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Thursday, 26 February 2015

Oxidative Stress in Endurance Flight: A study of the European Robin. Jenni-Eiermann et al PLoS ONE May 2014

Oxidative Stress in Endurance Flight: An Unconsidered Factor in Bird Migration

Authors
Susanne Jenni-Eiermann (E-mail: susi.jenni@vogelwarte.ch)

Swiss Ornithological Institute, Sempach, Switzerland
Lukas Jenni,
Swiss Ornithological Institute, Sempach, Switzerland
Shona Smith,
Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom
David Costantini
Institute for Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Glasgow, United Kingdom, Department of Biology, University of Antwerp, Wilrijk, Belgium

Citation
Jenni-Eiermann S, Jenni L, Smith S, Costantini D (2014) Oxidative Stress in Endurance Flight: An Unconsidered Factor in Bird Migration. PLoS ONE 9(5): e97650. doi:10.1371/journal.pone.0097650

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Abstract
Migrating birds perform extraordinary endurance flights, up to 200 h non-stop, at a very high metabolic rate and while fasting. Such an intense and prolonged physical activity is normally associated with an increased production of reactive oxygen and nitrogen species (RONS) and thus increased risk of oxidative stress. However, up to now it was unknown whether endurance flight evokes oxidative stress. We measured a marker of oxidative damage (protein carbonyls, PCs) and a marker of enzymatic antioxidant capacity (glutathione peroxidase, GPx) in the European robin (Erithacus rubecula), a nocturnal migrant, on its way to the non-breeding grounds. Both markers were significantly higher in European robins caught out of their nocturnal flight than in conspecifics caught during the day while resting. Independently of time of day, both markers showed higher concentrations in individuals with reduced flight muscles. Adults had higher GPx concentrations than first-year birds on their first migration. These results show for the first time that free-flying migrants experience oxidative stress during endurance flight and up-regulate one component of antioxidant capacity. We discuss that avoiding oxidative stress may be an overlooked factor shaping bird migration strategies, e.g. by disfavouring long non-stop flights and an extensive catabolism of the flight muscles.


Review Summary
Migratory birds have evolved specialised biochemical and cellular mechanisms, such as the method of lipid transport from adipose tissue direct to the mitochondria of the flight muscles. This allows them to manage the stresses of migratory flight that may include days of non-stop flying, whilst fasting, at a high metabolic rate. These high levels of catabolic processes are likely to generate quantities of reactive oxygen and nitrogen species (RONS) which should be harmful to the bird due to oxidative stress effects. The mechanism of oxidative balance in the Robin during migration across Europe is the subject of this paper.
The authors investigated a marker of oxidative damage and a marker of enzymatic antioxidant capacity in red blood cells of a migrant passerine, the European robin. These birds were caught out of migratory flight, towards the non-breeding grounds, at a Swiss Alpine Pass (Col de Bretolet located at the border between Switzerland and France) during the Autumn migration of 2011. They chose the European robin because it is the only nocturnal migrant which uses the Alpine pass for resting and feeding at day in noticeable numbers, and therefore they could compare markers of oxidative stress in two metabolic phases; the phase of extremely high metabolic rate during endurance exercise while fasting, and the phase of low metabolic rate during resting and foraging. 

Capture and Analysis
A total of 101 European robins were caught, 62 at night (44 first-year birds, 16 adults, 2 undetermined) and 39 during daylight or at dawn (29 first-years, 9 adults, 1 undetermined). 
Measurements of each bird were made as follows:

  1. Age
  2. Weight
  3. Third outermost primary feather length
  4. Subcutaneous fat score (The visible amount of subcutaneous fat deposits between the furcula and on the abdomen was scored on a scale ranging from 0 to 8; with 0 representing no visible fat.)
  5. Breast muscle score (0-3; with 0 leanest)
  6. Blood: protein carbonyls (PCs) - biomarker of oxidative damage
  7. Blood: activity of glutathione peroxidase (GPx) - biomarker of antioxidant activity
  8. Time of capture relative to dawn - negative values (i.e. before dawn) indicating captures at night and positive values indicating captures after dawn, during the day


Results

Figure 1
Relationship between (a) protein carbonyls (PCs) (nmol/mg protein) of European robins and capture time since dawn, and (b) glutathione peroxidase (GPx) (U/l haemolysate) and capture time since dawn (N = 95).

Dawn is set to zero. Negative values (i.e. before dawn) indicate captures at night and positive values captures after dawn during the day. Dots are raw data points. The linear and cubic relationships with 95% confidence interval are derived from the models presented in Table 1 and given for muscle score 2 (PCs) and for young birds with muscle score 2 (GPx), respectively.



Figure 2
(a) Mean (95% confidence intervals) protein carbonyls (PCs) (nmol/mg protein) corrected for the linear relationship with time since dawn for muscle score 1 (N = 23), 2 (N = 63) and 3 (N = 9). For statistics see Table 1. (b) Mean (95% confidence intervals) glutathione peroxidase (GPx) (U/l haemolysate) corrected for the cubic relationship with time since dawn and age for muscle score 1 (N = 22), 2 (N = 64) and 3 (N = 9). (c) Mean (95% confidence intervals) glutathione peroxidase (U/l haemolysate) corrected for the cubic relationship with time since dawn and muscle for first-year (N = 70) and adult (N = 25) European robins.


Protein Carbonyl Levels - oxidative damage marker
The level of PCs was shown to reduce over time with the highest levels during the night and the lowest during the hours after dawn, however the confidence limits are quite large as there are fewer birds sampled at the upper and lower sampling times. 
Muscle score of 1 (lean birds) showed higher PC levels than those with muscle scores 2 and 3. Muscle score estimates the thickness of the breast muscle, representing breast muscle protein mass, and ranges from 0 to 3.
Neither fat score nor age had significant effects on PC level.

Glutathione Peroxidase Levels - antioxidant activity marker
The concentration of GPx in red blood cells was significantly dependent on time since dawn and on muscle score and age, but not fat score. It was high during the first part of the night, slightly lower in the middle part and peaked at dawn. After dawn GPx concentration decreased throughout the day in robins resting and feeding. 
The highest GPx concentrations were found in lean birds (muscle score 1), medium levels for muscle score 2, and the lowest levels for muscle score 3. Adults had significantly higher GPx concentrations than first-year birds.


Concluding Remarks
The study shows good evidence that this migratory bird, the European robin, is showing evidence of both oxidative stress and increase in a marker for the subsequent biochemical protection response. Migration journeys that cover significant distances over lengthy time-spans must therefore have measurable effects on a bird's fitness and therefore will partially determine the success or failure to meet breeding deadlines or areas of food supplies. It is crucial that the birds are fit and healthy with good muscle development to withstand the effects of the long flights undertaken. Understanding the costs versus benefits of oxidative stress response in migratory birds may be another tool, useful in research into avian migration studies.

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