Gábor Á. Czirják

Sexual dimorphism in immune function changes during the annual cycle in house sparrows

Difference between sexes in parasitism is a common phenomenon among birds, which may be related to differences between males and females in their investment into immune functions or as a consequence of differential exposure to parasites. Because life-history strategies change sex specifically during the annual cycle, immunological responses of the host aiming to reduce the impact of parasites may be sexually dimorphic. Despite the great complexity of the immune system, studies on immunoecology generally characterise the immune status through a few variables, often overlooking potentially important seasonal and gender effects. However, because of the differences in physiological and defence mechanisms among different arms of the immune system, we expect divergent responses of immune components to environmental seasonality. In male and female house sparrows (Passer domesticus), we measured the major components of the immune system (innate, acquired, cellular and humoral) during four important life-history stages across the year: (1) mating, (2) breeding, (3) moulting and (4) during the winter capture and also following introduction to captivity in aviary. Different individuals were sampled from the same population during the four life cycle stages. We found that three out of eight immune variables showed a significant life cycle stage × sex interaction. The difference in immune response between the sexes was significant in five immune variables during the mating stage, when females had consistently stronger immune function than males, while variables varied generally non-significantly with sex during the remaining three life cycle stages. Our results show that the immune system is highly variable between life cycle stages and sexes, highlighting the potential fine tuning of the immune system to specific physiological states and environmental conditions.

Preen gland removal increases plumage bacterial load but not that of feather-degrading bacteria

The preen gland is a holocrine sebaceous gland of the avian integument which produces an oily secretion that is spread on the plumage during preening. It has been suggested that birds may defend themselves against feather-degrading bacteria (FDB) and other potential pathogens using preen gland secretions. However, besides some in vitro studies, the in vivo bacterial inhibitory effects of the preen oil on the abundance of feather-associated bacterial species has not yet been studied in passerines. Here we tested the effect of gland removal on the abundance of FDB and other-cultivable bacterial loads (OCB) of male house sparrows (Passer domesticus). Our results did not support earlier results on in vitro antibacterial activity of preen oil against FDB since the absence of the preen gland did not significantly affect their loads related to the control birds. In contrast, we found that preen gland removal led to higher loads of OCB. This result suggests that the antimicrobial spectrum of the preen oil is broader than previously thought and that, by reducing the overall feather bacterial loads, the preen gland could help birds to protect themselves against a variety of potentially harmful bacteria.

The Effect of Coccidians on The Condition and Immune profile of Molting House Sparrows (Passer Domesticus)

ABSTRACT. Feather molt is recognized as an energetically costly activity for birds, and parasite infestation during molt has the potential to reduce host fitness because parasites sequester essential nutrients and stimulate the immune system. We manipulated the coccidian parasite load of captive male House Sparrows (Passer domesticus) by suppressing the natural infection of control birds with an anticoccidial drug and infecting experimental birds with coccidian oocysts. Following infestation, the effect of chronic coccidian infection on individual condition, molt and 12 indices of physiological and immunological function was assessed. We found a significant positive relationship between infestation and heterophil/lymphocyte ratio measured at capture, indicating infectioninduced stress. We also found that coccidians negatively affected feather growth during molt: the increase in wing length of the noninfected birds was significantly higher than that of infected birds. In comparison to control birds, infected birds showed a significantly higher concentration of white blood cells and greater blood bactericidal activity. There was also a positive correlation between infection intensity, agglutination and lysis of blood in the experimentally infested birds, which indicated activation of the constitutive innate immune system during infection. Finally, the total antioxidant capacity of the blood increased significantly, while the carotenoid concentration decreased significantly in infected compared with control birds. Therefore, we showed that coccidians stimulated several measures of the constitutive innate immunity, including the bactericidal activity of the blood, and that coccidians can have significant negative effects on the health and possibly fitness of molting House Sparrows.

Inflammatory challenge increases measures of oxidative stress in a free-ranging, long-lived mammal

SUMMARY Oxidative stress – the imbalance between reactive oxygen species (ROS) and neutralising antioxidants – has been under debate as the main cause of ageing in aerobial organisms. The level of ROS should increase during infection as part of the activation of an immune response, leading to oxidative damage to proteins, lipids and DNA. Yet, it is unknown how long-lived organisms, especially mammals, cope with oxidative stress. Bats are known to carry a variety of zoonotic pathogens and at the same time are, despite their high mass-specific basal metabolic rate, unusually long lived, which may be partly the result of low oxidative damage of organs. Here, we asked whether an immune challenge causes oxidative stress in free-ranging bats, measuring two oxidative stress markers. We injected 20 short-tailed fruit bats (Carollia perspicillata) with bacterially derived lipopolysaccharide (LPS) and 20 individuals with phosphate-buffered saline solution (PBS) as a control. Individuals injected with LPS showed an immune reaction by increased white blood cell count after 24 h, whereas there was no significant change in leukocyte count in control animals. The biological antioxidant potential (BAP) remained the same in both groups, but reactive oxygen metabolites (ROMs) increased after treatment with LPS, indicating a significant increase in oxidative stress in animals when mounting an immune reaction toward the inflammatory challenge. Control individuals did not show a change in oxidative stress markers. We conclude that in a long-lived mammal, even high concentrations of antioxidants do not immediately neutralise free radicals produced during a cellular immune response. Thus, fighting an infection may lead to oxidative stress in bats.

Maternal investment of female mallards is influenced by male carotenoid-based coloration

The differential allocation hypothesis predicts that females modify their investment in a breeding attempt according to its reproductive value. One prediction of this hypothesis is that females will increase reproductive investment when mated to high-quality males. In birds, it was shown that females can modulate pre-hatch reproductive investment by manipulating egg and clutch sizes and/or the concentrations of egg internal compounds according to paternal attractiveness. However, the differential allocation of immune factors has seldom been considered, particularly with an experimental approach. The carotenoid-based ornaments can function as reliable signals of quality, indicating better immunity or ability to resist parasites. Thus, numerous studies show that females use the expression of carotenoid-based colour when choosing mates; but the influence of this paternal coloration on maternal investment decisions has seldom been considered and has only been experimentally studied with artificial manipulation of male coloration. Here, we used dietary carotenoid provisioning to manipulate male mallard (Anas platyrhynchos) bill coloration, a sexually selected trait, and followed female investment. We show that an increase of male bill coloration positively influenced egg mass and albumen lysozyme concentration. By contrast, yolk carotenoid concentration was not affected by paternal ornamentation. Maternal decisions highlighted in this study may influence chick survival and compel males to maintain carotenoid-based coloration from the mate-choice period until egg-laying has been finished.

Variation in haematological indices and immune function during the annual cycle in the Great Tit Parus major

We investigated seasonal variation in haematological indices and immune function in the non-migratory Great Tit Parus major over a complete annual cycle. The haematocrit value showed a marked reduction in spring and summer, reaching a lowest value during moult, after which it increased to reach a maximum in winter and spring. The peak in the heterophil to lymphocyte ratio (H/L) during July indicated that Great Tits were the most stressed during the first half of the moulting period. The increase in heterophils and H/L ratio, concurrent with a reduced number of lymphocytes during the breeding season, probably reflected the cost of reproduction in terms of physiological stress and immune suppression. After breeding the number of heterophils and the H/L ratio decreased, reaching a lowest value during winter. The concentration of immunoglobulins followed the seasonal pattern in the number of heterophils, though highest values occurred somewhat later, in July–September during the second part of the moulting period, Our observations indicated large differences in activity throughout the year of different components of the immune system, This suggests differences in function among the components and possibly differences in susceptibility to stress, parasitism and hormones during the annual cycle. When juveniles became independent of their parents, the immunoglobulin concentration increased, whereas other immune measures did not show a significant change. This indicates a rapid increase of at least one component of the immune system after the young fledge.

Measures of the Constitutive Immune System Are Linked to Diet and Roosting Habits of Neotropical Bats

Ecological and social factors are central in the emergence and transmission of infectious diseases, thus bearing the potential for shaping a species’ immune functions. Although previous studies demonstrated a link between social factors and the cellular immune system for captive mammals, it is yet poorly understood how ecological factors are connected with the different branches of the immune system in wild populations. Here, we tested how variation in aspects of the constitutive cellular and humoral immune system of free ranging bats is associated with two ecological factors that likely influence the putative risk of species to become infected by parasites and pathogens: diet and shelter. We found that white blood cell counts of 24 syntopic Neotropical bat species varied with the species’ diet and body mass. Bats that included at least partially vertebrates in their diet exhibited the highest white blood cell counts, followed by phytophagous and insectivorous species, which is in agreement with the assumption that the immune system varies with the pathogen transmission risk of a trophic level. The soluble part of the constitutive immune response, assessed by an in vitro bacterial killing assay, decreased with increasing roost permanence. Our results suggest that the ecology is an important factor in the evolution of the immune system in bats and probably also other mammals.

Effect of preen oil on plumage bacteria: An experimental test with the mallard

Feathers are essential for avian thermoregulation, communication or flight and a reduction of plumage condition may alter these functions and reduce individual fitness. Recently, descriptive studies provided evidence that birds carry feather-degrading bacteria on their plumage that have the ability to degrade feathers rapidly under laboratory conditions. If such bacteria reduce avian fitness, natural selection should favour the evolution of anti-bacterial defences to limit the effects of these detrimental microorganisms. Preening behaviour and associated preen gland secretions have been proposed as the main factor used by birds to limit feather-degrading bacterial growth and some recent in vitro studies provided evidence that uropygial oil inhibited the growth of some keratinolytic strains in passerines. However, preen oil antimicrobial properties remained to be experimentally tested in vivo. We conducted an experiment with mallards (Anas platyrhynchos) onto which we fixed a removable mechanism that blocked access to the uropygial gland in a first group of mallards, whilst birds in a second group had the same removable mechanism but access to their gland and a third group of birds had normal access to their gland. We found no significant effect of our treatment on total and feather-degrading bacterial loads. Three hypotheses may explain the discrepancy between our results and previous in vitro studies. First, in vitro studies may have over-estimated the bactericidal properties of the preen oil. Second, preen gland deprivation may have affected only a small portion of the feather-degrading bacterial community. Third, ducks and passerine oils might have different bactericidal properties.

Carotenoids modulate the effect of coccidian infection on the condition and immune response in moulting house sparrows.

SUMMARY In the present study, we experimentally manipulated coccidian parasitism and dietary carotenoid availability in a fully factorial experiment in male house sparrows (Passer domesticus Linnaeus), and tested whether carotenoid supplementation reduces the cost of parasitism in terms of condition, moult and immune responses. We found that coccidians have a significant but transient negative effect on body mass, which can be reduced if birds have access to carotenoid supplementation in their diet. Experimental manipulation had no significant effect on the moulting parameters of the birds measured following coccidian infestation and during the whole moulting period. Carotenoid supplementation increased the plasma carotenoid concentration in both infested and medicated birds treated with a coccidiostatic drug; however, after two months exposure to parasites, plasma carotenoid concentration increased only in the carotenoid-supplemented and medicated group whereas no difference was observed between the carotenoid-supplemented and infested and non-supplemented groups. On the contrary, coccidian infestation was not affected by carotenoid supplementation. Experimental infestation decreased the antibody response to sheep red blood cells (SRBCs), although no significant effect was observed in the capacity of the birds to respond to a mitogenic challenge with phytohemagglutinin. Within the experimentally infested groups birds with carotenoid-supplemented food tended to have an increased anti-SRBC humoral immune response. The positive correlation between coccidian infestation and the strength of the humoral immune response against SRBCs in the non-supplemented and infested groups indicates that this part of the immune system plays an important role in defence against these parasites.

Correlates between Feeding Ecology and Mercury Levels in Historical and Modern Arctic Foxes (Vulpes lagopus)

Changes in concentration of pollutants and pathogen distribution can vary among ecotypes (e.g. marine versus terrestrial food resources). This may have important implications for the animals that reside within them. We examined 1) canid pathogen presence in an endangered arctic fox (Vulpes lagopus) population and 2) relative total mercury (THg) level as a function of ecotype (‘coastal’ or ‘inland’) for arctic foxes to test whether the presence of pathogens or heavy metal concentration correlate with population health. The Bering Sea populations on Bering and Mednyi Islands were compared to Icelandic arctic fox populations with respect to inland and coastal ecotypes. Serological and DNA based pathogen screening techniques were used to examine arctic foxes for pathogens. THg was measured by atomic absorption spectrometry from hair samples of historical and modern collected arctic foxes and samples from their prey species (hair and internal organs). Presence of pathogens did not correlate with population decline from Mednyi Island. However, THg concentration correlated strongly with ecotype and was reflected in the THg concentrations detected in available food sources in each ecotype. The highest concentration of THg was found in ecotypes where foxes depended on marine vertebrates for food. Exclusively inland ecotypes had low THg concentrations. The results suggest that absolute exposure to heavy metals may be less important than the feeding ecology and feeding opportunities of top predators such as arctic foxes which may in turn influence population health and stability. A higher risk to wildlife of heavy metal exposure correlates with feeding strategies that rely primarily on a marine based diet.