Lauri Saks

Do dietary antioxidants alleviate the cost of immune activation? An experiment with greenfinches.

Reactive oxygen and nitrogen species produced by metabolism and immune defenses can cause extensive damage to biomolecules. To counteract this damage, organisms rely on exogenous and endogenous antioxidants, although their relative importance in maintaining redox balance is unclear. We supplemented captive greenfinches with dietary antioxidants—carotenoids and vitamin E—and injected them with an inflammatory agent, phytohemagglutinin. Compared to controls, immune‐challenged birds circulated more lipid peroxidation products but also increased total plasma antioxidativity. Carotenoid (but not vitamin E) supplementation generally reduced lipid peroxidation, but this did not compensate for the effects of immune activation. Levels of an endogenous antioxidant—uric acid—strongly contributed to plasma antioxidativity. We found no evidence that dietary antioxidants are immunostimulatory. These results demonstrate the antioxidant function of carotenoids in birds and show that simultaneous assessment of oxidative stress‐driven damage, antioxidant barrier, and individual antioxidants is critical for explaining the potential costs of immune system activation.

Antioxidant protection, carotenoids and the costs of immune challenge in greenfinches.

SUMMARY Costs accompanying immune challenges are believed to play an important role in life-history trade-offs and warranting the honesty of signal traits. We performed an experiment in captive greenfinches (Carduelis chloris L.) in order to test whether and how humoral immune challenge with non-pathogenic antigen [sheep red blood cells (SRBC)] affects parameters of individual condition including intensity of coccidian infection, estimates of total antioxidant protection, plasma carotenoids and ability to mount a cell-mediated immune response. We also asked whether the potential costs of immune challenge can be alleviated by dietary carotenoid supplementation. None of the treatments affected intensity of coccidiosis. Humoral immune challenge suppressed the cell-mediated response to phytohemagglutinin (PHA), suggesting a trade-off between the uses of different arms of the immune system. Immune challenge reduced body-mass gain, but only among the carotenoid-depleted birds, indicating that certain somatic costs associated with immune system activation can be alleviated by carotenoids. No evidence for oxidative stress-induced immunopathological damages could be found because immune activation did not affect total antioxidant protection or carotenoid levels. Carotenoid supplementation inclined birds to fattening, indicating that lutein interfered with lipid metabolism. Altogether, our results support the hypotheses of biological importance of carotenoids and exemplify the overwhelming complexity of their integrated ecophysiological functions.

Host resistance and parasite virulence in greenfinch coccidiosis

The question why different host individuals within a population differ with respect to infection resistance is of fundamental importance for understanding the mechanisms of parasite‐mediated selection. We addressed this question by infecting wild‐caught captive male greenfinches with intestinal coccidian parasites originating either from single or multiple hosts. Birds with naturally low pre‐experimental infection retained their low infection status also after reinfection with multiple strains, indicating that natural infection intensities confer information about the phenotypic ability of individuals to resist novel strains. Exposure to novel strains did not result in protective immunity against the subsequent infection with the same strains. Infection with multiple strains resulted in greater virulence than single‐strain infection, indicating that parasites originating from different host individuals are genetically diverse. Our experiment thus demonstrates the validity of important but rarely tested assumptions of many models of parasite‐mediated selection in a wild bird species and its common parasite.

Dexamethasone inhibits corticosterone deposition in feathers of greenfinches

Corticosterone (CORT) content of feathers is a potent source of information about activation of hypothalamus-pituitary-adrenal (HPA) axis during feather growth, which is used for assessment of well-being and stress history of individuals and populations in avian studies. However, little is known about factors affecting deposition of CORT into feathers and how feather CORT covaries with other markers of stress imposed upon individuals during feather growth. We addressed these questions by measuring CORT levels in feathers of wild-caught greenfinches (Carduelis chloris) brought into captivity. One tail feather was removed from all the birds upon arrival to the laboratory and the CORT levels of replacement feathers, grown in captivity were recorded. The birds were subjected to treatments of immune activation (by injection of phytohaemagglutinin) and synthetic glucocorticoid (dexamethasone, DEX) administration. Only DEX injection affected feather CORT levels. DEX-injected birds deposited on average 37% less of CORT in their feathers than saline-injected birds. Despite significant effects of DEX and immune activation treatments on differential leukocyte counts, we did not find any correlations between CORT and leukocyte hemoconcentrations or heterophil/lymphocyte ratios (a haematological index of stress), measured at three stages of feather growth. Our findings provide novel evidence that feather CORT levels are sensitive to manipulation of hormonal balance of birds, thereby supporting the diagnostic value of feather CORT measurements. However, we did not find any evidence about covariation between feather CORT and other markers of stress perceived during the period of feather growth. This calls for further research on information content of feather CORT, preferably in experiments manipulating more diverse array of psychological, immunological and abiotic stressors.

Parasite infection and decreased thermal tolerance: impact of proliferative kidney disease on a wild salmonid fish in the context of climate change

Summary Parasites and pathogens can have an important effect on their hosts thermal resistance. The impact of parasite infection on host physiological performances has traditionally been studied in controlled laboratory conditions, and much less is known about its actual effects in wild populations. Nonetheless, such knowledge is critical when assessing the effect of climate change on the future survival of the host. Tetracapsuloides bryosalmonae is a myxozoan endoparasite causing proliferative kidney disease (PKD) in salmonids. Infection and clinical symptoms of PKD are dependent on environmental temperature and PKD has become an emerging disease of primary importance for farmed and wild salmonids in the last decades. Despite important achievements in understanding PKD pathology in recent years, there are still crucial gaps in the knowledge of the disease ecology, notably in how the parasite affects host performance in the wild. We sampled juvenile (0+) brown trout (Salmo trutta) from the wild during early and late summer and assessed relative parasite load (DNA quantification with qPCR) and disease severity (kidney hyperplasia). We also measured haematocrit, leucocyte formula, aerobic scope and upper thermal tolerance in a field-physiology approach in order to better understand the relationships between PKD severity and host performance. By using wild-caught individuals and performing measurements directly on location, we aimed to gain insights into host physiology in a natural environment while avoiding biases caused by laboratory acclimation. We found that most physiopathological symptoms in the wild were strongly correlated with kidney hyperplasia, but more weakly linked to parasite load. Disease severity was positively correlated with anaemia and abundance of circulating thrombocytes, and negatively correlated with aerobic scope and thermal tolerance. Our results suggest that impaired aerobic performances and thermal tolerance in infected fish may potentially result in decreased host survival in the wild, especially in relation with predicted higher average summer temperatures and increased frequency of extreme events (summer heatwaves) in the context of global climate change. A Lay Summary is available for this article.

Carotenoid Coloration in Greenfinches Is Individually Consistent Irrespective of Foraging Ability

Carotenoid‐based plumage coloration of birds has been hypothesized to honestly reflect individual quality, either because carotenoids are difficult to acquire via food or because of a trade‐off in allocation of carotenoids between maintenance and signaling functions. We tested whether differential foraging ability is a necessary precondition for maintaining individual differences in carotenoid‐based plumage coloration in male greenfinches (Carduelis chloris). Wild‐caught birds were brought into captivity, where half of them were supplemented with carotenoids while the other half was maintained on a carotenoid‐poor diet. Color of the yellow parts of tail feathers, grown under natural conditions, was compared with that of the replacement feathers, grown in captivity. Carotenoid supplementation increased feather chroma (saturation). Color of wild‐grown feathers significantly correlated with the color of lab‐grown feathers. This result demonstrates the existence of a significant component of variation in carotenoid coloration, which reflects physiological qualities or genetic differences among individuals independent of foraging ability. Among both experimental groups, plasma carotenoid concentration during feather growth strongly correlated with chroma of the feathers grown in captivity. This indicates that carotenoid‐based plumage coloration can reveal circulating carotenoid levels over a very wide range of concentrations, suggesting the ample signaling potential of such a mechanism.

Carotenoid-based plumage coloration is not affected by vitamin E supplementation in male greenfinches

Carotenoid-based colours have become an important model of honest signalling as carotenoids are suggested to play vital roles in several physiological functions including antioxidants and immunostimulators, while they are also required for sexual displays. However, it has been recently suggested that carotenoid-based signals may be used mainly as reflectors of the systems that prevent their oxidation (mainly the amount of other non-pigmented antioxidants) rather than the antioxidative properties of carotenoids themselves. We tested this hypothesis by examining the effect of simultaneous supplementation of carotenoids and an uncoloured antioxidant—vitamin E—on the coloration of growing tail feathers in captive male greenfinches (Carduelis chloris chloris L.). While carotenoid supplementation enhanced the coloration of the feathers, manipulation of dietary vitamin E had no effect. Thus, our results do not support the idea that carotenoids are mainly used as indicators of the abundance of other antioxidants.

Antioxidant protection, immune function and growth of nestling great tits Parus major in relation to within-brood hierarchy

Differences in competitive abilities of siblings in birds can be caused by a combination of hatching asynchrony and intra-clutch variation in egg quality. However, very little is known how within-brood hierarchies affect the allocation of resources between different functions of the body. We examined the effects of within-brood hierarchy on growth of morphological parameters, blood plasma antioxidant protection and immune function of free-living great tit Parus major nestlings. To assure that competitive hierarchies occur, we experimentally delayed the start of incubation of the last two eggs in the clutch. At pre-fledging stage (day 13 post-hatch), late-hatched nestlings were smaller in body mass and wing length when compared to early-hatched nestlings, but no differences between siblings were found in tarsus length, plasma antioxidant potential, uric acid concentration, residual antioxidant potential (from regression with uric acid), hematocrit and response to phytohaemagglutinin injection. In early-hatched nestlings, the antioxidant potential and residual antioxidant potential measured in the middle of nestling period (day 6 post-hatch) were negatively related to body mass growth at early nestling stage, indicating that fast initial growth could reduce antioxidant properties of blood plasma.

Comparative analysis reveals a possible immunity-related absence of blood parasites in Common Gulls (Larus canus) and Black-headed Gulls (Chroicocephalus ridibundus)

AbstractBlood parasites often incur a substantial fitness cost to the infected individuals, sometimes resulting in death of the host. Some bird species, however, are apparently free of blood parasites, presumably due to the lack of exposure to blood parasite vectors. Protective immunity may be also responsible for the absence of infections by haematozoa. In this study, we tested the presence of blood parasites in Common Gulls (Larus canus) and Black-headed Gulls (Chroicocephalus ridibundus) nesting in environments with varying vector exposure. We failed to find blood parasites in Common Gulls irrespective of vector exposure, whereas infection rates of Black-headed Gulls were generally very low. We propose that the absence of haematozoa and low prevalence of blood parasites in these species of gulls is probably not a function of vector exposure and suggest alternative explanations such as enhanced immunity.ZusammenfassungVergleichende Analysen zeigen eine möglicherweise mit dem Immunsystem zusammenhängende Abwesenheit von Blutparasiten bei Sturmmöwen (Larus canus) und Lachmöwen (Chroicocephalus ridibundus) Blutparasiten bedingen oft substantielle Fitness-Aufwendungen für die betroffenen Individuen, die nicht selten zum Tod des Wirts führen. Manche Vogelarten sind jedoch offensichtlich frei von Blutparasiten, vermutlich deshalb, weil sie deren Überträgern nicht ausgesetzt sind. Diese Art von schützender Immunität ist wahrscheinlich auch dafür verantwortlich, dass es bei ihnen keine durch Hämatozoen bedingte Infektionen gibt. In unserer Studie untersuchten wir das Vorhandensein von Blutparasiten bei Sturm- und Lachmöwen, die ihre Nester in Umgebungen gebaut hatten, in denen sie in unterschiedlicher Weise einer möglichen Übertragung der Parasiten ausgesetzt waren. Unabhängig davon, wie sehr sie einer möglichen Übertragung ausgesetzt waren, konnten wir bei den Sturmmöwen gar keine Blutparasiten nachweisen, und bei den Lachmöwen war die Infektionsrate durchweg sehr niedrig. Wir vermuten deshalb, dass bei diesen Vogelarten das Fehlen von Hämatozoen und die geringe Verbreitung von Blutparasiten nicht davon abhängen, ob und wie sehr sie den Überträgern ausgesetzt sind. Stattdessen vermuten wir hier andere Erklärungen wie z. B. ein stärkeres Immunsystem.

Food selection of Coregonus lavaretus in a brackish water ecosystem.

This study examined how variability in the abundance and biomass structure of benthic invertebrates affected the feeding choice of the whitefish Coregonus lavaretus on a hard bottom habitat of the brackish Baltic Sea. In general, crustaceans such as Idotea balthica and Gammarus spp. were preferred over molluscs. Although being the most numerous taxon in the invertebrate samples, Mytilus trossulus was the lowest ranking in C. lavaretus food preference. The availability of benthic invertebrate prey set the dietary range of fish but the selectivity largely described fish feeding within this range. There was no clear link between fish predation and the dominance structure of benthic invertebrate communities, suggesting that species composition, abundance and biomass of invertebrate species had no impact on the feeding selectivity of the fish. Thus, while fish predation may not affect the dominant species within a benthic community, due to strong selectivity fish may impose strong pressure on some rarer but highly preferred invertebrate prey species.