buntings (Plectrophenax nivalis), we compared the 'Oxidation Handicap Hypothesis', which predicts that testosterone-induced increases in oxidative stress provide a direct mechanistic basis for ensuring the honesty of many secondary sexual signals, to the 'Aerobic Activity Hypothesis, which predicts that it is the aerobic activity involved with signal production (i.e. vocal performance or defending a large territory) and not testosterone directly that links signal quality and oxidative stress. Males singing at faster rates had higher levels of both reactive oxygen metabolites and non-enzymatic antioxidant capacity in the plasma (i.e. without an increase in overall oxidative stress), enabling certain males to produce high-quality signals while also mitigating the costs of an associated increase in oxidative stress. However, these results were completely independent of plasma testosterone levels, supporting the role of aerobic performance in directly affecting oxidative stress. Although song performance was not linked to reproductive parameters in our data set, our research is the first to test these competing hypotheses in a behavioural trait and results suggest that oxidative stress may be an underlying physiological cost preventing low-quality individuals from producing high-quality signals.

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

“…This correlative relationship suggests that oxidative costs arising from song prevent low-quality males from singing at a higher rate. To the best of our knowledge, this is the only study thus far suggesting that song activity is costly in terms of oxidative stress (Baldo et al, 2015). However, from such a correlative approach it is impossible to discern whether the effect was directly caused by singing activity or indirectly induced by other trade-offs that individuals have to face when singing in the wild.…”

“…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.…”

“…A different perspective emerged when free-living birds were studied, as in the case of snow buntings (Plectrophenax nivalis) breeding in a challenging environment such as the Arctic tundra (Baldo et al, 2015). Male snow buntings were sampled upon their arrival on the breeding grounds and were followed through the late egg-laying/early incubation stages.…”

“…(B) Acoustic signals are honest because they are costly, by producing oxidative damage. In this case an up-regulation of enzymatic antioxidants is expected together with a perturbation of other antioxidants processes that mainly depend on the quality of the individual or of their territory (Baldo et al, 2015). In both cases, the environment (and its interaction with the physiological state) is an important factor that needs to be taken into account.…”

“…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).…”