House sparrows offset the physiological trade‐off between immune response and feather growth by adjusting foraging behavior

Growing feathers and mounting immune responses are both energetically costly for birds. According to the life history trade‐off hypothesis, it has been posited that the costs of feather growth lead to temporal isolation between molt and other expensive activities, reproduction for example. In contrast to life cycle events, the need to mount an immune response can occur at any time, including during feather growth. Thus, we hypothesized that mounting an immune response during feather growth may divert energy and resources from feather growth and impair feather renewal. To test this hypothesis, we clipped or plucked the same feathers of male house sparrows Passer domesticus biblicus. In the clipped group (n = 16), the feathers were absent with no regrowth; in the plucked group (n = 14), feathers were absent and regrowth was initiated. We also had an intact control group of 15 sparrows. We then initiated an inflammatory immune response by subcutaneous injection over the left breast muscle of the birds with a lipopolysaccharide (LPS) and quantified behavioral and physiological responses. We predicted that sparrows with plucked feathers would incur the highest energetic costs while mounting an immune response, and would increase their foraging effort to offset this cost. We found no difference in body mass and resting metabolic rates among sparrows subjected to the different feather and immune treatments. However, we did find that while sparrows with plucked feathers increased foraging efficiency following the immune challenge by paying fewer but longer visits to the food tray, allowing them to maintain food consumption. Foraging efficiency in sparrows with clipped feathers was reduced. We also found that quality of newly grown feathers after the immune challenge was poorer in the plucked group, suggesting that mounting an immune response competes with feather growth for resources.     

Immune challenge affects basal metabolic activity in wintering great tits

The costs of exploiting an organism's immune function are expected to form the basis of many life-history trade-offs. However, there has been debate about whether such costs can be paid in energetic and nutritional terms. We addressed this question in a study of wintering, free-living, male great tits by injecting them with a novel, non-pathogenic antigen (sheep red blood cells) and measuring the changes in their basal metabolic rates and various condition indices subsequent to immune challenge. The experiment showed that activation of the immune system altered the metabolic activity and profile of immune cells in birds during the week subsequent to antigen injection: individuals mounting an immune response had nearly 9% higher basal metabolic rates, 8% lower plasma albumin levels and 37% higher heterophile-to-lymphocyte ratios (leucocytic stress indices) than sham-injected control birds. They also lost nearly 3% (0.5 g) of their body mass subsequent to the immune challenge. Individuals that mounted stronger antibody responses lost more mass during the immune challenge. These results suggest that energetic expenditures to immune response may have a non-trivial impact upon an individual's condition.     

Rhodopechys obsoleta (desert finch): a pale ancestor of greenfinches ( Carduelis spp.) according to molecular phylogeny

The evolutionary history of three out of four birds traditionally classified into the genus Rhodopechys birds has been studied by comparing their mitochondrial cytochrome b DNA sequence with that of greenfinches and other genus Carduelis finches. The desert finch (Rhodopechys obsoleta) or a sister extinct species seems to have existed about 6 million years ago in Asian and perhaps African desert-like areas. This bird has no molecular relationship with other Rhodopechys birds and seems to have given rise to the greenfinches radiation, probably by allopatry of marginal or isolated groups; the latter would have evolved to green plumage colours and more simple song modulations (i.e., greenfinches). The possible role of assortative mating and the newly postulated acquired phenotypic characters in greenfinches speciation are discussed.     

Swainson’s thrushes in migratory disposition exhibit reduced immune function

Evidence indicates that the immune system, which protects an organism from parasitic and pathogenic infections, is frequently suppressed when animals are engaged in activities involving strenuous exercise. We tested the hypothesis that birds reduce immune function during the migratory period in preparation for the anticipated heightened energetic demands of long flights. Swainson’s thrushes (Catharus ustulatus), captured in fall, were held in an indoor aviary until January, when migratory disposition was induced in half of the birds with an artificially prolonged daylength. Experimental birds became hyperphagic and deposited fat stores, and then displayed nocturnal activity (Zugunruhe) characteristic of the spring migratory period. Cell-mediated immunity was measured by intradermal injection of phytohemagglutinin in the wing patagium of both control and experimental birds. Birds exhibiting migratory restlessness had a reduced cell-mediated immune response compared to control birds. Our results suggest that birds are immunosuppressed during the migratory period. The suppression may be a nonadaptive response due to unrelated physiological processes, or it may be an adaptive response to the physiological demands associated with migration, such as high energetic demands and the negative consequences of a hyperactive immune system.     

Immune response is energetically costly in white cabbage butterfly pupae

Parasite-driven coevolution has led hosts to develop a complicated and potentially costly defence machinery, consisting mainly of the immune system. Despite the evidence for the trade-offs between immune function and life-history traits, it is still obscure how the costs of using and maintaining the immune function are paid. We tested whether immune challenge is energetically costly for white cabbage butterfly (Pieris brassicae L.) diapausing pupa. Individuals challenged with nylon implant raised their standard metabolic rate nearly 8% compared to the controls. Hence, costs of activation of immune system in insect pupa can be expressed in energetic currency.     

A pre‐breeding immune challenge delays reproduction in the female dark‐eyed junco Junco hyemalis

Precise timing of life‐history transitions in predictably changing environments is hypothesized to aid in individual survival and reproductive success, by appropriately matching an animal's physiology and behavior with prevailing environmental conditions. Therefore, it is imperative for individuals to time energetically costly life‐history stages (i.e. reproduction) so they overlap with seasonal peaks in food abundance and quality. Female lifetime reproductive fitness is affected by several factors that influence energy balance, including arrival date, timing of egg production, and energetic condition. Therefore, any extra energetic costs during reproduction may negatively affect timing of egg production, and ultimately a female's fitness. For example, mounting an immunological response elicits a high energetic cost, and this transfer of resources towards cell and immune system maintenance could have direct negative effects on reproductive timing. In order to determine whether an immune challenge delays onset of breeding (i.e. egg production), we administered either a humoral immune challenge (keyhole limpet hemocyanin (KLH)) (treatment) or physiological saline (control) to free‐living female dark‐eyed juncos Junco hyemalis in the period immediately prior to egg‐laying (～4 weeks). We found that KLH‐injected females artificially delayed clutch initiation when compared to control females. These data help to refine our understanding of how free‐living birds allocate resources between reproduction and self‐maintenance processes during the critical pre‐laying period of the annual cycle.     

The Plasmodium parasite—a ‘new’ challenge for insect innate immunity

Though lacking adaptive immunity, insects possess a powerful innate immune system, a genome-encoded defence machinery used to confront infections. Studies in the fruit fly Drosophila melanogaster revealed a remarkable capacity of the innate immune system to differentiate between and subsequently respond to different bacteria and fungi. However, hematophagous compared to non-hematophagous insects encounter additional blood-borne infectious agents, such as parasites and viruses, during their lifetime. Anopheles mosquitoes become infected with the malaria parasite Plasmodium during feeding on infected human hosts and may then transmit the parasite to new hosts during subsequent bites. Whether Anopheles has developed mechanisms to confront these infections is the subject of this review. Initially, we review our current understanding of innate immune reactions and give an overview of the Anopheles immune system as revealed through comparative genomic analyses. Then, we examine and discuss the capacity of mosquitoes to recognize and respond to infections, especially to Plasmodium, and finally, we explore approaches to investigate and potentially utilize the vector immune competence to prevent pathogen transmission. Such approaches constitute a new challenge for insect immunity research, a challenge for global health.     

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.     

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.     

A label of health: a previous immune challenge is reflected in the expression of a female plumage trait

Studies of ornaments as indicators of individual quality have hitherto focused on males, while studies of female ornaments have been almost absent. However, females within the same species may show large variation in both outer appearance and individual quality. We experimentally examined the effect of an immune challenge on the size of white fringes in the wing feathers produced one to two months after the challenge in female common eiders (Somateria mollissima), a long-lived sea duck. Immune-challenged females produced feathers with smaller white fringes, showing that a previous immune challenge may affect the expression of a plumage trait. We also report an unexpected difference in the expression of this white plumage trait within the immune-challenged group, related to the specific immune response against one of the injected antigens.     

Identity,prevalence and intensity of infestation with wing feather mites on birds (Passeriformes) from the Setubal Peninsula of Portugal

The results of a 4 year project investigating species of mites infesting wing primary feathers on 21 species of Passeriformes are reported. The majority of species were identified as belonging to the genus Proctophyllodes Robin, 1877 with one new host record. In addition Pteronyssoides obscurus Berlese 1884 was found on European swallows, also a new host record. A novel method to enable quantification of mite intensities without causing harm to the birds was devised and evaluated. This relied on visual inspection of wing primary feathers and assignment of subjective infestation scores to individual feathers, the sum of the individual scores comprising the primary feather total mite infestation score (PTMIS). Comparisons between species revealed that birds could be grouped into four categoris depending on their infestation intensity with mites. Swallows, sand martins and greenfinches showed the highest prevalence and most intense infestations (mean PTMIS 6.8). Blackbirds, blackcaps, serins, goldfinches, Cetti's warblers, great tits and house sparrows showed moderate levels of infestation with prevalence in the range 60–90.9% but a mean PTMIS lower than in the former group (1.6–5.8). The third group comprised Sardinian warblers, nightingales and short-toed tree creepers and was characterized by a prevalence of mites 40% and a mean PTMIS of 0.6–1.4. The final group, representing wrens, chiffchaffs, fan-tailed warblers and waxbills were without detectable mites, the only exception being wrens on which mites were identified in only three birds of the 32 sampled. These results are interpreted in the light of published information and possible explanations for the observations are discussed.     

Hohe Steuerfederverluste beim Neunt?terLanius collurio: Handelt es sich um eine sommerliche Mauser?

Zusammenfassung 33% der in der Brutsaison in Südwestdeutschland gefangenen Neuntöter besaßen lückenhafte Schwänze. Vögel mit mehreren defekten Steuerfedern waren häufiger als statistisch erwartet. Die inneren S1 gingen häufiger verloren und wurden langsamer ersetzt als die anderen. Von Mai bis Juli gefangene Neuntöter besaßen mehr fehlende als wachsende Steuerfedern. Ein Teil der verlorenen Schwanzfedern wird — besonders im Juli — erst verzögert während der postnuptialen Körpergefiedermauser erneuert. Weder bei den Brutvögeln noch bei Junggesellen wurden Hinweise auf eine reguläre sommerliche Steuerfedermauser gefunden. Selbst abgebrochene Federn werden nicht ersetzt. Es wird vermutet, daß Würger und andere Arten, die in dichter Vegetation leben oder jagen, schwach befestigte Steuerfedern als Schutz gegen das Hängenbleiben besitzen.

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Frequent losses of rectrices in Red-Backed ShrikesLanius collurio: Is it a matter of a summer moult?

33% of the Red-backed Shrikes controlled in Southwest Germany during breeding season had tails with deficiencies. Birds with several defective rectrices are more frequent as statistically expected. The innermost R1 were lost more frequently than the others and were more slowly regenerated. From May to July, birds had more missing feathers than growing ones. A part of the lost rectrices, especially in July, is replaced retarded, often during postnuptial moult of body feathers. There are no hints for a regulary moult of tail feathers, neither in breeding birds nor in bachelors. Even broken feathers are not replaced. It is supposed that shrikes and other bird species living or hunting in dense vegetation have rectrices, which they lose easily; this may be an adaption against adherence.

     

Metabolic consequences of overlapping food restriction and cell‐mediated immune response in a long‐distance migratory shorebird,the little ringed plover Charadrius dubius

Investment in immunity is commonly viewed as an energetically costly activity in birds. Although several studies have focused on the energy cost of mounting an immune response and its concomitant physiological trade‐offs, nothing is known about the metabolic adjustments experienced by immunochallenged birds under resource limitation, or about the basal metabolism cost of mounting cell‐mediated immune (CMI) responses in bird species other than non‐migratory passerines. Here we measured the basal metabolic rate (BMR), inflammatory response, and body mass in ad libitum fed and food‐restricted little ringed plovers Charadrius dubius challenged with phytohemagglutinin (PHA) in order to assess the energy cost, the strength, and the time course of the CMI response in a long‐distance migratory bird in different nutritional states. We found that ad libitum birds injected with PHA significantly increased both mass‐independent BMR and inflammatory response, whereas birds with an induced food restriction‐immune response overlap experienced a mass‐independent BMR downregulation and decreased inflammatory response relative to ad libitum birds. We suggest that both the BMR downregulation and the diminished inflammatory response observed in birds facing such an overlap could be energy‐saving mechanisms to maintain the body mass above a critical level and maximize fitness.     

Immune deployment increases larval vulnerability to predators and inhibits adult life‐history traits in a dragonfly

While deploying immune defences early in ontogeny can trade‐off with the production and maintenance of other important traits across the entire life cycle, it remains largely unexplored how features of the environment shape the magnitude or presence of these lifetime costs. Greater predation risk during the juvenile stage may particularly influence such costs by (1) magnifying the survival costs that arise from any handicap of juvenile avoidance traits and/or (2) intensifying allocation trade‐offs with important adult traits. Here, we tested for predator‐dependent costs of immune deployment within and across life stages using the dragonfly, Pachydiplax longipennis. We first examined how larval immune deployment affected two traits associated with larval vulnerability to predators: escape distance and foraging under predation risk. Larvae that were induced to mount an immune response had shorter escape distances but lower foraging activity in the presence of predator cues. We also induced immune responses in larvae and reared them through emergence in mesocosms that differed in the presence of large predatory dragonfly larvae (Aeshnidae spp.). Immune‐challenged larvae had later emergence overall and lower survival in pools with predators. Immune‐challenged males were also smaller at emergence and developed less sexually selected melanin wing coloration, but these effects were independent of predator treatment. Overall, these results highlight how mounting an immune defence early in ontogeny can have substantial ecological and physiological costs that manifest both within and across life stages.     

Growth, developmental stability and immune response in juvenile Japanese quails (Coturnix coturnix japonica).

Stresses are environmental factors which restrict growth or cause a potentially adverse change in an organism. The exposure of developing organisms to environmental stresses may have several physiological consequences including a decrease in immunocompetence. However, mounting an immune response against a foreign antigen may in itself constitute a cost for developing organisms. This cost has potentially long-term consequences for adult function and fitness. This study examines the growth and developmental stability of Japanese quail++ chicks challenged by three non-pathogenic antigens: sheep red blood cells, which assess T-cell-dependent immune responses, and Mycoplasma synoviae and Newcastle disease virus, which assess T-cell-independent responses. Increases in both body mass and wing length were significantly reduced in antigen-challenged birds compared to control birds. Fluctuating asymmetry (FA) in the masses of primary feathers increased from the innermost (1) to the outermost (10) position on the wing. In addition, antigen challenge by M. synoviae and sheep red blood cells was associated with an increase in FA. The cell-mediated response measured by reaction to phytohaemagglutinin was significantly depressed in M. synoviae-challenged birds. White blood cell counts, except for monocytes, were elevated in response to all three antigen treatments. Total plasma protein and haematocrit also differed between treatments but exhibited no clear relationship to antigen challenge. Immune responses clearly impose a stress on developing chicks. Additional research will be required to determine the long-term consequences of developmental stress and assess the selective forces that influence the strength of the immune responses of chicks.     

Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect

1.?When parasitized, both vertebrates and invertebrates can enhance the immune defence of their offspring, although this transfer of immunity is achieved by different mechanisms. In some insects, immune-challenged males can also initiate trans-generational immune priming (TGIP), but its expressions appear qualitatively different from the one induced by females similarly challenged. 2.?The existence of male TGIP challenges the traditional view of the parental investment theory, which predicts that females should invest more into their progeny than males. However, sexual dimorphism in life-history strategies and the potential costs associated with TGIP may nevertheless lead to dissymmetric investment between males and females into the immune protection of the offspring. 3.?Using the yellow mealworm beetle, Tenebrio molitor, we show that after parental exposure to a bacterial-like infection, maternal and paternal TGIP are associated with the enhancement of different immune effectors and different fitness costs in the offspring. While all the offspring produced by challenged mothers had enhanced immune defence, only those from early reproductive episodes were immune primed by challenged fathers. 4.?Despite the fact that males and females may share a common interest in providing their offspring with an immune protection from the current pathogenic threat, they seem to have evolved different strategies concerning this investment.     

Using stable isotopes to investigate the dietary trophic level of fledgling songbirds

ABSTRACT Use of early successional habitat by mature forest birds during the postfledging period is well documented, but reasons for this habitat shift remain elusive. Although forest‐breeding songbirds are primarily insectivorous during the nestling and early fledgling periods due to high protein requirements, older fledglings may adopt a heavily frugivorous diet. Our objectives were to use stable isotopes to examine the dietary trophic level of juveniles of three species of mature forest songbirds to determine if juvenile songbirds heavily consume fruit resources during the postfledging period and to evaluate a possible link between diet and energetic condition. We collected the outer right rectrix and several body feathers from 34 Wood Thrushes (Hylocichla mustelina), 34 Ovenbirds (Seiurus aurocapilla), and 35 Scarlet Tanagers (Piranga olivacea) captured in regenerating clearcuts in southeastern Ohio in 2005 and 2006. We also collected fruit and arthropod samples from each clearcut. Isotopic values of body feathers were significantly higher (more enriched) than those of rectrices in all cases except values of δ¹³C for Ovenbirds where we found no difference between body and rectrix feathers. These results suggest that juvenile songbirds did not undergo a strong shift to frugivory during the postfledging period, and arthropods were the primary source of protein during the period when rectrix and body feathers were growing. In addition, the energetic condition of birds was not related to the isotopic signature of feathers. Although our results are inconsistent with the hypothesis that juveniles move into regenerating clearcuts enabling them to shift to a primarily frugivorous diet during the postfledging period, they may consume fruit for nonprotein requirements, such as lipids and carbohydrates.     

Two estimates of the metabolic costs of antibody production in migratory shorebirds: low costs, internal reallocation, or both?

We measured the costs of mounting a humoral immune response using two novel antigens (tetanus and diphtheria) in two shorebird species (Scolopacidae): Red Knot (Calidris canutus, measured in autumn) and Ruff (Philomachus pugnax, measured in spring). Metabolic rate was measured during the preinjection phase, at the building phase of the primary immune response, and at peak secondary immune response by determining the oxygen consumption of the postabsorptive birds at rest. Confirming earlier studies, Red Knots and Ruffs responded with lower antibody titers to the diphtheria than to the tetanus antigen. Although Red Knots and Ruffs produced the same amounts of antibodies, Red Knots showed a significant 13% increase in basal metabolic rate (BMR) during the secondary antibody response, whereas Ruffs showed a 15%, but only marginally significant, reduction in BMR. The results from this study suggest that the energetic costs of an immune response may be small, but the "negative cost" in Ruffs hints at the possibility of resource reallocation and the concomitant difficulty of measuring such costs during "basal" metabolic rate measurements.     

Energetic trade-offs between immunity and reproduction in male Japanese quail (Coturnix coturnix)

We investigated a postulated trade-off between reproduction and immune function by comparing the energetic costs of an immune response with phytohemagglutinin challenge (or injection) in castrated (low testosterone [T]) and intact (high T) Japanese Quail (Coturnix coturnix). Intact birds had higher resting metabolic rate (RMR) and significantly lower immune response than castrates. RMR of intact birds did not change in response to an immune challenge, suggesting that maintenance of reproductive tissues and associated high T is both immunosuppressive and energetically costly. Despite having a greater immune response than intact quail, castrates had a lower pre-challenge RMR than intact birds and paradoxically tended to decrease RMR during an immune challenge. This paradox may be because of pro-inflammatory cytokines that are released during immune responses. Cytokines promote energy conservation through malaise and soporific behaviors, possibly explaining the co-occurrence of a relatively strong immune response and a decrease in nocturnal RMR in castrates. The lower immune response in intact birds may not elicit as great a response of pro-inflammatory cytokines owing to an already elevated RMR from reproductive state, thus reducing any effect on RMR. The suppressed immune response and elevated RMR in intact birds may be because of T; however, we cannot separate the effects of T per se from the metabolic requirements of reproductive tissues.     

Effects of Endotoxin and Psychological Stress on Redox Physiology,Immunity and Feather Corticosterone in Greenfinches

Assessment of costs accompanying activation of immune system and related neuroendocrine pathways is essential for understanding the selective forces operating on these systems. Here we attempted to detect such costs in terms of disruption to redox balance and interference between different immune system components in captive wild-caught greenfinches (Carduelis chloris). Study birds were subjected to an endotoxin-induced inflammatory challenge and temporary exposure to a psychological stressor (an image of a predator) in a 2*2 factorial experiment. Injection of bacterial endotoxin resulted in up-regulation of two markers of antioxidant protection – erythrocyte glutathione, and plasma oxygen radical absorbance (OXY). These findings suggest that inflammatory responses alter redox homeostasis. However, no effect on markers of oxidative damage to proteins or DNA in erythrocytes could be detected. We found no evidence that the endotoxin injection interfered with antibody production against Brucella abortus antigen or the intensity of chronic coccidiosis. The hypothesis of within-immune system trade-offs as a cost of immunity was thus not supported in our model system. We showed for the first time that administration of endotoxin can reduce the level of corticosterone deposited into feathers. This finding suggests a down-regulation of the corticosterone secretion cascade due to an endotoxin-induced immune response, a phenomenon that has not been reported previously. Exposure to the predator image did not affect any of the measured physiological parameters.