The energy savings-oxidative cost trade-off for migratory birds during endurance flight
- Department of Natural Resources Science, University of Rhode Island, United States
- Department of Biology, Sacred Heart University, United States
- Max Planck Institute for Ornithology, Germany
- Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, China
- Institute of Biological and Environmental Sciences, University of Aberdeen, United Kingdom
- Institute of Environmental Sciences, Jagiellonian University, Poland
- Nencki Institute of Experimental Biology PAS, Poland
Figures
Figure 1
Fatty acid composition of stored fat in European starlings was largely determined by their diet.
Hand-raised European starlings were fed over 4+ months one of two isocaloric diets (MUFA or PUFA) that differed only in the relative amounts of mono- and polyunsaturated fats (Table 1, Table 2), specifically the amounts of omega-9 (18:1), and the so-called ‘essential’ omega-6 (18:2) and omega-3 (18:3) (no. carbons in fatty acid backbone: no. double bonds, and the ‘omega’ designation identifies the location of the first double bond from the terminal end). The stored fat (in the furcular region) of MUFA-fed birds was 75% 18:1% and 10% 18:2, whereas that of PUFA-fed birds was 60% 18:1% and 20% 18:2 and 18:3. Importantly, these three fatty acids primarily composing the fat stores of our hand-raised starlings (i.e. 16:0, 18:1, 18:2) are the same three fatty acids that predominate in the fat stores of free-living passerines sampled during their migration (Pierce and McWilliams, 2005).
Figure 2 with 1 supplement
Dietary fatty acid manipulation affects flight costs but not costs of self-maintenance.
Box plots (mean, 5% and 95% CI, range) for (a) Energy expenditure (measured with doubly labeled water) during a 6 hr ca. 260 km flight in a windtunnel for starlings (n = 33) fed one of two diets (n = 16, 17) and after 15 days of flight-training. Body mass was used as a covariate in the ANCOVA comparison of diet effects on energy expenditure, and (b) Basal metabolic rate (BMR; measured using open-flow respirometry) of MUFA- (n = 19) and PUFA-fed (n = 17) European starlings that were flight-trained or sedentary. Means with different letters within each panel are significantly different (p<0.05).
Figure 2—figure supplement 1
Change in (a) body mass, (b) Beta-hydroxbutyrate, and (c) uric acid in plasma of European starlings (n = 33) during their long-duration (6 hr) flights in Experiment I.
Plasma samples were collected just before departure on the flight and immediately after completion of their long-duration flight. Body mass was included as a fixed covariate so we report the results as least square means (LSM).
Figure 3 with 1 supplement
Oxidative status of European starlings associated with flight-training and in relation to diet quality.
Oxidative status (see Materials and methods, Experiment II) of MUFA-fed or PUFA-fed European starlings was measured in blood plasma at three different time points for flight-trained (black symbols and dashed lines) and untrained, sedentary control (gray symbols and lines) birds: before the start of flight training in the windtunnel (Pre-training), immediately after a long-duration flight on Day 15 (Post-flight), and ca. 1.5 days afterwards (Recovery). Untrained sedentary birds were sampled on the same days but were never exposed to flight-training. Body mass and date of measurement were included as a fixed covariate so we report the results as least square means (LSM). The comparison of Recovery and Post-flight timepoints reveals the effect of the long-duration flight: birds had very similar total flight times over the 15 days of exercise training with the primary difference being whether we sampled the bird’s blood immediately after flight (Post-flight) or 2 days after their final flight (Recovery). The main effect of diet (MUFA vs. PUFA) on oxidative status is shown in the right panels. Means with different letters across the three timepoints, or for the main effect of diet, are significantly different (p<0.05).
Figure 3—figure supplement 1
Plasma metabolites of European starlings associated with flight-training and in relation to diet quality.
Change in circulating levels of (a) Beta-hydroxybutyrate, and (b) Triglycerides in plasma of European starlings over the 15-day flight-training for Trained birds (dark triangles and dashed lines) and over the same 15-day period for Sedentary birds that were not flight-trained (gray triangles, solid lines) in Experiment II. Plasma samples were collected in the early morning after an overnight without food on Day O (Pre-training), before the start of flight-training, on Day 15 immediately after the birds longest flight (Post-flight), and in the early morning after an overnight without food on Day 17 (1.5 days after recovery from the last flight). Body mass and date of measurement were included as a fixed covariate so that we report the results as least square means (LSM). Comparisons between Pre-training and Recovery indicate changes associated with the 15-day flight-training, whereas those between Recovery and Post-flight indicate changes associated with the longest flight on Day 15. Means with different letters across the three timepoints, and for the main effect of diet, are significantly different (p<0.05).
Figure 4
Experimental design for both Experiments I and II from hand-raising of nestling European starlings, to acclimation to one of two experimental diets (both composed of 42% carbohydrates, 23% protein, and 20% fat but differing in the amount of polyunsaturated (PUFA) or monounsaturated (MUFA) fatty acids), and then to flight training in a windtunnel.
During fall, cohort groups of 2–3 starlings were flight trained in the windtunnel for 14 days and then flew on Day 15 a long-duration (usually 6 hr) flight (see Figure 5) during which energy expenditure and plasma indicators of metabolism and oxidative status were measured. For Experiment I, we flight-trained 36 starlings of which 33 completed their 6 hr long-duration flight (16 fed the MUFA diet, 17 fed the PUFA diet). For Experiment II, we added 1–2 untrained, sedentary (control) starlings in each training cohort which resulted in a total of 19 MUFA-fed birds (11 flight-trained, eight sedentary) and 17 PUFA-fed birds (nine flight-trained, eight sedentary).
Figure 5
Fifteen-day flight-training schedule used for European starlings that were flown in the Max Planck Institute for Ornithology (MPIO) windtunnel.
(a) Amount of flying time each day was increased until the final 6 hr flight on Day 15; BMR was measured overnight on the day after this longest flight (b) Schematic of the MPIO windtunnel showing the 2 × 1.5 m working section (closest to the person) that the birds were trained to fly into through the gap (which was then closed during flights). A large fan, shown directly across from the working section, created the wind which was made laminar with a series of screens just before the compression of the tunnel (bottom left). The wind velocity was accelerated with the 20:1 compression of the tunnel just before the working section.
Tables
Table 1
Ingredients and composition of the two semi-synthetic diets fed to European starlings used in Experiments I and II.
The two diets were isocaloric and composed of 42% carbohydrates, 23% protein, and 20% fat. Different amounts of soybean and olive oil were used to produce two diets that differed only in their fatty acid composition (see Table 2).
| MUFA | PUFA | |||
|---|---|---|---|---|
| Ingredients | % wet mass | % dry mass | % wet mass | % dry mass |
| Glucose* | 16.87 | 39.35 | 16.87 | 39.19 |
| Casein† | 8.23 | 19.20 | 8.23 | 19.12 |
| Cellulose‡ | 2.14 | 4.99 | 2.14 | 4.97 |
| Salt mixture§ | 2.06 | 4.80 | 2.06 | 4.78 |
| Olive oil¶ | 7.82 | 18.24 | 4.11 | 9.60 |
| Soybean oil** | 0.41 | 0.96 | 4.11 | 9.60 |
| Amino acid mix†† | 1.15 | 2.69 | 1.15 | 2.68 |
| Vitamin mix‡‡ | 0.16 | 0.38 | 0.16 | 0.38 |
| Mealworms§§ | 2.65 | 6.19 | 2.65 | 6.16 |
| Agar¶¶ | 1.37 | 3.20 | 1.37 | 3.19 |
| Water | 57.14 | 57.14 | ||
-
*Glucose, VWR International GmbH, Darmstadt, Germany;.
†Casein, Affymetrix UK Ltd., High Wycombe, UK.
-
‡Alphacel, MP Biomedicals, Solon, OH, USA.
§Brigg’s salt mix, MP Biomedicals, Solon, OH, USA.
-
¶Tip Native brand Olive oil (glass bottle, Vandemoortele Deutschland GmbH).
**Soya oil, Sojola-brand Soja Oil; Vandemoortele Deutschland GmbH.
-
††Amino Acid Mix, Sigma-Aldrich, St. Louis, MO, USA.
‡‡AIN-76 vitamin mix, MP Biomedicals, Solon, OH, USA.
-
§§Freeze-dried mealworms: Futtermittel Hungenberg Brand, Germany; ca. 45% protein, 33% fats, 7% carbohydrates, and 15% indigestible fiber and ash (Finke, 2002).
¶¶Agar, Ombilab-laborenzentrum GmbH, Bremen, Germany.
Table 2
Fatty acid composition (% ± SE) of the monounsaturated (MUFA) and polyunsaturated (PUFA) fatty acid diets plus mealworms, and of furcular fat from European starlings fed each diet for 4+ months.
Fatty acid concentration was directly measured by gas chromatography in lipids extracted from the diets and the furcular fat.
| MUFA | PUFA | |||
|---|---|---|---|---|
| Fatty acid* | Diet w/mealworms | Furcular fat (n = 13) | Diet w/mealworms | Furcular fat (n = 16) |
| 16:0 | 12.52 | 16.61 ± 0.81 | 12.73 | 16.63 ± 0.65 |
| 16:1 | 0.00 | 3.34 ± 0.34 | 0.00 | 3.35 ± 0.32 |
| 18:0 | 1.38 | 2.69 ± 0.74 | 1.81 | 3.74 ± 0.56 |
| 18:1† | 70.65 | 67.81 ± 1.18 | 51.70 | 56.73 ± 0.90 |
| 18:2† | 14.65 | 9.54 ± 1.32 | 29.34 | 17.70 ± 1.17 |
| 18:3† | 0.50 | 0.00 ± 0.00 | 4.11 | 1.75 ± 0.34 |
-
*Fatty acid nomenclature = C:D where C refers to the number of carbon atoms in the chain and D refers to the number of double bonds present. Other fatty acids found in <1% of the lipid portions of diet were 12:0, 14:0, 20:1, 22:6, 24:1.
†Fatty acid composition (% ± SE) of furcular fat from birds fed MUFA diets was significantly different from that of birds fed PUFA diets, in 18:1, 18:2, and 18:3 fatty acids. .
Table 3
The effect of flight (flight-trained for 15 days in windtunnel or not; Trained or Sedentary), diet (MUFA or PUFA), and time (blood sampled at three different time points: before the start of flight training in the windtunnel (‘Pre-training’), immediately after a long-duration flight on Day 15 (‘Post-flight’), and 1.5 days afterwards (‘Recovery’)) on plasma metabolites and oxidative status in European starlings in Experiment II. Individuals that did not undergo flight training (i.e. control ‘sedentary’ birds) were sampled on the same days as flight-trained birds in their same cohort. Test statistics: F-value with denominator degrees of freedom (ddf) and significance level p-value for main factors and their interactions from the linear mixed models.
| Marker | Flight | Diet | Time point | Flight × Diet | Time × Flight | Time × Diet | Diet × Flight × Time | |||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| F ddf | p | F ddf | p | F ddf | p | F ddf | p | F ddf | p | F ddf | p | F ddf | p | |
| β-Hydroxybutyrate | 4.72 32.9 | 0.04 | 14.0 32.9 | <0.001 | 14.0 62.3 | <0.001 | 0.26 32.9 | 0.61 | 9.44 62.3 | <0.001 | 0.52 62.3 | 0.60 | 0.32 62.3 | 0.73 |
| Total triglicerydes | 0.32 32.6 | 0.57 | 0.13 32.6 | 0.72 | 9.62 60.0 | <0.001 | 0.22 32.6 | 0.88 | 6.90 60.0 | 0.002 | 0.40 60.0 | 0.67 | 0.26 60.0 | 0.97 |
| Uric acid | 9.12 33.5 | 0.004 | 0.65 33.5 | 0.43 | 25.94 63.5 | <0.001 | 1.44 33.5 | 0.24 | 4.32 62.5 | 0.02 | 0.34 62.5 | 0.71 | 0.4262.5 | 0.66 |
| Antioxidant capacity (Oxy adsorbent assay) | 1.05 31.5 | 0.31 | 1.72 31.5 | 0.20 | 6.00 58.9 | 0.004 | 1.9 31.5 | 0.18 | 4.34 58.9 | 0.17 | 0.90 58.8 | 0.41 | 0.36 58.8 | 0.70 |
| Oxidative damage (dROM assay) | 0.26 33.1 | 0.61 | 5.71 33.1 | 0.02 | 0.27 62.0 | 0.77 | 1.86 33.1 | 0.18 | 1.2 62.0 | 0.31 | 1.50 62.0 | 0.23 | 0.27 62.0 | 0.80 |
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The energy savings-oxidative cost trade-off for migratory birds during endurance flight
eLife 9:e60626.
https://doi.org/10.7554/eLife.60626
