Glasgow Theses Service

Roles of dietary antioxidants and oxidative stress in mediating fitness related traits in birds

Larcombe, Stephen Donald (2008) Roles of dietary antioxidants and oxidative stress in mediating fitness related traits in birds. PhD thesis, University of Glasgow.

Full text available as:
[img]
Preview
PDF
Download (4Mb) | Preview

Abstract

Trade-offs occur where different physiological systems compete for the same limited resource. Reactive oxygen species (ROS) can potentially damage all endogenous cells and processes, and antioxidants help prevent this oxidative stress. Since dietary acquired antioxidants are a limited resource, there is growing interest in the roles of dietary antioxidants in mediating life-history trade-offs. During reproduction, mothers must trade-off investing antioxidants in reproduction, and retaining them for self maintenance. Improving maternal antioxidant condition may allow increased investment of antioxidants in chicks and/or in self maintenance during breeding. Outwith the breeding season animals may also trade-off antioxidants between roles in physiological systems associated with large amounts of ROS production. During exercise, energy metabolism increases production of ROS, and dietary antioxidants may remove these, protecting tissue associated with exercise and potentially improving exercise performance. Most previous studies of antioxidants in birds have focused on carotenoids, but the antioxidant functions of carotenoids have recently been questioned. In this thesis I studied the effects of antioxidants, with proven antioxidant function in vivo on a range of fitness related traits in birds. Specifically, I assessed the effects of dietary antioxidant availability on maternal and offspring phenotype and fitness in blue tits Cyanistes caeruleus. I also investigated the role of dietary antioxidants in reducing oxidative stress produced during exercise in adult captive budgerigars Melopsittacus undulatus. Supplementing blue tit parents with [alpha]-tocopherol, a potent dietary antioxidant, before and during egg laying did not affect maternal condition, nor reproductive performance. Mothers supplemented with [alpha]-tocopherol produced significantly more daughters than control mothers. I initially predicted [alpha]-tocopherol supplementation may result in male-biased sex ratios, since an improvement in maternal condition may allow increased investment in the larger, more costly sex. I discuss potential reasons for this difference in sex ratio between control and [alpha]-tocopherol supplemented broods. Of course, the true test of maternal allocation decisions is in effects on phenotype and fitness of mothers and offspring alike. Next, I cross-fostered half broods from [alpha]-tocopherol treated pairs with control treated pairs, to separate effects due to egg quality from those of rearing environment. Chicks from [alpha]-tocopherol treated egg parents were smaller on day three, than control chicks. However, chicks from [alpha]-tocopherol eggs grew faster than controls, and by day 14 there was no difference in mass. The [alpha]-tocopherol chicks did not pay the expected oxidative cost of this increased growth rate, indicating efficient antioxidant systems in these chicks. There was no obvious benefit of this increased growth rate in [alpha]-tocopherol chicks, in terms of phenotype at fledging. Despite the difference in sex ratio previously described, daughters from [alpha]-tocopherol supplemented egg parents were not in better condition than control daughters. There was some evidence that male chicks reared by control parents had longer tarsi than male chicks reared by [alpha]-tocopherol parents. Interestingly, retrapping adults and F1 chicks the year following experimental supplementation suggested increased survival, and future reproduction of [alpha]-tocopherol supplemented mothers. The effect on F1 offspring was less clear, but we captured more chicks from [alpha]-tocopherol supplemented egg parents in winter two years following the experiment. There was no evidence that survival of adults was related to the sex ratio of their broods. In the next experiment, I tested the Red Herring hypothesis. The Red Herring hypothesis suggests that carotenoids are unlikely to be used as antioxidants in nature. However, carotenoid mediated plumage traits may still reveal antioxidant levels as non-pigmentary antioxidants may increase expression of carotenoid mediated plumage colour, through antioxidative protection of carotenoid pigments. By supplementing chicks within a brood with either; [alpha]-tocopherol, carotenoids or control, I hoped to assess the roles of different antioxidants during development in blue tits, with particular reference to plumage colouration and oxidative stress. Contrary to the Red Herring hypothesis, [alpha]-tocopherol supplemented chicks did not have reduced oxidative stress compared to controls or carotenoid treated birds, as measured by malonidialdehyde (MDA), a by-product of lipid-peroxidation. Only chicks supplemented with carotenoids increased in plumage colour, thus I found no evidence that non-pigmentary antioxidants protect carotenoid pigments from oxidation and bleaching. In addition to growth, another process that can lead to increased ROS production is physical activity. In captive adult budgerigars, I found a relationship between the propensity to engage in active behaviours during undisturbed observations, and a measure of DNA damage. This suggests individual differences in oxidative stress may be partly mediated by differences in activity rates. It was not possible to rule out a role for stress-related behaviour mediating this relationship. Interestingly, I also found a positive relationship between DNA damage, and selection of an antioxidant rich food item. This has two implications; firstly, that birds may detect oxidative damage levels and react accordingly. Secondly, that dietary antioxidants may play an important role in alleviating oxidative stress. Of particular note, was the fact that three different measures of oxidative stress carried out for each individual did not correlate with one another. Different measures may therefore reveal specific types of oxidative damage, and selection of an appropriate test will be important when interpreting results relating to oxidative stress. Flight is the most metabolically expensive behaviour in birds, and the most likely to result in oxidative stress. By subjecting relatively sedentary budgerigars to measured exercise, I manipulated an oxidative cost for each bird. I assessed individual differences in oxidative stress and take-off escape time in birds following both an enhanced or reduced quality diet. Birds always had reduced levels of oxidative stress on the enhanced quality diet, rich in antioxidants, regardless of diet order. This shows that flight activity can increase oxidative stress in birds, and that dietary antioxidants may ameliorate this. All three indices of oxidative stress used showed an effect of flight exercise. There was no difference in escape time on different diets, but differences in exercise performance may only be detectable in tests of stamina, or with longer experimental manipulation of diet and activity. Using a captive population of wild-type budgerigars, I assessed the role of exercise training on oxidative stress. I found that birds had reduced levels of MDA after long-term flight training than after one day of flight training. This result was independent of diet quality. This shows that performing the same exercise task repeatedly attenuates oxidative stress, perhaps mediated by an upregulation of endogenous antioxidant enzymes. Whether or not such an upregulation in antioxidant activity is possible in wild birds is unclear; antioxidant activity may operate maximally at all times. This has important implications for all studies of antioxidants in life-history trade-offs. I conclude that dietary acquired antioxidants are important nutrients, mediating a range of trade-offs in birds. The multifaceted effects of dietary antioxidants merit further investigation, to elucidate their precise role in determining oxidative stress, and ultimately fitness.

Item Type: Thesis (PhD)
Qualification Level: Doctoral
Keywords: antioxidants, oxidative stress, behaviour, behavioural ecology
Subjects: Q Science > QL Zoology
Colleges/Schools: College of Medical Veterinary and Life Sciences
Supervisor's Name: Arnold, Dr. Kathryn E.
Date of Award: 2008
Depositing User: Mr Stephen Larcombe
Unique ID: glathesis:2008-403
Copyright: Copyright of this thesis is held by the author.
Date Deposited: 10 Nov 2008
Last Modified: 10 Dec 2012 13:18
URI: http://theses.gla.ac.uk/id/eprint/403

Actions (login required)

View Item View Item