The costs of immunological challenge to developing mountain chickadees, Poecile gambeli, in the wild

The tradeoff between immunocompetence and development in avian species could have long-term consequences relating to fitness. This study investigated the developmental cost of mounting a humoral immune response in growing mountain chickadees, Poecile gambeli . We immunologically challenged nestling chickadees using nonpathogenic antigens of either Newcastle disease virus vaccine or sheep red blood cells. Body mass, tarsal length, haematocrit, total plasma protein, and survival did not vary significantly between antigen treatment groups and control groups. Developmental stability was assessed using fluctuating asymmetry (FA) between the right and left ninth primary feather length. FA was increased significantly in the antigen-challenged birds. This result indicates that the up-regulation of the humoral immune response was developmentally costly to the nestlings by causing an increase in FA.     

Energetic and developmental costs of mounting an immune response in greenfinches (<Emphasis Type="Italic">Carduelis chloris</Emphasis>)

It is assumed that there is a trade-off between the costs allocated to mounting an immune defence and those allocated to costly functions such as breeding and moulting. The physiological basis for this is that mounting an immune response to pathogen challenge has energetic and/or nutrient costs which may interfere with metabolic processes of the challenged individual. If the energetic costs of mounting an immune response are not too high, animals may face such costs by increasing their acquisition of food energy, suggesting that limited nutrients may be responsible for the costs of immune defence. We assessed the energetic and developmental costs of mounting an immune response in an experiment in captivity with first-year greenfinches (Carduelis chloris) challenged with sheep red blood cells and Brucella abortus. Antibody production against both antigens increased the daily energy expenditure (4.7%) of immune-challenged birds relative to control birds, although the difference was non-significant. We estimated that the maximum effect size supported by the data would be 9.9% higher in immune-challenged birds relative to control birds. We plucked the two outermost rectrices of each bird to assess the effects of the immune challenge on growth of the regenerated feathers. The immune challenge had no significant effect on the length of the regenerated rectrices. However, these feathers were more asymmetric in length in immune-challenged birds than in control birds. Although first-year male greenfinches paid a relatively low energetic cost when mounting an immune response, we suggest that immune-challenged individuals may have paid some costs over the long term based on the increased fluctuating asymmetry in the developing feathers.     

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.     

Brood size and immunity costs in zebra finches Taeniopygia guttata

Birds rearing experimentally enlarged broods have lower antibody responses to a novel antigen, and we tested three hypotheses that could explain this result. We used zebra finches Taeniopygia guttata inoculated with sheep red blood cells (SRBC) as a study system, for which this trade-off was previously demonstrated. 1. Compensatory cellular immunity: The humoral immune response is slow, and removal of SRBC through up-regulated cellular immunity could pre-empt an antibody response. However, cellular immune response to PHA decreased with increasing brood size, allowing rejection of this hypothesis. 2. Costs of antibody-production: Chicks in large broods grow less well, and birds with large broods may allocate resources to chicks instead of antibodies when these are costly. Compared to saline controls, SRBC suppressed metabolic rate in the hours following immunisation, but there was no effect in the following night, or at any time 4 and 8 days later. Fitness costs were measured by repeatedly immunising parents with SRBC while rearing young. Chick growth, parental condition, and subsequent reproduction of the parents were not affected by SRBC. We conclude that the costs of antibody formation cannot explain the trade-off between brood size and antibody responsiveness. 3. Costs of immune system maintenance: Maintaining a system enabling antibody-formation may be very costly, and birds rearing large broods may have down-regulated this system. Based on this hypothesis we predicted that antibody formation would still be reduced in parents rearing large broods when immunised after rearing the chicks. Our results confirmed this prediction, and we suggest that birds rearing large broods have lower antibody responses because they economised on the maintenance costs of the immune system.     

Costs of immunity: immune responsiveness reduces survival in a vertebrate

Immune defences are undoubtedly of great benefit to the host, reducing the impact of infectious organisms. However, mounting immune responses also entails costs, which may be measured by inducing immune responses against artificial infections. We injected common eider (Somateria mollissima) females with three different non-pathogenic antigens, sheep red blood cells (SRBC), diphtheria toxoid and tetanus toxoid, early in their incubation period. In the group of females that mounted a humoral immune response against SRBC, the return rate was only 27%, whereas the group of females that did not mount a response against SRBC had a return rate of 72%. Moreover, responding against diphtheria toxoid when also responding against SRBC led to a further reduction in return rate. These results are repeatable, as the same effect occurred independently in two study years. The severely reduced return rate of females producing antibodies against SRBC and diphtheria toxoid implies that these birds experienced considerably impaired long-term survival. This study thus documents severe costs of mounting humoral immune responses in a vertebrate. Such costs may explain why many organisms suppress immunity when under stress or when malnourished, and why infections may sometimes be tolerated without eliciting immune responses.     

Reproductive state, but not testosterone, reduces immune function in male house sparrows (Passer domesticus)

The immune system requires energetic and nutritional resources to optimally defend organisms against pathogens and parasites. Because resources are typically limited, immune function may require a trade-off with other physiologically demanding activities. Here, we examined whether photoperiodically induced seasonal states (breeding, molting, or nonbreeding) affected the cutaneous immune response of captive male house sparrows (Passer domesticus). To assess immune function in these birds, we injected the mitogen phytohemagglutinin (PHA) into the patagium and measured the resulting wing web swelling. Molting and nonbreeding birds had similar immune responses to PHA injection. However, males in a breeding state showed lower immune responses than both molting and nonbreeding birds even though they did not actually breed. We tested whether this decrease in the PHA swelling response in birds in a breeding state was due to elevated plasma concentrations of testosterone (T) by administering T to birds in a nonbreeding state. Contrary to some evidence in the literature, T did not suppress the response to PHA in house sparrows. Our data show that passerine birds show seasonal modulation in immune function, even in benign environmental conditions. However, even though T is often cited as a strong immunosuppressant, it is not fully responsible for this seasonal modulation.     

Injectable selenium: effect on the primary response of mice (38472).

Sodium selenite administered to mice ip (ca.5 mug Se) enhances the primary immune response to the sheep red blood cell angigen. Enhancement of the primary immune response is greatest when Se is administered prior to or simultaneously with the sheep red blood cell antigen.     

Offspring survival is negatively related to maternal response to sheep red blood cells in zebra finches

The immune system is an important player in individual trade-offs, but what has rarely been explored is how different strategies of investment in immune response may affect reproductive decisions. We examined the relationship between the strength of maternal immune response and offspring viability and immune response in captive zebra finches Taeniopygia guttata. In three independent experiments, the females and subsequently their adult offspring were challenged with sheep red blood cells, and their responses were measured. There was no relationship between offspring immune response and that of their mothers. However, we found offspring survival until adulthood to be negatively related to maternal antibody titers. That effect was consistent among all experiments and apparent despite the fact that we partially cross-fostered newly hatched nestlings between nests of different females. This suggests that the observed effects of maternal immune response is not mediated by potentially altered female rearing abilities. To our knowledge, this is the first study showing the relationship between the strength of the immune response and between-generational fitness costs in birds.     

The secondary immune response of young carp, Cyprinus carpio L., following injection of cortisol

Cyprinus carpio immunized at 9 weeks after hatching with either human gamma globulin or trinitrophenylated sheep red blood cells either fail to respond or respond poorly on secondary exposure at 17 weeks of age. Injection of cortisol either simultaneously with the antigen, or 3 days prior to, or 3 days after antigen, permits the antibody response to proceed upon subsequent challenge. The implication of these results for the ontogeny of the fish immune response is discussed.     

Lipopolysaccharide-induced suppression of the primary immune response to a thymus-dependent antigen.

The immune response to a thymus-dependent antigen was depressed in vivo and in vitro in spleen cells from mice injected with LPS i.p. a few days before challenge with the antigen. Spleen cells from LPS-injected mice could, however, respond with increase DNA synthesis after activation with polyclonal B and T cell activators in vitro. The LPS-activated spleen cells could actively suppress normal cells in their response to the antigen sheep red blood cells. The suppressor cells contained in the LPS-activated spleens were most likely B lymphocytes, and the possible mechanism for their inhibitory function is discussed.     

Experimental Mycoplasma pulmonis infection of rats suppresses humoral but not cellular immune response

Humoral antibody response to sheep red blood cells and cellular immune response to bovine serum albumin were studied in Mycoplasma pulmonis infected, adult, male Sprague-Dawley rats. The hemagglutinating antibody response to sheep red blood cells was evaluated at 0, 3, 5, 7, 14, 21 and 28 days postinfection. Antibody titers during all days postinfection were depressed significantly (p less than 0.05) in infected rats as compared to noninfected controls. Cellular immune responses were evaluated by a delayed hypersensitivity response. Rats were sensitized at 0, 3, 5, 7, 14, 21 or 28 days postinfection with bovine serum albumin and challenged with heat aggregated bovine serum albumin 7 days later. Cell-mediated immune responses in infected rats were not significantly different at any point from controls. These results indicate that M. pulmonis infection in rats suppresses the humoral antibody response to sheep red blood cells, but not the cellular immune response to bovine serum albumin.     

Effects of housing conditions during the rearing and laying period on adrenal reactivity, immune response and heterophil to lymphocyte (H/L) ratios in laying hens

This study was conducted to evaluate the effect of early rearing conditions on physiological, haematological and immunological responses relevant to adaptation and long-term stress in white Leghorn hens with intact beaks housed in furnished cages (FC) or conventional cages (CC) during the laying period. Pullets were cage reared (CR) or litter floor reared (FR). From 16 to 76 weeks of age, hens were housed in FC (eight hens per cage) or in CC (three hens per cage). As measures of long-term stress at the end of the laying period, adrenal reactivity was quantified by assessing corticosterone responses to adrenocorticotropin challenge, and immune response was assessed by measuring antibody responses after immunization with sheep red blood cells (SRBC) and keyhole limpet haemocyanin (KLH). Heterophil to lymphocyte (H/L) ratio was employed as an indicator of stress. Rearing conditions significantly affected anti-SRBC titres (P < 0.0001) and tended to affect H/L ratios (P = 0.07), with the highest values found in FR hens. Layer housing affected H/L ratio (P < 0.01); the highest ratio was found in FR birds housed in FC during the laying period. This study shows that early rearing environment affects immunological indicators that are widely used to assess stress in laying hens. However, while results on H/L ratio indicated that FR birds experienced more stress particularly when they were housed in FC during the laying period, the immune responses to SRBC in FR hens was improved, indicating the opposite. This contradiction suggests that the effects on immune response may have been associated with pathogenic load due to environmental complexity in FR and FC hens rather than stress due to rearing system or housing system per se.     

The relation among gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus)

Abstract We experimentally examined the effect of testosterone on the antibody response to a single immunization with sheep red blood cells in young black-headed gulls. This species performs a number of testosterone-mediated elaborate postural displays in social interactions and breeds in dense colonies in which there is a high likelihood of infectious diseases. In young chicks, only one-third were capable of responding to immunization. In the responding chicks, testosterone enhanced antibody titers. Even when antibody responsiveness was measured >1 mo after the termination of hormonal treatment, antibody responses were enhanced in birds treated with androgen but not estrogen. At 9 mo of age, all birds responded to immunization, but there was no effect of testosterone on antibody titers. In these juveniles, frequency of display behavior was negatively related to changes in body mass, which suggests that displaying is energetically costly. Despite decreased body mass, antibody titers were highest in birds that displayed more frequently. This suggests that displaying signals immunocompetence. The results are discussed in relation to the immunocompetence handicap hypothesis and to what is known of the influence of the bursa of Fabricius and social stress on antibody production.     

Predation on ground-nesting seabirds by island populations of red deer Cervus elaphus and sheep Ovis

On Foula, Shetland, sheep were observed biting off the legs, wings or head of unfledged young Arctic terns. Large numbers of tern chicks and a few Arctic skua chicks were found with amputations characteristic of these attacks by sheep. On Rhum, Inner Hebrides, red deer were watched biting the heads off manx shearwater chicks and occasionally also chewing the shearwaters' legs and wings to excise bone. Killing of birds and the selective ingestion of bone-rich parts by ruminants has not previously been widely documented. It is presumably a response to mineral deficiencies in the vegetation, and it may only occur in rare situations where ruminants feed on mineral-deficient vegetation on which there are dense colonies of ground-nesting birds.     

Effect of highly purified thymus factor on the cellular and humoral indices of immunity in thymectomized mice]

Effect of homogeneous polypeptide thymus factor of mol weight about 5000 (thymarin-III) on cellular and humoral immune responses of thymectomized adult CBA mice was studied. Thymectomy proved to greatly decrease the number of T-cells in the spleen. Accordingly, the capability of these mice to produce both IgM and IgG antibody-forming cells in response to the thymus-dependent antigen (sheep red blood cells) was significantly depressed. Subcutaneous injections of thymarin-III (1 microgram per g of body weight) for 7 days completely restored the T-cell spleen population and normalized the animals' immune response.     

Delayed-type hypersensitivity response in an isogenic murine model of paracoccidioidomycosis

The specific delayed-type hypersensitivity (DTH) response was evaluated in resistant (A/SN) and susceptible (B10.A) mice intraperitoneally infected with yeasts from a virulent (Pb18) or from a non-virulent (Pb265)Paracoccidioides brasiliensis isolates. Both strains of mice were footpad challenged with homologous antigens. Pb18 infected A/SN mice developed an evident and persistent DTH response late in the course of the disease (90th day on) whereas B10.A animals mounted a discrete and ephemeral DTH response at the 14th day post-infection. A/SN mice infected with Pb265 developed cellular immune responses whereas B10.A mice were almost always anergic. Histological analysis of the footpads of infected mice at 48 hours after challenge showed a mixed infiltrate consisting of predominantly mononuclear cells. Previous infection of resistant and susceptible mice with Pb18 did not alter their DTH responses against heterologous unrelated antigens (sheep red blood cells and dinitrofluorobenzene) indicating that the observed cellular anergy was antigen-specific. When fungal related antigens (candidin and histoplasmin) were tested in resistant mice, absence of cross-reactivity was noted. Thus, specific DTH responses againstP. brasiliensis depend on both the host's genetically determined resistance and the virulence of the fungal isolate.Abbreviations DTH delayed-type hypersensitivity - DNFB dinitrofluorobenzene - FN18 Fava Netto's antigen obtained from isolate Pb18 - FN265 Fava Netto's antigen obtained from isolate Pb265 - SRBC sheep red blood cells     

Host alkaloids differentially affect developmental stability and wing vein canalization in cactophilic Drosophila buzzatii

Host shifts cause drastic consequences on fitness in cactophilic species of Drosophila. It has been argued that changes in the nutritional values accompanying host shifts may elicit these fitness responses, but they may also reflect the presence of potentially toxic secondary compounds that affect resource quality. Recent studies reported that alkaloids extracted from the columnar cactus Trichocereus terscheckii are toxic for the developing larvae of Drosophila buzzatii. In this study, we tested the effect of artificial diets including increasing doses of host alkaloids on developmental stability and wing morphology in D. buzzatii. We found that alkaloids disrupt normal wing venation patterning and affect viability, wing size and fluctuating asymmetry, suggesting the involvement of stress–response mechanisms. Theoretical implications are discussed in the context of developmental stability, stress, fitness and their relationship with robustness, canalization and phenotypic plasticity.     

Alterations in immune responses in prenatally irradiated dogs

Immunologic responses were studied in beagle dogs following prenatal (35 days gestation) irradiation to evaluate the effects of ionizing radiation on the developing immune system. Each dog received 1.5 Gy 60Co gamma irradiation or sham irradiation. Prenatally irradiated dogs exhibited a significant reduction in primary humoral antibody responses to inoculated sheep red blood cells, a T-dependent antigen, and a concurrent decrease in T-helper lymphocyte subpopulations in the peripheral blood at 3 to 4 months of age. Similarly, irradiated fetuses have been shown to have defects in epitheliostromal development of the thymus. It is suggested that the postnatal immunologic deficits may relate to the prenatal thymic injury.     

Experimental avian aspergilosis

One-day-old chicks were infected by aerosolized conidia ofAspergillus fumigatus orA. flavus. Plaques containing viable organisms were observed on the third day of infection. Although plaques persisted for several weeks, cultures could not be recovered from them after about ten days. Flourescent antibody methods revealed an immune response to both agents within three days of challenge. Precipitin titers againstAspergillus active protein (AAP) did not appear until the tenth day, and was not detected after seven weeks. Aspergillus polysaccharide (APS) failed to react antigenically in infected birds. AAP was separated by Sephadex chromatography into nine distinct fractions. One fraction from each species was associated with an immediate and one with a delayed type of skin response in wattles. A low molecular weight fraction which lacked skin reactivity was an effective antigen in precipitin tests. Except for a weak skin reaction toA. fumigatus APS in rabbits, skin tests with extracts and APP fractions correlated with wattle reactions in chicks.     

Inhibition of the immune response by membrane-bound antibody.

Cells from the spleens of "normal" swine, which were pretreated with pronase to remove surface membrane-bound immunoglobulin, gave an enhanced hemolytic plaque-forming cell response to sheep red blood cells in vitro in comparison with untreated controls. The enhancement could be abrogated by preincubating pronase-treated spleeen cells in preparations containing antibody to sheep red blood cells. This effect was demonstrated by autologous sera, immune sera, and all three known classes of porcine serum immunoglobulins, including IgM, IgA, and IgG and could be removed by absorption with sheep red blood cells. Surface membrane-bound antibody exerted its effect by binding to the nonadherent cell population. The response of normal spleen cells was unaffected by antibody treatment. Pronase-treatment was not mitogenic, did not function as a polyclonal B cell activator, and did not selectively eliminate T or B cells. The results indicate that removal of antibody from the surface of lymphoid cells enhanced the humoral immune response invitro and confirm that membrane-bound antibody can inhibit response to antigen.