Differential effects of vitamins E and C and carotenoids on growth, resistance to oxidative stress, fledging success and plumage colouration in wild great tits

Abstract

Oxidative stress is the imbalance between the production of reactive species and antioxidants, which causes damage to lipids, proteins and DNA. Antioxidants, like vitamins and carotenoids, can limit oxidative damage and can therefore regulate the trade-off between growth, which is a period of high reactive species production, and self-maintenance. However, the role of carotenoids as antioxidants in vivo has been debated, and it has been suggested that carotenoidbased signals indicate the availability of non-pigmentary antioxidants (e.g. vitamins) that protect carotenoids from oxidation, known as the 'protection hypothesis'. To evaluate the importance of vitamins versus carotenoids as antioxidants during growth and to test the protection hypothesis, we supplemented nestling great tits, Parus major, 3, 5 and 7 days after hatching with a single dose of carotenoids and/or vitamins in a 2×2 full-factorial design. We subsequently measured body condition, antioxidant capacity, oxidative damage, fledging success and plumage reflectance. Vitamins enhanced antioxidant capacity, but did not affect oxidative damage. Vitamin-treated nestlings had higher growth rates and higher probability of fledging. In contrast, carotenoids did not affect any of these traits. Furthermore, carotenoid-based colouration increased over the breeding season in nestlings that received vitamins only. This study shows that vitamins are limiting for growth rate and fledging success, and suggests that vitamins could regulate the trade-off between growth and selfmaintenance in favour of the former. Moreover, our results are consistent with the idea that carotenoids are minor antioxidants in birds, but they do not support the protection hypothesis.

The role of the antioxidant system during intense endurance exercise: lessons from migrating birds

“…Carotenoids are responsible for most pigmentation in bird plumage, and the role of these molecules as advertisements for an individual's antioxidant or immune defense capacity has been widely studied (Chui et al, 2011;Giraudeau et al, 2013;Hill et al, 2006;Marri and Richner, 2014;Mcgraw, 2011;Negro et al, 2014). In plants, carotenoids serve as powerful scavengers of singlet oxygen radicals (Halliwell and Gutteridge, 2007), but in animals, their role as antioxidants is less clear.…”

“…Great tits supplemented with carotenoids and experimentally manipulated to increase physical activity showed increased circulating carotenoid concentrations, but also displayed increased oxidative damage and reduced antioxidant capacity (Vaugoyeau et al, 2015). Therefore, the role of carotenoids as potent antioxidants is debated (Costantini and Møller, 2008;Halliwell and Gutteridge, 2007;Hill and Johnson, 2012;Marri and Richner, 2014;Pamplona and Costantini, 2011), and recent research has emphasized that carotenoids may act as a signal for oxidative health rather than as antioxidants themselves (Costantini and Møller, 2008;Hill and Johnson, 2012;Johnson and Hill, 2013). Other evidence suggests that carotenoids stored in subcutaneous fat depots may protect fats from damage by RS or act as a reservoir of antioxidants for activities that result in oxidative challenges, such as flight (Metzger and Bairlein, 2011;Pamplona and Costantini, 2011;Tomášek et al, 2016).…”

Plasma markers of oxidative stress are uncorrelated in a wild mammal

“…2011; Wilson et al. 2012; Marri and Richner 2014). Laboratory studies that manipulate oxidative challenge or life‐history investment are pivotal to our ability to establish whether OS may underpin life‐history variation (Metcalfe and Monaghan 2013), and there is emerging experimental evidence that supports this overarching hypothesis (Sohal et al.…”

Interactive effects of early and later nutritional conditions on the adult antioxidant defence system in zebra finches

“…Most of the studies that have investigated the early-life influence of dietary micronutrients on antioxidant protection have focused on a single developmental period, usually during pre-or early postnatal development (de Ayala et al, 2006;Hall et al, 2010;Marri and Richner, 2014;Noguera et al, 2011b). However, the diet during later developmental periods is also relevant since there may be compensation for earlier periods of undernutrition if conditions subsequently improve (Metcalfe and Monaghan, 2001).…”