Lower adaptive immunity in invasive Egyptian geese compared to sympatric native waterfowls.

Successful invasive species increase their spreading success by trading-off nutritional and metabolic resources allocated to reproduction and range expansion with other costly body functions. One proposed mechanism for the reallocation of resources is a trade-off with the immune function and the regulation of oxidative status. Relying on a panel of blood-based markers of immune function and oxidative status quantified in an invasive species (Egyptian goose) and two native competing species (mallard and mute swan) in Germany, we tested the hypothesis that the invasive species would have (i) lower investment in immune function, (ii) lower levels of oxidative damage, and (iii) no higher antioxidant defences compared to the native species. We found lower levels of adaptive immune markers (lymphocytes and immunoglobulin Y), in the invasive species compared to the two native species. Innate immune profile was generally similar between Egyptian geese and mallards. By contrast, mute swans showed higher levels of heterophils and lysozymes, and lower levels of bacteria killing ability compared to both Egyptian geese and mallards. Mute swans also showed higher levels of haemolysis and haemagglutination, but lower levels of monocytes and haematocrit compared to Egyptian geese. Reactive oxygen metabolites, a marker of oxidative damage, were higher in mallards and lower in Egyptian geese compared to the other waterfowl species, while levels of antioxidants were generally similar among the three species. Our results point to a reduced investment in adaptive immune function in the invasive species as a possible resources-saving immunological strategy due to the loss of co-evolved parasites in the new colonised habitats, as observed in a previous study. A lower investment in immune function may benefit other energy-demanding activities, such as reproduction, dispersal, and territoriality, while maintaining relatively higher innate immunity is beneficial since invasive species mainly encounter novel pathogens. Results pointed out also other important species-specific differences in baseline immune status, supporting previous findings on the relationship between species' body mass and immune profile.

Age-specific gastrointestinal parasite shedding in free-ranging cheetahs (Acinonyx jubatus) on Namibian farmland.

The cheetah (Acinonyx jubatus Brookes 1828) is classified as "vulnerable" by the International Union for Conservation of Nature (IUCN). Threats to cheetah populations are a decrease of suitable habitats, an increase of conflicts with livestock farmers and potentially pathogens. While there is some information on the viral and bacterial pathogens circulating in cheetah populations, information on gastrointestinal parasites is scarce. Here, we investigate the gastrointestinal parasites in 39 free-ranging cheetahs in east-central Namibia using a coproscopical parasitological method. Most cheetahs (82%) shed eggs from Ancylostoma which comprised the majority of the total eggs in feces. Eggs and oocysts from Toxascaris (21% of cheetahs), Coccidia (13%), Physaloptera (8%), Taeniidae (5%), Dipylidium (3%), and Diphyllobothriidae (3%) were present at a lower prevalence. Parasite richness and Ancylostoma egg load were higher in juveniles and adults compared to cubs, but were not associated with sex. To our knowledge, this is the first study that assessed gastrointestinal parasites in free-ranging cheetahs and is a key starting point for future studies on the effect of parasites in this threatened species.

Feather bacterial load shapes the trade-off between preening and immunity in pigeons.

BACKGROUND: Complex communities of bacteria inhabit the feathers of all birds. Under normal conditions, individuals maintain a healthy state by defending themselves against these potential invaders by preening. The immune system is only triggered when bacteria gain access into the body. Preening is, however, costly and may trade-off with investment in the immune system. To shed light on how birds balance the trade-off between immunity and preen secretions when facing high or low feather bacterial load, we experimentally manipulated feather bacteria load of feral pigeons (Columba livia), and investigated the effects on immune defenses. RESULTS: Birds facing high feather bacterial load had lower immune response to PHA skin-swelling test (a measure of induced pro-inflammatory capacity) than controls, while birds facing low feather bacterial load had higher blood bacterial killing ability (a measure of the capacity to eliminate bacterial pathogens) than controls. No other components of the immune system (i.e., hemagglutination and hemolysis capacity of plasma, primary and secondary responses to KLH and quantity of blood parasites) were found to be affected by feather bacterial load. CONCLUSION: Pigeons had previously been shown to adjust preening to feather bacterial load. The decrease in the energetically costly inflammatory response of birds experiencing high bacterial load suggests a trade-off between investment in preen secretion and immunity and reinforces the idea that feather microbiota may have a strong impact on the ecology and evolution of the avian host.

Physiological pace of life: the link between constitutive immunity, developmental period, and metabolic rate in European birds.

Constitutive innate immunity is the first lined of defence against infections, but the causes determining its variability among species are poorly understood. The pace of life hypothesis predicts that species with a fast speed of life, characterized by high energy turnover and short developmental time, invest relatively little in defence in favour of growth and early reproduction, whereas 'slow-living' species are predicted to invest more resources into costly defence. We conducted phylogenetic comparative analysis on 105 European bird species and determined that the number of leukocytes, and the levels of natural antibodies (NAbs) and complement, measured on adult birds, increased or tended to positively correlate with the length of incubation period. However, we found that the length of incubation and fledging periods have opposite effects on immune defence (i.e. immune parameters show a negative association with the length of fledging period). Our results suggest that the contrasting effects of the incubation and fledging periods are related to the timing of the development of immune cells and of NAbs and complement, which largely mature during the embryonic phase of development. In support of this hypothesis, we found that species with a long relative incubation period [i.e. whose total pre-fledging developmental time (incubation plus fledging) consists largely of the incubation period] invested more in constitutive innate immunity. Finally, in support of the pace of life hypothesis, for a subsample of 63 species, we found that the basal metabolic rate significantly or tended to negatively correlate with immune measures.

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.

Sexual ornamentation reflects antibacterial activity of ejaculates in mallards.

Bacteria present in ejaculates can impair sperm function and reduce male reproductive success. Thus, selection should favour the evolution of antimicrobial defences to limit the detrimental effects of sperm-associated bacteria. Additionally, current hypotheses suggest that ornamental traits may signal information about the infection status of an individual or the ability of an individual to resist bacterial-induced sperm damage. However, despite the evolutionary implications of ejaculate antimicrobials, and the putative importance of pathogens for the evolution of male ornamentation, tests of these hypotheses are lacking. We examined the antibacterial activity of semen from mallard ducks (Anas platyrhynchos) and tested whether the bactericidal capacity of semen was associated with bill coloration, a sexually selected trait. We show that mallard semen exhibits significant antibacterial activity, as measured by the in vitro capacity to kill Escherichia coli and Staphylococcus aureus. Furthermore, we demonstrate that males with more colourful bills have semen with superior bacterial-killing ability. These results suggest that females could use male phenotypic traits to avoid sexually transmitted pathogens and acquire partners whose sperm suffer less bacteria-induced damage.

GPS Telemetry Reveals a Zebra With Anthrax as Putative Cause of Death for Three Cheetahs in the Namib Desert.

Anthrax is a bacterial disease caused by Bacillus anthracis that affects wildlife, livestock and also humans in different parts of the world. It is endemic in some parts of Africa, including Namibia, with species differing in their susceptibility to the disease. Carnivores are typically less susceptible to anthrax than herbivores. Most carnivore species survive infection and have high seroprevalence against anthrax, whereas most herbivore species have low seroprevalence and typically die quickly when infected. Several reports have shown that cheetahs, unlike most other large carnivores, are susceptible to anthrax leading to a sudden death. This finding was suggested to be linked to the low genetic variability of cheetahs which might reduce an adequate immune response and thus explain such a high susceptibility to the disease. Here, we report an incidence of three free-ranging cheetahs that died within 24 h after feeding on a mountain zebra that tested positive for anthrax in the Namib Desert. We were able to reconstruct this incidence with the data recorded in the GPS (Global Positioning System) collar worn by one of the cheetahs and retrieved in the field. It is very likely that the cheetahs died from anthrax, although Bacillus anthracis could not be isolated from tissue and soil samples by bacterial culturing. The mountain zebra is the first described case of a wild animal that tested positive for anthrax in this arid area in southwestern of Namibia. We discuss the negative laboratory results of the cheetahs in the light of new insights of their immune system and its potential to mount a response against this bacteria.

Microorganisms associated with feathers of barn swallows in radioactively contaminated areas around chernobyl.

The Chernobyl catastrophe provides a rare opportunity to study the ecological and evolutionary consequences of low-level, environmental radiation on living organisms. Despite some recent studies about negative effects of environmental radiation on macroorganisms, there is little knowledge about the effect of radioactive contamination on diversity and abundance of microorganisms. We examined abundance patterns of total cultivable bacteria and fungi and the abundance of feather-degrading bacterial subset present on feathers of barn swallows (Hirundo rustica), a colonial migratory passerine, around Chernobyl in relation to levels of ground level environmental radiation. After controlling for confounding variables, total cultivable bacterial loads were negatively correlated with environmental radioactivity, whereas abundance of fungi and feather-degrading bacteria was not significantly related to contamination levels. Abundance of both total and feather-degrading bacteria increased with barn swallow colony size, showing a potential cost of sociality. Males had lower abundance of feather-degrading bacteria than females. Our results show the detrimental effects of low-level environmental radiation on total cultivable bacterial assemblage on feathers, while the abundance of other microorganism groups living on barn swallow feathers, such as feather-degrading bacteria, are shaped by other factors like host sociality or host sex. These data lead us to conclude that the ecological effects of Chernobyl may be more general than previously assumed and may have long-term implications for host-microbe interactions and overall ecosystem functioning.

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.

Increased immune marker variance in a population of invasive birds.

Immunity and parasites have been linked to the success of invasive species. Especially lower parasite burden in invasive populations has been suggested to enable a general downregulation of immune investment (Enemy Release and Evolution of Increased Competitive Ability Hypotheses). Simultaneously, keeping high immune competence towards potentially newly acquired parasites in the invasive range is essential to allow population growth. To investigate the variation of immune effectors of invasive species, we compared the mean and variance of multiple immune effectors in the context of parasite prevalence in an invasive and a native Egyptian goose (Alopochen aegyptiacus) population. Three of ten immune effectors measured showed higher variance in the invasive population. Mean levels were higher in the invasive population for three effectors but lower for eosinophil granulocytes. Parasite prevalence depended on the parasite taxa investigated. We suggest that variation of specific immune effectors, which may be important for invasion success, may lead to higher variance and enable invasive species to reduce the overall physiological cost of immunity while maintaining the ability to efficiently defend against novel parasites encountered.

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

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.

Resistance of Feather-Associated Bacteria to Intermediate Levels of Ionizing Radiation near Chernobyl.

Ionizing radiation has been shown to produce negative effects on organisms, although little is known about its ecological and evolutionary effects. As a study model, we isolated bacteria associated with feathers from barn swallows Hirundo rustica from three study areas around Chernobyl differing in background ionizing radiation levels and one control study site in Denmark. Each bacterial community was exposed to four different γ radiation doses ranging from 0.46 to 3.96 kGy to test whether chronic exposure to radiation had selected for resistant bacterial strains. Experimental radiation duration had an increasingly overall negative effect on the survival of all bacterial communities. After exposure to γ radiation, bacteria isolated from the site with intermediate background radiation levels survived better and produced more colonies than the bacterial communities from other study sites with higher or lower background radiation levels. Long-term effects of radiation in natural populations might be an important selective pressure on traits of bacteria that facilitate survival in certain environments. Our findings indicate the importance of further studies to understand the proximate mechanisms acting to buffer the negative effects of ionizing radiation in natural populations.

Hemorrhagic stomatitis in a natural hybrid of Vipera ammodytes × Vipera berus due to inappropriate substrate in terrarium.

A natural hybrid of Vipera ammodytes × Vipera berus was presented having low body weight, seizures and generalized swelling of the cephalic region. Based on the history of the case and clinical examination, hemorrhagic stomatitis of traumatic origin was diagnosed. The snake was kept in a terrarium with wood chips as a substrate, and the material had induced trauma in the oral mucosa which was further complicated with Salmonella Arizonae and Morganella morganii co-infection, abscessation and osteomyelitis. To the best of the authors' knowledge, this is the first reported case of bacterial infection in European snake hybrids and one of a few case reports in European snakes. Although wood chips are an inexpensive substrate, based on our findings, they should be avoided when keeping and breeding European vipers.

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.