How Birds During Migration Maintain (Oxidative) Balance

Animals dynamically adjust their physiology and behavior to survive in changing environments, and seasonal migration is one life stage that demonstrates these dynamic adjustments. As birds migrate between breeding and wintering areas, they incur physiological demands that challenge their antioxidant system. Migrating birds presumably respond to these oxidative challenges by up-regulating protective endogenous systems or accumulating dietary antioxidants at stopover sites, although our understanding of the pre-migration preparations and mid-migration responses of birds to such oxidative challenges is as yet incomplete. Here we review evidence from field and captive-bird studies that address the following questions: (1) Do migratory birds build antioxidant capacity as they build fat stores in preparation for long flights? (2) Is oxidative damage an inevitable consequence of oxidative challenges such as flight, and, if so, how is the extent of damage affected by factors such as the response of the antioxidant system, the level of energetic challenge, and the availability of dietary antioxidants? (3) Do migratory birds ‘recover’ from the oxidative damage accrued during long-duration flights, and, if so, does the pace of this rebalancing of oxidative status depend on the quality of the stopover site? The answer to all these questions is a qualified ‘yes’ although ecological factors (e.g., diet and habitat quality, geographic barriers to migration, and weather) affect how the antioxidant system responds. Furthermore, the pace of this dynamic physiological response remains an open question, despite its potential importance for shaping outcomes on timescales ranging from single flights to migratory journeys. In sum, the antioxidant system of birds during migration is impressively dynamic and responsive to environmental conditions, and thus provides ample opportunities to study how the physiology of migratory birds responds to a changing and challenging world.

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Flight and dietary antioxidants influence antioxidant expression and activity in a migratory bird

Integrative Organismal Biology ◽

10.1093/iob/obab035 ◽

2021 ◽

Author(s):

Kristen J DeMoranville ◽

Wales A Carter ◽

Barbara J Pierce ◽

Scott R McWilliams

Keyword(s):

Transcription Factors ◽

Antioxidant Enzymes ◽

Antioxidant System ◽

Ecological Factors ◽

Antioxidant Enzyme Activities ◽

Antioxidant Protection ◽

Dietary Antioxidants ◽

Antioxidant Genes ◽

Oxidative Balance ◽

Endogenous Antioxidant

Abstract Ecologically-relevant factors such as exercise and diet quality can directly influence how physiological systems work including those involved in maintaining oxidative balance; however, to our knowledge, no studies to date have focused on how such factors directly affect expression of key components of the endogenous antioxidant system (i.e., transcription factors, select antioxidant genes, and corresponding antioxidant enzymes) in several metabolically active tissues of a migratory songbird. We conducted a 3-factor experiment that tested the following hypotheses: (H1) Daily flying over several weeks increases the expression of transcription factors NRF2 and PPARs as well as endogenous antioxidant genes (i.e., CAT, SOD1, SOD2, GPX1, GPX4), and upregulates endogenous antioxidant enzyme activities (i.e., CAT, SOD, GPx). (H2) Songbirds fed diets composed of more 18:2n-6 PUFA are more susceptible to oxidative damage and thus upregulate their endogenous antioxidant system compared to when fed diets with less PUFA. (H3) Songbirds fed dietary anthocyanins gain additional antioxidant protection and thus upregulate their endogenous antioxidant system less compared to songbirds not fed anthocyanins. Flight training increased the expression of 3 of the 6 antioxidant genes and transcription factors measured in the liver, consistent with H1, but for only one gene (SOD2) in the pectoralis. Dietary fat quality had no effect on antioxidant pathways (H2) whereas dietary anthocyanins increased the expression of select antioxidant enzymes in the pectoralis, but not in the liver (H3). These tissue-specific differences in response to flying and dietary antioxidants are likely explained by functional differences between tissues as well as fundamental differences in their turnover rates. The consumption of dietary antioxidants along with regular flying enables birds during migration to stimulate the expression of genes involved in antioxidant protection likely through increasing the transcriptional activity of NRF2 and PPARs, and thereby demonstrates for the first time that these relevant ecological factors affect the regulation of key antioxidant pathways in wild birds. What remains to be demonstrated is how the extent of these ecological factors (i.e., intensity or duration of flight, amounts of dietary antioxidants) influences the regulation of these antioxidant pathways and thus oxidative balance.

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Flight training and dietary antioxidants have mixed effects on the oxidative status of multiple tissues in a female migratory songbird

Journal of Experimental Biology ◽

10.1242/jeb.243158 ◽

2021 ◽

Author(s):

Abigail E. Frawley ◽

Kristen J. DeMoranville ◽

Katherine M. Carbeck ◽

Lisa Trost ◽

Amadeusz Bryła ◽

...

Keyword(s):

Antioxidant Activity ◽

Oxidative Damage ◽

Antioxidant Capacity ◽

Antioxidant System ◽

Spring Migration ◽

Flight Training ◽

Lipid Hydroperoxides ◽

Enzymatic Antioxidants ◽

Dietary Antioxidants ◽

Enzymatic Antioxidant

Birds, like other vertebrates, rely on a robust antioxidant system to protect themselves against oxidative imbalance caused by energy-intensive activities such as flying. Such oxidative challenges may be especially acute for females during spring migration, since they must pay the oxidative costs of flight while preparing for reproduction; however, little previous work has examined how the antioxidant system of female spring migrants responds to dietary antioxidants and the oxidative challenges of regular flying. We fed two diets to female European starlings, one supplemented with a dietary antioxidant and one without, and then flew them daily in a windtunnel for two weeks during the fall and spring migration periods. We measured the activity of enzymatic antioxidants (GPx, SOD, CAT), non-enzymatic antioxidant capacity (ORAC), and markers of oxidative damage (protein carbonyls and lipid hydroperoxides) in four tissues: pectoralis, leg, liver, and heart. Dietary antioxidants affected enzymatic antioxidant activity and lipid damage in the heart, non-enzymatic antioxidant capacity in the pectoralis, and protein damage in leg muscle. In general, birds fed less antioxidants appear to incur increased oxidative damage while upregulating non-enzymatic and enzymatic antioxidant activity, though these effects were strongly tissue-specific. We also found trends for diet x training interactions for enzymatic antioxidant activity in the heart and leg. Flight-training may condition the antioxidant system of females to dynamically respond to oxidative challenges, and females during spring migration may shift antioxidant allocation to reduce oxidative damage.

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Effects of Desiccation on Metamorphic Climax in Bombina variegata: Changes in Levels and Patterns of Oxidative Stress Parameters

Animals ◽

10.3390/ani11040953 ◽

2021 ◽

Vol 11 (4) ◽

pp. 953

Author(s):

Tamara G. Petrović ◽

Ana Kijanović ◽

Nataša Kolarov Kolarov Tomašević ◽

Jelena P. Gavrić ◽

Svetlana G. Despotović ◽

...

Keyword(s):

Oxidative Stress ◽

Oxidative Damage ◽

Antioxidant System ◽

Water Availability ◽

System Control ◽

Glutathione S Transferase ◽

Oxidative Stress Parameters ◽

Metamorphic Climax ◽

Bombina Variegata ◽

Stress Parameters

In this paper, we examined how the oxidative status (antioxidant system and oxidative damage) of Bombina variegata larvae changed during the metamorphic climax (Gosner stages: 42—beginning, 44—middle and 46—end) and compared the patterns and levels of oxidative stress parameters between individuals developing under constant water availability (control) and those developing under decreasing water availability (desiccation group). Our results revealed that larvae developing under decreasing water availability exhibited increased oxidative damage in the middle and end stages. This was followed by lower levels of glutathione in stages 44 and 46, as well as lower values of catalase, glutathione peroxidase, glutathione S-transferase and sulfhydryl groups in stage 46 (all in relation to control animals). Comparison between stages 42, 44 and 46 within treatments showed that individuals in the last stage demonstrated the highest intensities of lipid oxidative damage in both the control and desiccation groups. As for the parameters of the antioxidant system, control individuals displayed greater variety in response to changes induced by metamorphic climax than individuals exposed to desiccation treatment. The overall decrease in water availability during development led to increased oxidative stress and modifications in the pattern of AOS response to changes induced by metamorphic climax in larvae of B. variegata.

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A manganese oxide nanozyme prevents the oxidative damage of biomolecules without affecting the endogenous antioxidant system

Nanoscale ◽

10.1039/c8nr09397k ◽

2019 ◽

Vol 11 (9) ◽

pp. 3855-3863 ◽

Cited By ~ 22

Author(s):

Namrata Singh ◽

Mohammed Azharuddin Savanur ◽

Shubhi Srivastava ◽

Patrick D'Silva ◽

Govindasamy Mugesh

Keyword(s):

Oxidative Stress ◽

Oxidative Damage ◽

Manganese Oxide ◽

Antioxidant System ◽

Mammalian Cells ◽

Redox State ◽

Stress Conditions ◽

System P ◽

Endogenous Antioxidant ◽

Antioxidant Machinery

Multi-enzyme mimetic Mn3O4 nanoflowers (Mp) modulate the redox state of mammalian cells without altering the cellular antioxidant machinery under oxidative stress conditions.

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Energy Stores, Oxidative Balance, and Sleep in Migratory Garden Warblers (Sylvia borin) and Whitethroats (Sylvia communis) at a Spring Stopover Site

Integrative Organismal Biology ◽

10.1093/iob/obaa010 ◽

2020 ◽

Vol 2 (1) ◽

Author(s):

Andrea Ferretti ◽

Scott R McWilliams ◽

Niels C Rattenborg ◽

Ivan Maggini ◽

Massimiliano Cardinale ◽

...

Keyword(s):

Food Intake ◽

High Energy ◽

Oxidative Status ◽

Energy Reserves ◽

Stopover Site ◽

Garden Warbler ◽

Oxidative Balance ◽

Energy Stores ◽

Sylvia Borin ◽

Sylvia Communis

Synopsis Little is known about how songbirds modulate sleep during migratory periods. Due to the alternation of nocturnal endurance flights and diurnal refueling stopovers, sleep is likely to be a major constraint for many migratory passerine species. Sleep may help to increase the endogenous antioxidant capacity that counteracts free radicals produced during endurance flight and reduces energy expenditure. Here, we investigated the relationship between sleep behavior, food intake, and two markers of physiological condition—the amount of energy reserves and oxidative status—in two migratory songbird species, the garden warbler (Sylvia borin) and the whitethroat (Sylvia communis). In garden warblers, birds with high energy stores were more prone to sleep during the day, while this condition-dependent sleep pattern was not present in whitethroats. In both species, birds with low energy stores were more likely to sleep with their head tucked in the feathers during nocturnal sleep. Moreover, we found a positive correlation between food intake and the extent of energy reserves in garden warblers, but not in whitethroats. Finally, we did not find significant correlations between oxidative status and sleep, or oxidative status and energy stores. Despite our study was not comparative, it suggests that different species might use different strategies to manage their energy during stopover and, additionally, it raises the possibility that migrants have evolved physiological adaptations to deal with oxidative damage produced during migration.

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Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions

AJP Cell Physiology ◽

10.1152/ajpcell.00203.2007 ◽

2007 ◽

Vol 293 (4) ◽

pp. C1302-C1308 ◽

Cited By ~ 50

Author(s):

A. Valle ◽

R. Guevara ◽

F. J. García-Palmer ◽

P. Roca ◽

J. Oliver

Keyword(s):

Sexual Dimorphism ◽

Energy Expenditure ◽

Oxidative Damage ◽

Caloric Restriction ◽

Oxidative Capacity ◽

Complex Iii ◽

Female Rats ◽

Oxidative Balance ◽

Wide Range ◽

Mitochondrial Oxidative Capacity

Caloric restriction (CR) without malnutrition has been shown to increase maximal life span and delay the rate of aging in a wide range of species. It has been proposed that reduction in energy expenditure and oxidative damage may explain the life-extending effect of CR. Sex-related differences also have been shown to influence longevity and energy expenditure in many mammalian species. The aim of the present study was to determine the sex-related differences in rat liver mitochondrial machinery, bioenergetics, and oxidative balance in response to short-term CR. Mitochondria were isolated from 6-mo-old male and female Wistar rats fed ad libitum or subjected to 40% CR for 3 mo. Mitochondrial O2 consumption, activities of the oxidative phosphorylation system (complexes I, III, IV, and V), antioxidative activities [MnSOD, glutathione peroxidase (GPx)], mitochondrial DNA and protein content, mitochondrial H2O2 production, and markers of oxidative damage, as well as cytochrome C oxidase and mitochondrial transcription factor A levels, were measured. Female rats showed a higher oxidative capacity and GPx activity than males. This sexual dimorphism was not modified by CR. Restricted rats showed slightly increased oxygen consumption, complex III activity, and GPx antioxidant activity together with lower levels of oxidative damage. In conclusion, the sexual dimorphism in liver mitochondrial oxidative capacity was unaffected by CR, with females showing higher mitochondrial functionality and ROS protection than males.

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Avian Influenza Viruses in Wild Birds: Virus Evolution in a Multihost Ecosystem

Journal of Virology ◽

10.1128/jvi.00433-18 ◽

2018 ◽

Vol 92 (15) ◽

Cited By ~ 22

Author(s):

Divya Venkatesh ◽

Marjolein J. Poen ◽

Theo M. Bestebroer ◽

Rachel D. Scheuer ◽

Oanh Vuong ◽

...

Keyword(s):

Avian Influenza ◽

Host Species ◽

Phylogenetic Trees ◽

Evolutionary Dynamics ◽

Natural Host ◽

Influenza Viruses ◽

Seasonal Migration ◽

The Black Sea ◽

Avian Influenza Viruses ◽

Stopover Site

ABSTRACTWild ducks and gulls are the major reservoirs for avian influenza A viruses (AIVs). The mechanisms that drive AIV evolution are complex at sites where various duck and gull species from multiple flyways breed, winter, or stage. The Republic of Georgia is located at the intersection of three migratory flyways: the Central Asian flyway, the East Africa/West Asia flyway, and the Black Sea/Mediterranean flyway. For six complete study years (2010 to 2016), we collected AIV samples from various duck and gull species that breed, migrate, and overwinter in Georgia. We found a substantial subtype diversity of viruses that varied in prevalence from year to year. Low-pathogenic AIV (LPAIV) subtypes included H1N1, H2N3, H2N5, H2N7, H3N8, H4N2, H6N2, H7N3, H7N7, H9N1, H9N3, H10N4, H10N7, H11N1, H13N2, H13N6, H13N8, and H16N3, and two highly pathogenic AIVs (HPAIVs) belonging to clade 2.3.4.4, H5N5 and H5N8, were found. Whole-genome phylogenetic trees showed significant host species lineage restriction for nearly all gene segments and significant differences in observed reassortment rates, as defined by quantification of phylogenetic incongruence, and in nucleotide sequence diversity for LPAIVs among different host species. Hemagglutinin clade 2.3.4.4 H5N8 viruses, which circulated in Eurasia during 2014 and 2015, did not reassort, but analysis after their subsequent dissemination during 2016 and 2017 revealed reassortment in all gene segments except NP and NS. Some virus lineages appeared to be unrelated to AIVs in wild bird populations in other regions, with maintenance of local AIVs in Georgia, whereas other lineages showed considerable genetic interrelationships with viruses circulating in other parts of Eurasia and Africa, despite relative undersampling in the area.IMPORTANCEWaterbirds (e.g., gulls and ducks) are natural reservoirs of avian influenza viruses (AIVs) and have been shown to mediate the dispersal of AIVs at intercontinental scales during seasonal migration. The segmented genome of influenza viruses enables viral RNA from different lineages to mix or reassort when two viruses infect the same host. Such reassortant viruses have been identified in most major human influenza pandemics and several poultry outbreaks. Despite their importance, we have only recently begun to understand AIV evolution and reassortment in their natural host reservoirs. This comprehensive study illustrates AIV evolutionary dynamics within a multihost ecosystem at a stopover site where three major migratory flyways intersect. Our analysis of this ecosystem over a 6-year period provides a snapshot of how these viruses are linked to global AIV populations. Understanding the evolution of AIVs in the natural host is imperative to mitigating both the risk of incursion into domestic poultry and the potential risk to mammalian hosts, including humans.

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Carious Lesion Severity Induces Higher Antioxidant System Activity and Consequently Reduces Oxidative Damage in Children’s Saliva

Oxidative Medicine and Cellular Longevity ◽

10.1155/2020/3695683 ◽

2020 ◽

Vol 2020 ◽

pp. 1-9

Author(s):

Heitor Ceolin Araujo ◽

Ana Cláudia Melo Stevanato Nakamune ◽

Wilson Galhego Garcia ◽

Juliano Pelim Pessan ◽

Cristina Antoniali

Keyword(s):

Oxidative Stress ◽

Antioxidant Activity ◽

Oxidative Damage ◽

Antioxidant System ◽

Oxidative Stress Biomarkers ◽

System Activity ◽

Enzymatic Antioxidant ◽

Stress Biomarkers ◽

Salivary Biomarkers ◽

Carious Lesions

Oxidative stress biomarkers can be found at detectable concentrations in saliva. These salivary biomarkers reflect specific oxidation pathways associated with caries and periodontitis. Our study evaluated the influence of dental caries severity (assessed using the ICCMS™ criteria) on the levels of oxidative stress biomarkers in saliva from children. Unstimulated saliva samples were collected from patients (from one to three years old) in a day care center in Birigui, SP, Brazil, two hours after fasting. Children were divided into four groups (n=30/group), according to caries severity: caries free (group A), early carious lesions (group B), moderate carious lesions (group C), and advanced carious lesions (group D). The following salivary biomarkers were determined: total proteins (TP), measured by the Lowry method; oxidative damage, measured by the TBARS method; total antioxidant capacity (TAC); superoxide dismutase (SOD) enzymatic antioxidant activity; and uric acid (UA) non-enzymatic antioxidant activity. Data were analyzed by ANOVA, followed by the Student-Newman-Keuls test, Pearson and Spearman correlation coefficients, and multivariable linear regression (p<0.05). TP, TAC, SOD enzymatic antioxidant activity, and UA non-enzymatic antioxidant activity increased with caries severity, consequently reducing salivary oxidative damage. It was concluded that higher caries severity increases salivary antioxidant system activity, with consequent reduction in salivary oxidative damage.

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Phenotypic divergence during speciation is inversely associated with differences in seasonal migration

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2015.1921 ◽

2015 ◽

Vol 282 (1819) ◽

pp. 20151921 ◽

Cited By ~ 11

Author(s):

Kira E. Delmore ◽

Haley L. Kenyon ◽

Ryan R. Germain ◽

Darren E. Irwin

Keyword(s):

Reproductive Isolation ◽

Migratory Birds ◽

Distinct Species ◽

Seasonal Migration ◽

Phenotypic Traits ◽

Phenotypic Differentiation ◽

Single Form ◽

Breeding Grounds ◽

Migratory Routes ◽

Two Populations

Differences in seasonal migration might promote reproductive isolation and differentiation by causing populations in migratory divides to arrive on the breeding grounds at different times and/or produce hybrids that take inferior migratory routes. We examined this question by quantifying divergence in song, colour, and morphology between sister pairs of North American migratory birds. We predicted that apparent rates of phenotypic differentiation would differ between pairs that do and do not form migratory divides. Consistent with this prediction, results from mixed effects models and Ornstein–Uhlenbeck models of evolution showed different rates of divergence between these groups; surprisingly, differentiation was greater among non-divide pairs. We interpret this finding as a result of variable rates of population blending and fusion between partially diverged forms. Ancient pairs of populations that subsequently fused are now observed as a single form, whereas those that did not fuse are observable as pairs and included in our study. We propose that fusion of two populations is more likely to occur when they have similar migratory routes and little other phenotypic differentiation that would cause reproductive isolation. By contrast, pairs with migratory divides are more likely to remain reproductively isolated, even when differing little in other phenotypic traits. These findings suggest that migratory differences may be one among several isolating barriers that prevent divergent populations from fusing and thereby increase the likelihood that they will continue differentiating as distinct species.

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