Carotenoids and the Costs of Reproduction: Studies in the Lesser Black-Backed Gull

1. Life history theory predicts that a reproduction is costly, and a physiological trade-off exists between investment in current and future reproduction; in one respect this could correspond to a trade-off between the allocation of resource(s) to reproduction and immune defence. However, the identity of the limiting resource(s) remains a contentious issue in evolutionary ecology. In birds, it seems possible that carotenoid pigments could be limiting; birds cannot synthesise carotenoids de novo (they must obtain them in their diet). Studies of domesticated hens have shown that carotenoids can enhance immune function, antioxidant activity, and also sperm quality, and carotenoids are also transferred from maternal circulation into egg yolk. This thesis consists of experiments designed to test whether a trade-off between reproduction and immune function is modulated by carotenoid supply, using free-living lesser black-backed gulls, Lams fuscus, as a study species. 2. The effects of carotenoid supply on maternal phenotype, and the implications for egg production capacity and egg phenotype were studied. It is shown that dietary carotenoid supplementation during the pre-laying period translated into increased maternal body levels of carotenoids and antioxidant activity, and lower plasma levels of immunoglobulins (Ig). In turn, carotenoid-fed females produced eggs containing high carotenoid but low Ig concentrations (i.e. passive immunity), whereas the opposite pattern was observed in controls. It is hypothesised that high yolk carotenoid levels might compensate for low levels of passive immunity in determining chick performance. 3. The role of physiological discrimination among ingested carotenoids (differential uptake, transport, deposition, or metabolic conversions) in determining yolk carotenoid profiles is examined in a carotenoid supplementation experiment. We supplementally fed pre-laying gulls with a cocktail of four carotenoids, or a carotenoid-free (control) supplement, then compared the yolk carotenoid profile and susceptibility to lipid peroxidation in eggs that they laid. In comparison with controls, there was an increase in the yolk concentrations of seven carotenoids, and also unidentified carotenoids in eggs produced by carotenoid-supplemented females. However, the relative proportions of five classes of carotenoid did not differ significantly, and consequently the percentage profile of yolk carotenoids was positively correlated, between feeding treatments, possibly indicating metabolic transformations and differential transfer of carotenoids from maternal diet to yolk. Potential energetic costs to females, and benefits in terms of antioxidant - capacity imparted to offspring, are discussed. 4. The role of carotenoid supply as a resource underlying a trade-off between chick-rearing capacity (i.e. work rate) and immune function is investigated in female gulls using a factorial experiment (carotenoid supplementation crossed with inoculation; the inoculum comprised a non-replicating antigen - sheep red blood cells (SRBC)). Experimental nests were given a control clutch of eggs produced by non-manipulated birds to incubate and rear. It is shown that females that had received an immune challenge and the control (carotenoid-free) supplement produced relatively light foster fledglings in comparison with females of the other treatments, consistent with the explanation that there was a trade-off between immune function and chick-rearing capacity which was mediated by carotenoid supply. 5. The role of carotenoid supply as a resource underlying a trade-off between egg production capacity and immune function is investigated in female gulls using a factorial experiment (carotenoid supplementation crossed with SRBC inoculation). Following removal of first clutches, it is shown that carotenoid-fed females had an increased egg production capacity (re-laying rate, clutch size), and produced eggs of higher quality than controls (higher yolk carotenoid levels; larger immune responses and higher survival in chicks reared singly in foster nests). However, there were no effects of maternal SRBC inoculation on any of these measures of egg production or egg quality. It is suggested that females facing an immune challenge maintained their level of investment in egg production, even at the expense of their own condition (chick-rearing capacity; see point 4, above), suggesting that egg quality may ultimately be more important than parental condition during the rearing period in determining reproductive success. 6. The fertility of males sometimes correlates with their ornamental display, but a mechanistic explanation to universally link these traits has been lacking. I hypothesise that both sperm quality (fertility; structural integrity of DNA), and the substrates responsible for male ornamentation, may be vulnerable to free ~ radical attack, which can be mitigated by antioxidants. I hypothesise that a link between ornamentation and sperm quality could arise if antioxidants are in limited supply, and the showiest males may be preferred because they are most likely to be fertile, or to provide sperm with undamaged genotypes that could give rise to fit offspring