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Article: Simulated bacterial infection disrupts the circadian fluctuation of immune cells in wrinkle-lipped bats (Chaerephon plicatus)

Czirják, Gábor Árpád / Lindecke, Oliver

PeerJ, 5:e3570

2017

Abstract: BACKGROUND: Leukocyte concentrations follow a circadian pattern in mammals, with elevated values at times of potential contact with pathogens and parasites. We hypothesized that this pattern is disturbed after an immune challenge. METHODS: In Thailand, ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	BACKGROUND: Leukocyte concentrations follow a circadian pattern in mammals, with elevated values at times of potential contact with pathogens and parasites. We hypothesized that this pattern is disturbed after an immune challenge. METHODS: In Thailand, we captured wrinkle-lipped bats (Chaerephon plicatus), when they returned to their colony at dawn. We challenged half of the animals (experimental group) with bacterial lipopolysaccharides and treated the others only with the carrier liquid (control group). We then compared body mass changes and differences in circulating immune cell counts at 8 h post-treatment. RESULTS: In experimental animals, we observed an increase in total leukocyte and neutrophil numbers of 17% and 95%, respectively. In control animals, concentrations of leukocytes decreased by 44% and those of neutrophils remained constant. Experimental treatment had no effect on lymphocytes, yet changes in eosinophil numbers were explained by sex. Eosinophils decreased by 66% in females and by 62% in males. Basophils and monocytes were rarest among all observed cell types and analysis was either impossible because of low numbers or yielded no significant effects, respectively. DISCUSSION: Our findings show that a simulated bacterial infection triggered a neutrophil-associated immune response in wrinkle-lipped bats, indicating a disruption of the diurnal fluctuation of immune cells. Our study suggests that bats exhibit circadian rhythms in immune cell counts. The magnitude of these fluctuations may vary across species according to specific-specific infection risks associated with colony sizes or specific roosting habits.
Language	English
Document type	Article
Database	Repository for Life Sciences

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Article: Leukocyte profiles reflect geographic range limits in a widespread neotropical bat

Escalera-Zamudio, Marina / Greenwood, Alex / Czirják, Gábor Árpád

Integrative and comparative biology, 59(5):1176-1189

2019

Abstract: Quantifying how the environment shapes host immune defense is important for understanding which wild populations may be more susceptible or resistant to pathogens. Spatial variation in parasite risk, food and predator abundance, and abiotic conditions ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	Quantifying how the environment shapes host immune defense is important for understanding which wild populations may be more susceptible or resistant to pathogens. Spatial variation in parasite risk, food and predator abundance, and abiotic conditions can each affect immunity, and these factors can also manifest at both local and biogeographic scales. Yet identifying predictors and the spatial scale of their effects is limited by the rarity of studies that measure immunity across many populations of broadly distributed species. We analyzed leukocyte profiles from 39 wild populations of the common vampire bat (Desmodus rotundus) across its wide geographic range throughout the Neotropics. White blood cell differentials varied spatially, with proportions of neutrophils and lymphocytes varying up to six-fold across sites. Leukocyte profiles were spatially autocorrelated at small and very large distances, suggesting that local environment and large-scale biogeographic factors influence cellular immunity. Generalized additive models showed that bat populations closer to the northern and southern limits of the species range had more neutrophils, monocytes, and basophils, but fewer lymphocytes and eosinophils, than bats sampled at the core of their distribution. Habitats with access to more livestock also showed similar patterns in leukocyte profiles, but large-scale patterns were partly confounded by time between capture and sampling across sites. Our findings suggest that populations at the edge of their range experience physiologically limiting conditions that predict higher chronic stress and greater investment in cellular innate immunity. High food abundance in livestock-dense habitats may exacerbate such conditions by increasing bat density or diet homogenization, although future spatially and temporally coordinated field studies with common protocols are needed to limit sampling artifacts. Systematically assessing immune function and response over space will elucidate how environmental conditions influence traits relevant to epidemiology and help predict disease risks with anthropogenic disturbance, land conversion, and climate change.
Keywords	blood ; disease ; ecological immunology ; expression ; immune function ; stress ; parasite infection ; responses ; vampire bats ; vertebrates
Language	English
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Database	Repository for Life Sciences

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Article: Comprehensive Serology Based on a Peptide ELISA to Assess the Prevalence of Closely Related Equine Herpesviruses in Zoo and Wild Animals

Czirják, Gábor Árpád / Greenwood, Alex

PLOS ONE, 10(9): e0138370

2015

Abstract: Equine herpesvirus type 1 (EHV-1) causes respiratory disorders and abortion in equids while EHV-1 regularly causes equine herpesvirus myeloencephalopathy (EHM), a stroke-like syndrome following endothelial cell infection in horses. Both EHV-1 and EHV-9 ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	Equine herpesvirus type 1 (EHV-1) causes respiratory disorders and abortion in equids while EHV-1 regularly causes equine herpesvirus myeloencephalopathy (EHM), a stroke-like syndrome following endothelial cell infection in horses. Both EHV-1 and EHV-9 infections of non-definitive hosts often result in neuronal infection and high case fatality rates. Hence, EHV-1 and EHV-9 are somewhat unusual herpesviruses and lack strict host specificity, and the true extent of their host ranges have remained unclear. In order to determine the seroprevalence of EHV-1 and EHV-9, a sensitive and specific peptide-based ELISA was developed and applied to 428 sera from captive and wild animals representing 30 species in 12 families and five orders. Members of the Equidae, Rhinocerotidae and Bovidae were serologically positive for EHV-1 and EHV-9. The prevalence of EHV-1 in the sampled wild zebra populations was significantly higher than in zoos suggesting captivity may reduce exposure to EHV-1. Furthermore, the seroprevalence for EHV-1 was significantly higher than for EHV-9 in zebras. In contrast, EHV-9 antibody prevalence was high in captive and wild African rhinoceros species suggesting that they may serve as a reservoir or natural host for EHV-9. Thus, EHV-1 and EHV-9 have a broad host range favoring African herbivores and may have acquired novel natural hosts in ecosystems where wild equids are common and are in close contact with other perissodactyls.
Keywords	Antibodies ; Asses ; Enzyme-linked immunoassays ; Equines ; Horses ; Somalian people ; Umbilical cord ; Zebras
Language	English
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Database	Repository for Life Sciences

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Article: Habitat disturbance results in chronic stress and impaired health status in forest-dwelling paleotropical bats

Czirják, Gábor Árpád / Voigt, Christian / Courtiol, Alexandre

Conservation Physiology, 5(1):cox020

2017

Abstract: Anthropogenic habitat disturbance is a major threat to biodiversity worldwide. Yet, before population declines are detectable, individuals may suffer from chronic stress and impaired immunity in disturbed habitats, making them more susceptible to ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	Anthropogenic habitat disturbance is a major threat to biodiversity worldwide. Yet, before population declines are detectable, individuals may suffer from chronic stress and impaired immunity in disturbed habitats, making them more susceptible to pathogens and adverse weather conditions. Here, we tested in a paleotropical forest with ongoing logging and fragmentation, whether habitat disturbance influences the body mass and immunity of bats. We measured and compared body mass, chronic stress (indicated by neutrophil to lymphocyte ratios) and the number of circulating immune cells between several bat species with different roost types living in recovering areas, actively logged forests, and fragmented forests in Sabah, Malaysia. In a cave-roosting species, chronic stress levels were higher in individuals from fragmented habitats compared with conspecifics from actively logged areas. Foliage-roosting species showed a reduced body mass and decrease in total white blood cell counts in actively logged areas and fragmented forests compared with conspecifics living in recovering habitats. Our study highlights that habitat disturbance may have species-specific effects on chronic stress and immunity in bats that are potentially related to the roost type. We identified foliage-roosting species as particularly sensitive to forest habitat deterioration. These species may face a heightened extinction risk in the near future if anthropogenic habitat alterations continue.
Language	English
Document type	Article
Database	Repository for Life Sciences

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Article: Predictors and immunological correlates of sublethal mercury exposure in vampire bats

Becker, Daniel / Bentz, Alexandra / Czirják, Gábor Árpád

Royal Society Open Science, 4:170073

2017

Abstract: Mercury (Hg) is a pervasive heavy metal that often enters the environment from anthropogenic sources such as gold mining and agriculture. Chronic exposure to Hg can impair immune function, reducing the ability of animals to resist or recover from ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	Mercury (Hg) is a pervasive heavy metal that often enters the environment from anthropogenic sources such as gold mining and agriculture. Chronic exposure to Hg can impair immune function, reducing the ability of animals to resist or recover from infections. How Hg influences immunity and susceptibility remains unknown for bats, which appear immunologically distinct from other mammals and are reservoir hosts of many pathogens of importance to human and animal health. We here quantify total Hg (THg) in hair collected from common vampire bats (Desmodus rotundus), which feed on blood and are the main reservoir hosts of rabies virus in Latin America. We examine how diet, sampling site and year, and bat demography influence THg and test the consequences of this variation for eight immune measures. In two populations from Belize, THg concentrations in bats were best explained by an interaction between long-term diet inferred from stable isotopes and year. Bats that foraged more consistently on domestic animals exhibited higher THg. However, relationships between diet and THg were evident only in 2015 but not in 2014, which could reflect recent environmental perturbations associated with agriculture. THg concentrations were low relative to values previously observed in other bat species but still correlated with bat immunity. Bats with higher THg had more neutrophils, weaker bacterial killing ability and impaired innate immunity. These patterns suggest that temporal variation in Hg exposure may impair bat innate immunity and increase susceptibility to pathogens such as bacteria. Unexpected associations between low-level Hg exposure and immune function underscore the need to better understand the environmental sources of Hg exposure in bats and the consequences for bat immunity and susceptibility.
Language	English
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Database	Repository for Life Sciences

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Article: Socioecological and environmental predictors of physiological stress markers in a threatened feline species

Wachter, Bettina / Melzheimer, Joerg / Czirják, Gábor Árpád

Conservation biology, 1(1):cox069

2017

Abstract: In recent years, ecological studies have shown that oxidative status can have a significant impact on fitness components in free-ranging animals. This has raised awareness by conservation practitioners about the importance of identifying the factors ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	In recent years, ecological studies have shown that oxidative status can have a significant impact on fitness components in free-ranging animals. This has raised awareness by conservation practitioners about the importance of identifying the factors associated with individual variation in markers of oxidative status because this might provide several potential benefits for conservation programmes. In this study, we measured five markers of oxidative status in the cheetah (Acinonyx jubatus), a carnivore species classified as vulnerable by the International Union for Conservation of Nature. We asked whether the five measures of oxidative damage and antioxidant blood-based markers are associated with a number of socioecological and environmental factors, including individual sex, age class, living condition (free-ranging vs. captive), restraint duration stress (i.e. capture duration stress), spatial tactic of males (territory holders vs. non-territory holders, i.e. floaters) and reproductive status of females (accompanied by offspring vs. solitary). Markers of oxidative damage were higher in those cheetahs that were physically restraint for a longer duration in the trap, indicating that oxidative stress may be increased by short-term unpredictable environmental stressors. Markers of oxidative damage were also higher in captive than free-ranging cheetahs, suggesting that oxidative stress might be a physiological mechanism underlying the detrimental effects of captivity on the health status of cheetahs. Variation of oxidative status markers was also significantly associated with individual age class, spatial tactic and reproductive status, opening new research avenues about the role of oxidative stress in influencing behavioural and life-history traits in cheetahs.
Keywords	Acinonyx jubatus ; captivity ; cheetah ; ageing ; oxidative stress ; restraint
Language	English
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Database	Repository for Life Sciences

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

Ruiz-González, Mario X. / Czirják, Gábor Árpád / Mousseau, Timothy

Scientific reports, 6:22969

2016

Abstract: 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 ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	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.
Keywords	Evolutionary ecology ; Microbial ecology
Language	English
Document type	Article
Database	Repository for Life Sciences

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Article: Immune response of hibernating European bats to a fungal challenge

Fritze, Marcus / Costantini, David / Fickel, Joerns / Czirják, Gábor Árpád / Voigt, Christian

Biology open, 8:bio046078

2019

Abstract: Immunological responses of hibernating mammals are suppressed at low body temperatures, a possible explanation for the devastating effect of the white-nose syndrome on hibernating North American bats. However, European bats seem to cope well with the ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	Immunological responses of hibernating mammals are suppressed at low body temperatures, a possible explanation for the devastating effect of the white-nose syndrome on hibernating North American bats. However, European bats seem to cope well with the fungal causative agent of the disease. To better understand the immune response of hibernating bats, especially against fungal pathogens, we challenged European greater mouse-eared bats (Myotis myotis) by inoculating the fungal antigen zymosan. We monitored torpor patterns, immune gene expressions, different aspects of the acute phase response and plasma oxidative status markers, and compared them with sham-injected control animals at 30 min, 48 h and 96 h after inoculation. Torpor patterns, body temperatures, body masses, white blood cell counts, expression of immune genes, reactive oxygen metabolites and non-enzymatic antioxidant capacity did not differ between groups during the experiment. However, zymosan injected bats had significantly higher levels of haptoglobin than the control animals. Our results indicate that hibernating greater mouse-eared bats mount an inflammatory response to a fungal challenge, with only mild to negligible consequences for the energy budget of hibernation. Our study gives a first hint that hibernating European bats may have evolved a hibernation-adjusted immune response in order to balance the trade-off between competent pathogen elimination and a prudent energy-saving regime.
Keywords	Acute phase response ; Body temperature ; Fungal challenge ; Myotis myotis ; Torpor ; Zymosan
Language	English
Document type	Article
Database	Repository for Life Sciences

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Article: Cheetahs have a stronger constitutive innate immunity than leopards

Hofer, Heribert / Courtiol, Alexandre / Czirják, Gábor Árpád / Wachter, Bettina

Scientific reports, 7:44837

2017

Abstract: As a textbook case for the importance of genetics in conservation, absence of genetic variability at the major histocompatibility complex (MHC) is thought to endanger species viability, since it is considered crucial for pathogen resistance. An ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin)
Abstract	As a textbook case for the importance of genetics in conservation, absence of genetic variability at the major histocompatibility complex (MHC) is thought to endanger species viability, since it is considered crucial for pathogen resistance. An alternative view of the immune system inspired by life history theory posits that a strong response should evolve in other components of the immune system if there is little variation in the MHC. In contrast to the leopard (Panthera pardus), the cheetah (Acinonyx jubatus) has a relatively low genetic variability at the MHC, yet free-ranging cheetahs are healthy. By comparing the functional competence of the humoral immune system of both species in sympatric populations in Namibia, we demonstrate that cheetahs have a higher constitutive innate but lower induced innate and adaptive immunity than leopards. We conclude (1) immunocompetence of cheetahs is higher than previously thought; (2) studying both innate and adaptive components of immune systems will enrich conservation science.
Keywords	Evolution ; Immunology
Language	English
Document type	Article
Database	Repository for Life Sciences

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Article: Plasma proteomic analysis of active and torpid greater mouse-eared bats (Myotis myotis)

Voigt, Christian / Greenwood, Alex / Czirják, Gábor Árpád

Scientific reports, 5:16604

2015

Abstract: Hibernation is a physiological adaptation to overcome extreme environmental conditions. It is characterized by prolonged periods of torpor interrupted by temporary arousals during winter. During torpor, body functions are suppressed and restored rapidly ... ...

Institution	Leibniz-Institut für Zoo- und Wildtierforschung (Berlin) Leibniz-Institut für Molekulare Pharmakologie
Abstract	Hibernation is a physiological adaptation to overcome extreme environmental conditions. It is characterized by prolonged periods of torpor interrupted by temporary arousals during winter. During torpor, body functions are suppressed and restored rapidly to almost pre-hibernation levels during arousal. Although molecular studies have been performed on hibernating rodents and bears, it is unclear how generalizable the results are among hibernating species with different physiology such as bats. As targeted blood proteomic analysis are lacking in small hibernators, we investigated the general plasma proteomic profile of European Myotis myotis and hibernation associated changes between torpid and active individuals by two-dimensional gel electrophoresis. Results revealed an alternation of proteins involved in transport, fuel switching, innate immunity and blood coagulation between the two physiological states. The results suggest that metabolic changes during hibernation are associated with plasma proteomic changes. Further characterization of the proteomic plasma profile identified transport proteins, coagulation proteins and complement factors and detected a high abundance of alpha-fetoprotein. We were able to establish for the first time a basic myotid bat plasma proteomic profile and further demonstrated a modulated protein expression during torpor in Myotis myotis, indicating both novel physiological pathways in bats in general, and during hibernation in particular.
Keywords	Ecophysiology ; Molecular ecology
Language	English
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Database	Repository for Life Sciences

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