Many birds experience fluctuations in body mass throughout the annual life cycle. The flight efficiency hypothesis posits that adaptive mass loss can enhance avian flight ability. However, whether birds can increase additional wing loading following mass loss and how birds adjust flight kinematics and postures remain largely unexplored. We investigated physiological changes in body condition in breeding female Eurasian tree sparrows (Passer montanus) through a dietary restriction experiment and determined the changes in flight kinematics and postures. Body mass decreased significantly, but the external maximum load and mass-corrected total load increased significantly after 3 days of dietary restriction. After 6 days of dietary restriction (DR6), hematocrit, pectoralis and hepatic fat content, take-off speed, theoretical maximum range speed and maximum power speed declined significantly. Notably, the load capacity and power margin remained unchanged relative to the control group. The wing stroke amplitude and relative downstroke duration were not affected by the interaction between diet restriction and extra load. Wing stroke amplitude significantly increased after DR6 treatment, while the relative downstroke duration significantly decreased. The stroke plane angle significantly increased after DR6 treatment only in the load-free condition. In addition, the sparrows adjusted their body angle and stroke plane angle in response to the extra load, but stroke amplitude and wingbeat frequency remained unchanged. Therefore, birds can maintain and even enhance their flight performance by adjusting flight kinematics and postures after a short-term mass loss.

Flight performance is fundamental for most birds to improve their fitness (Hedenström and Alerstam, 1995; Alerstam, 2011; Clemente and Wilson, 2016). In theory, flight ability is expected to change when individuals are in poor physical condition, as it highly depends on their immediate physiological status (Rayner, 1985; Kvist et al., 2001). Mass loss has a considerable impact on flight performance as it decreases wing loading (the ratio of body mass to wing area), thus reducing the energy required for lift generation (Hillström, 1995; Merkle and Barclay, 1996; Cichoń, 2001; Boyle et al., 2012). The flight efficiency hypothesis proposes that adaptive mass loss can improve flight performance, e.g. escape performance (Dietz et al., 2007; Van den Hout et al., 2009) and behavior (Walters et al., 2017), by reducing wing loading (Harrison and Roberts, 2000; Engel et al., 2006). Therefore, it seems that undamaged or even enhanced flight ability when encountering a period of mass loss is essential to promote individual survival. However, whether birds' flight aerodynamic power output increases and how birds adjust their flight kinematics and postures as a result of physiological changes induced by mass loss remain largely unknown.

Many birds exhibit fluctuations in body mass throughout the annual life cycle, specifically during reproduction and migration. Female birds often experience mass loss after the hatching of their offspring, which is attributed to mobilizing fuel reserves for their survival and offspring's development (Freed, 1981; Boyle et al., 2012). In artificial nest boxes, female breeding pied flycatchers (Ficedula hypoleuca) provided with additional food still show a significant mass decline similar to the control group (Slagsvold and Johansen, 1998), indicating an adaptive mass loss during the breeding period. Such mass loss can enhance flight ability as it reduces flight costs (Elliott et al., 2008), increases relative flight muscle mass (Kullberg et al., 2005; Van den Hout et al., 2009) and increases vertical take-off speed (Kullberg et al., 2002). Some shorebirds show a significant decrease in body mass after migration (Scott et al., 1994). Meanwhile, some organs (e.g. the small intestine and liver) that are not directly related to flight function also experience a significant decrease in mass to reduce the cost of long-distance flight (Karasov et al., 2004). Physiologically, mass loss in birds can be attributed to mobilizing endogenous fat and protein reserves through catabolism (Pennycuick, 1998). However, the relative pectoral muscle mass can remain unchanged as body mass decreases, e.g. in red knots (Calidris canutus) during long-term flight (Pennycuick, 1998; Van den Hout et al., 2009). How birds can safeguard flight performance to promote individual survival when experiencing dramatic reductions in body fat storage remains largely unknown.

Maximum power output should be constant despite concurrent mass loss if metabolic output power from flight muscle keeps constant. However, kinematically, force production derives from the alternation of flight muscle efficiency affected by wingbeat frequency and wing stroke amplitude or the proportion of muscle fibers used (Rayner, 1985; Kvist et al., 2001). Thus, enhanced flight performance should come from the moment of maximum efficiency of flight muscle, optimal body mass, and maximum wingbeat frequency and stroke amplitude (Kvist et al., 2001). Although heavier individuals have higher wingbeat frequency than their lighter conspecifics (Rayner, 1988; Schmidt-Wellenburg et al., 2007; Sato et al., 2008), how free-living birds balance this allocation within tight constraints on energy stores and flight muscle efficiency while maintaining unchanged flight performance is still largely unknown.

Apart from body mass and physiological condition, flight performance is determined by multiple trade-offs among speed-related energetics, wingbeat kinematics and flight postures. Flying birds can regulate wingbeat kinematics and flight postures to meet the requirements of lift and thrust (Klein Heerenbrink et al., 2015). Increasing wingbeat frequency and stroke amplitude are fundamental ways to enhance flight power output. Moreover, the relative downstroke duration and flight postures, such as the body angle and stroke plane angle, are also involved in the adjustments of force production (Snelling et al., 2012; Kou et al., 2022). A theoretical model of forward flight in insects reveals that decreasing body angle and increasing stroke plane angle are always accompanied by reduced lift force and increasing thrust, and decreasing relative downstroke duration that can increase thrust power output but has no effect on the lift (Yu and Tong, 2005). However, little information is available on the effects of mass loss on the variations of wingbeat kinematics and flight postures in birds.

Flight power and speed generally follow a U-shaped relationship in level flight. Therefore, birds flying at a lower or higher speed generally require more energy and are less efficient (Alerstam, 2011; Wang et al., 2020). Birds fly at the maximum range speed to acquire the best cruising power and the optimal energy efficiency and fly at the maximum power speed (based on the maximum power) to increase maneuverability and enhance escape opportunities (Hedenström, 2002; Clemente and Wilson, 2016). Such a relationship between flight speed and power predicts alternative flight speeds that should be under intense selective pressure depending on the ecological context. Indeed, birds can fly at an advisable context-related speed in broad agreement with predictions (Klein Heerenbrink et al., 2015). In addition, more available aerodynamic power (power margin) and higher take-off speed also represent a faster escape when encountering risks (Altshuler et al., 2004; Berg and Biewener, 2010).

Load-lifting experiments are a way of measuring flight performance by providing an extra load to animals that can fly. This technique is an effective way to evaluate the maximum power output, wing kinematics and flight postures, and has been employed in a variety of avian species (Altshuler et al., 2004; Sun et al., 2016; Wang et al., 2020; Kou et al., 2022). It enables us to explore the effects of mass loss induced by dietary restriction on underlying flight aerodynamic strategies. We used an experimental manipulation of the body mass of female Eurasian tree sparrows (Passer montanus) during the early breeding period and identified the effects of dietary restrictions on a suite of changes in physiology, flight kinematics and postures. We examined: (1) differences between load-free and load-lifting flight performances, including wingbeat kinematics, flight postures and flight power output; (2) how load-free and load-lifting flight performances vary with mass loss induced by 3-day dietary restriction (DR3) and 6-day dietary restriction (DR6); (3) the volume of stored lipids available in flight muscle and liver; and (4) how morphological correlates including flight muscle mass and heart and liver size relative to both aerodynamic force production and metabolic capacity vary with mass loss after a 6-day dietary restriction. The aim was to determine the relationship between mass loss and flight ability, especially focusing on variations in flight posture and power output by concurrently determining morphological, physiological and kinematic variations in relation to flight performance.

Study animals

Free-living Eurasian tree sparrows [Passer montanus (Linnaeus 1758)] in the nest building stage (Li et al., 2012, 2017) on the Hebei Normal University campus (38°0.24′N, 114°31.50′E, elevation: 75 m) were opportunistically captured in mist nets from 6 to 8 May 2016, in Hebei Province, China. Birds were transported to an outdoor aviary (4.4×2.6 m in area and 2.5 m high) shortly after capture and provided with food [foxtail millet (Setaria italica) mixed with mealworms] and water ad libitum, and with boxes and tree branches for hiding and perching. Birds were kept under natural photoperiod (14.3 h of daylight on average) and temperature (21.8°C on average). Female birds were identified for the experiment by their brood patch (a female-specific trait). To eliminate the possible effects of age, we only used first-year females, which have small yellow spots on the base of the beak. All capture, handling and experimental protocols were approved by the Ethics and Animal Welfare Committee and by the Institutional Animal Care and Use Committee of Hebei Normal University, China, and were carried out under the auspices of scientific collecting permits issued by the Departments of Wildlife Conservation (Forestry Bureau) of Hebei Provinces, China.

Experimental design

After acclimatization for 12–14 days, each bird was individually caged in an indoor husbandry room (50×34×33 cm) and housed next to its neighbors so that they could see and hear each other, with access to food and water ad libitum. Before the experiment, each bird was given 20 g of millet each morning, and the remaining food was weighed the following day. Eight birds were randomly selected to monitor their daily food intake for six continuous days (average daily food intake was 4.25±1.29 g). For the dietary restriction treatment, these birds were then subjected to 66.7% of their daily food intake for 6 days. Our pre-experiments showed that the birds exhibited a significant mass loss after 3 days, and some became weak and inactive after 8 days. Flight performance was evaluated under load-lifting and load-free conditions (without extra load) on the initial day (DR0), and after the third day (DR3) and the sixth day (DR6) of dietary restriction. After the DR6 treatment, the physiological parameters of the birds were measured immediately. A separate group of birds (n=9) was housed at the same time without dietary restriction and served as the control group for physiological parameters. The control group was not measured for flight performance because their flight performance remained unchanged within 30 days of captivity (Kou et al., 2022).

Load-free and load-lifting assays

To determine flight capability, birds were individually placed in a rectangular flight chamber (45×45 cm in area and 150 cm high) made from transparent Plexiglas on two adjacent sides and with a transparent cover on the top (Fig. 1A). Each bird was evaluated under asymptotic load-lifting with a successively longer string of plastic beads (∼1 g each) tied to its left tarsometatarsus (Sun et al., 2016). The birds (∼20 g before food restriction) typically flew vertically toward the top of the chamber, gradually lifting more beads until a maximum value was reached. Each bird was released from the chamber only after completing five vertical take-offs within 150 s, and the attempt with the most lifted beads was considered as the maximum load (∼119±16% of its body mass). The total load was calculated as the sum of body mass and maximum load, and the mass-corrected total load was the total load divided by the body mass. In the control group, the flight behavior of the birds was monitored in a load-free condition without any beads or string. The body mass of each bird was measured to the nearest 0.01 g before each flight assay.

Fig. 1.

Schematic diagram. (A) Flight chamber with the two high-speed video cameras. (B) Measurements of body angle (χ) and stroke plane angle (β). (C) Upstroke (t1) and downstroke (t2) duration of the wingbeat and angles (angle 1, angle 2) between the two wings at the extreme positions.

Fig. 1.

Schematic diagram. (A) Flight chamber with the two high-speed video cameras. (B) Measurements of body angle (χ) and stroke plane angle (β). (C) Upstroke (t1) and downstroke (t2) duration of the wingbeat and angles (angle 1, angle 2) between the two wings at the extreme positions.

Two synchronized high-speed video cameras (GCP100BAC, JVC, Yokohama, Japan) were used to record all flight kinematic parameters (Fig. 1A). Although calculations derived from the use of two cameras to capture actual flight postures may exhibit slight deviations from realistic conditions, this method has been validated as a reliable means for measuring stable flight posture during vertical climbs (Chai et al., 1997; Altshuler et al., 2010; Sun et al., 2016). One camera was positioned on a 50 cm tripod perpendicular to one transparent side of the flight chamber at a distance of 80 cm (operated at 50 frames s−1). It was used to record the duration of a take-off flight (successive segments of 20 cm from the floor to 140 cm of height), to film the beads leaving the flight chamber floor one after another during load-lifting, and to record body axis and stroke plane during flight.

We naturally spread out the right wing of each bird and laid it flat on a whiteboard with a scale, and used a camera positioned vertically on the whiteboard to take photographs. ImageJ (National Institutes of Health, Bethesda, MD, USA) was used to calculate the wing length (cm) and wing area (cm2) of each bird photographed in advance, and the total wing area was obtained by doubling the area of the right wing. We divided the total load by the wing area to calculate the maximum wing loading. We divided the 1.25 m at the beginning of the bird's take-off into five equal segments (S) of 25 cm each. The flight time (t) of each segment was obtained from the number of video frames. The vertical take-off speed (v) of each segment was calculated according to the equation:
(1)
The take-off acceleration (a) was calculated based on the velocity and distance of each segment and their preceding segment using the formula:
(2)

where vt is the velocity through the current segment and v0 is the velocity of the previous segment. We used the maximum values of speed and acceleration from these five segments as the maximum take-off speed and acceleration. This approach attempted to get as close as possible to the real situation under equipment limitations. Body angle (χ) was calculated as the inclination of the body axis relative to the horizontal axis, and stroke plane angle (β) was calculated from the horizontal axis and the vector formed by the wing tip at the upstroke beginning and the downstroke ending (Fig. 1B).

The other camera was positioned to face downward from the top of the flight chamber and operated at 250 frames s−1. It was used to obtain the following parameters of wingbeat kinematics. Mean wing stroke amplitude was calculated from three to five separate measurements within each bout between downstroke and upstroke extreme positions within the final 0.5 s of load-lifting or load-free take-offs. The calculation formula was: [360 deg–(angle 1+angle 2)]/2 (see Fig. 1C).

Wingbeat frequency was calculated by the interaction frequency between wing motions and the camera filming speed for the same measurement period (an average of four consecutive wingbeats were recorded at each trial for the calculation). Duration of upstroke (t1) and downstroke (t2) were recorded as the duration of the wingtip moved back and forth from the nadir limit to the peak limit, respectively (Fig. 1C). The relative downstroke duration of each flight was calculated by the ratio of downstroke duration to that of the upstroke plus the downstroke in an entire wingbeat cycle.

Aerodynamic power and theoretical speed

Our testing chamber allowed the birds to climb nearly vertically upwards. The maximum flight power during each load-free and load-lifting flight was represented as the induced power (Pind), which encompasses the power to create an induced velocity (w) in the air and the lift to support body mass (Askew et al., 2001; Tobalske, 2007). Pind was calculated as:
(3)
where Mb is body mass (g, in load-lifting trials, it is the sum of the body mass and maximum load), and k is a correction factor. Because classical actuator disc theory assumes w to be constant and steady over the disc area (Askew et al., 2001), the value of k used was 1.2, based on experiments on airplane wings and helicopter blades (Pennycuick, 2013), and in previous studies of insect and bird flight (Ellington, 1984; Askew and Ellerby, 2007). w is calculated from classical actuator disc theory and follows the equations described by Wakeling and Ellington (1997). The specific formula is:
(4)
where ρ represents the air density, D is the area swept by the wings [stroke amplitude (rad)×(wing length)2], g is the gravitational acceleration (9.81 m s2), and and are the vertical speed (m s−1) and acceleration (m s−2), respectively. Owing to the confined space of the flight chamber, turbulence generated during wing beating may cause the calculated power output not to reflect the natural flying state accurately. However, it remains a valid method for comparing individual power output differences in flight capacity within identical test scenarios, both pre- and post-experimental treatment, as the conditions were consistent.

The theoretical maximum range speed and maximum power speed were obtained for every individual using findMaximumRangeSpeed and findMaximumPowerSpeed functions in the afpt package (Klein Heerenbrink et al., 2015) in R software (R version 4.1.1, https://www.r-project.org/). The power margin was calculated as the difference between maximum and minimum power required for flight (computeFlightPerfomance function, afpt package). Here, we used the aerodynamic flight power during maximum load-lifting flight as the maximum power output of the birds because we could not measure an actual maximum.

Physiological parameters

We used a 26-gauge needle to puncture the alar vein of each bird and collected approximately 80 μl of blood into heparinized micro-hematocrit capillary tubes. All blood samples were stored on ice until they could be centrifuged at 855 g for 10 min. The hematocrit was measured as the relative volume of red blood cells per total blood volume. Next, birds were euthanized by hypodermic injection of phenobarbitone (7.5 μl g−1 body mass). The flight muscles, including pectoralis major and pectoralis minor (supracoracoideus muscle), heart and liver, were excised and weighed with a precision of 0.1 mg (Ohaus CPJ603 balance, Parsippany, NJ, USA). The heart was isolated from its connections to the blood vessels; the vessels and hepatic ducts attached to the two lobes of the liver were also cut at the connections, and the liver was stripped off. All the organs were rinsed with saline, and the remaining moisture was removed with absorbent paper. Dry masses of the pectoralis major, pectoralis minor and liver were obtained after desiccation in an oven at 65°C for 72 h; their lipid contents were then determined following extraction by a 2:1 chloroform:methanol mixture (Folch et al., 1957). The relative flight muscle mass and heart and liver indices were divided by body mass.

Data analysis

The effects of dietary restriction on body mass, maximum load, total load, mass-corrected total load, maximum take-off speed, theoretical maximum range speed, maximum power speed and power margin were assessed using one-way repeated-measures ANOVA, with individual identity as a repeated factor. We examined the treatment differences relative to hematocrit, heart mass, heart index, liver mass, liver index, flight muscle mass, relative flight muscle mass, pectoralis major and minor masses, the ratio of pectoralis major to pectoralis minor masses, and pectoralis and hepatic fat content using independent-sample t-tests. Effects of loading conditions (load-free and load-lifting), dietary restriction treatment, and the interaction of loading condition and dietary restriction on aerodynamic flight power, wing stroke amplitude, wingbeat frequency, relative downstroke duration, body angle and stroke plane angle were analyzed using a two-way repeated-measures ANOVA, with individual identity as a repeated factor. Differences between pairs of means were identified by Bonferroni-adjusted tests. Effect size was estimated using Cohen's d or partial eta-squared (η2) to measure the strength of significance between groups (Tomczak and Tomczak, 2014). Differences in flight kinematics parameters between load-free and load-lifting conditions under the same dietary restriction stage were determined using paired-sample t-tests. Statistical analysis was performed using SPSS software (version 21.0; IBM, NY, USA), and figures were generated in GraphPad Prism 8.0 (GraphPad Software, San Diego, CA, USA). The significant differences were set as P<0.05.

Variations in physiological parameters induced by dietary restriction

In female Eurasian tree sparrows, body mass varied significantly among dietary restriction treatments (Table 1). Specifically, body mass significantly decreased in treatments of DR3 (P=0.044) and DR6 (P=0.016) relative to the DR0 group, but it was indistinguishable between DR3 and DR6 groups (P=0.255; Fig. 2A). The flight muscle mass, relative flight muscle mass, pectoralis major mass, pectoralis minor mass, ratio of pectoralis major to pectoralis minor masses, heart mass, liver mass and liver index did not change after the DR6 treatment (Table 2). However, values of heart index, hematocrit, pectoralis fat content and hepatic fat content significantly decreased (Fig. 2B-E).

Fig. 2.

Comparisons of body mass (n=8) under normal conditions (DR0) and following 3-day (DR3) and 6-day dietary restriction treatments (DR6), and other physiological parameters (n=9) under normal conditions (control group, CON) and DR6 treatment of female Eurasian tree sparrows. (A) Body mass, (B) heart index, (C) hematocrit, (D) pectoralis fat content and (E) hepatic fat content. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and 5th percentiles. Groups with different letters are significantly different (P<0.05).

Fig. 2.

Comparisons of body mass (n=8) under normal conditions (DR0) and following 3-day (DR3) and 6-day dietary restriction treatments (DR6), and other physiological parameters (n=9) under normal conditions (control group, CON) and DR6 treatment of female Eurasian tree sparrows. (A) Body mass, (B) heart index, (C) hematocrit, (D) pectoralis fat content and (E) hepatic fat content. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and 5th percentiles. Groups with different letters are significantly different (P<0.05).

Table 1.

Effects of 3-day (DR3) and 6-day dietary restriction (DR6) on flight-related parameters in female Eurasian tree sparrows

Effects of 3-day (DR3) and 6-day dietary restriction (DR6) on flight-related parameters in female Eurasian tree sparrows
Effects of 3-day (DR3) and 6-day dietary restriction (DR6) on flight-related parameters in female Eurasian tree sparrows
Table 2.

Effects of 6-day dietary restriction (DR6) on physiological and morphological parameters in female Eurasian tree sparrows

Effects of 6-day dietary restriction (DR6) on physiological and morphological parameters in female Eurasian tree sparrows
Effects of 6-day dietary restriction (DR6) on physiological and morphological parameters in female Eurasian tree sparrows

Variations in flight performance induced by dietary restriction

The maximum load, maximum wing loading, total load and mass-corrected total load varied significantly among dietary restriction treatments (Table 1). Specifically, maximum load and mass-corrected total load significantly increased in the DR3 group but remained unchanged in the DR6 group relative to the DR0 group (Table S1). Maximum wing loading and total load remained unchanged in either the DR3 or DR6 groups relative to the DR0 group. Maximum load, maximum wing loading, total load and mass-corrected total load significantly decreased in the DR6 group relative to those in the DR3 group (Fig. 3A,B; Table S1).

Fig. 3.

Comparisons of loading capacity, flight speed and power margin of female Eurasian tree sparrows (n=8 each group) under normal conditions (DR0), and following 3-day (DR3) and 6-day dietary restriction treatments (DR6). (A) Maximum load and maximum wing loading, (B) total load and total load per body mass, (C) maximum take-off speed and theoretical maximum range speed, (D) maximum power speed and power margin. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and the 5th percentiles. Groups (DR0, DR3, DR6) with different lowercase letters are significantly different from one another (P<0.05).

Fig. 3.

Comparisons of loading capacity, flight speed and power margin of female Eurasian tree sparrows (n=8 each group) under normal conditions (DR0), and following 3-day (DR3) and 6-day dietary restriction treatments (DR6). (A) Maximum load and maximum wing loading, (B) total load and total load per body mass, (C) maximum take-off speed and theoretical maximum range speed, (D) maximum power speed and power margin. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and the 5th percentiles. Groups (DR0, DR3, DR6) with different lowercase letters are significantly different from one another (P<0.05).

The maximum take-off speed, maximum power speed, maximum range speed and power margin varied significantly among dietary restriction treatments (Table 1). Specifically, the maximum take-off speed, maximum range speed and maximum power speed did not change in the DR3 group compared with the DR0 group, but significantly decreased in the DR6 group relative to the DR0 group. There were no significant differences in these parameters between the DR3 and DR6 groups (Fig. 3C,D; Table S1). Notably, the power margin in the DR6 group was significantly lower than that of the DR3 group, although neither DR3 nor DR6 groups differed significantly from the DR0 group (Fig. 3D; Table S1).

Variations in flight kinematics induced by dietary restriction

The aerodynamic flight power varied with load condition and dietary restriction, but there was no interaction between load condition and dietary restriction (Table 3). Specifically, flight power in the DR3 group did not differ from that in the DR0 group (P=1.000), but that in the DR6 group significantly decreased relative to the DR0 and DR3 groups (DR0: P=0.008; DR3: P<0.001; Fig. 4A). Furthermore, aerodynamic flight power increased significantly when challenged by extra load (load-free versus loaded: P<0.001; Table S2).

Fig. 4.

Comparisons of flight power and flight kinematic parameters between load-free and maximum load-lifting flight of female Eurasian tree sparrows (n=8 each group) under normal conditions (DR0) and following 3-day (DR3) and 6-day dietary restriction treatments (DR6). (A) Flight power, (B) stroke amplitude, (C) body angle, (D) stroke plane angle, (E) relative downstroke duration. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and 5th percentiles. Groups (DR0, DR3, DR6) with different letters are significantly different from one another (P<0.05), and asterisks represent significant differences between load-free and load-lifting treatments in a certain group (P<0.05).

Fig. 4.

Comparisons of flight power and flight kinematic parameters between load-free and maximum load-lifting flight of female Eurasian tree sparrows (n=8 each group) under normal conditions (DR0) and following 3-day (DR3) and 6-day dietary restriction treatments (DR6). (A) Flight power, (B) stroke amplitude, (C) body angle, (D) stroke plane angle, (E) relative downstroke duration. Values depicted are the median for each group with the upper and lower limits of the box representing the 75th and 25th percentiles, respectively. The error bars represent the 95th and 5th percentiles. Groups (DR0, DR3, DR6) with different letters are significantly different from one another (P<0.05), and asterisks represent significant differences between load-free and load-lifting treatments in a certain group (P<0.05).

Table 3.

Effects of dietary restriction, load condition and their interaction on flight kinematics in female Eurasian tree sparrows

Effects of dietary restriction, load condition and their interaction on flight kinematics in female Eurasian tree sparrows
Effects of dietary restriction, load condition and their interaction on flight kinematics in female Eurasian tree sparrows

Wingbeat frequency did not vary with load condition, dietary restriction or their interaction (Table 3). Wing stroke amplitude and relative downstroke duration varied significantly with dietary restriction treatment, but not with load condition or the interaction between load condition and dietary restriction (Table 3, Fig. 4B,E). Specifically, in the DR6 group relative to the DR0 group, stroke amplitude increased significantly (P=0.012) and relative downstroke duration decreased significantly (P=0.026), although those in the DR3 group did not (stroke amplitude: P=0.078; downstroke duration: P=0.914).

Body angle varied significantly with load condition but not with dietary restriction or interaction between load condition and dietary restriction (Table 3). Body angle decreased significantly under load-lifting relative to load-free conditions (P <0.001; Fig. 4C; Table S2). However, the stroke plane angle varied significantly with load condition, dietary restriction and their interaction (Table 3, Fig. 4D). Specifically, the stroke plane angle increased significantly with the duration of dietary treatment under load-free conditions, whereas it remained unchanged under the load-lifting condition (Table S1). The stroke plane angle increased significantly under the load-lifting condition relative to load-free condition in the DR0 and DR3 groups, but did not change in the DR6 group (Table S2).

Variations in physiological parameters

Our results showed that Eurasian tree sparrows significantly reduced the hematocrit and fat contents in the pectoralis and liver, along with mass loss in response to the DR6 treatment. Such changes are believed to be physiological responses to environmental perturbations (Norberg, 1981; Lind and Jakobsson, 2001; Fair et al., 2007). Decreases in hematocrit and fat deposits may reflect malnutrition and a consequent metabolic challenge. Effects of food restriction on body mass, hematocrit and fat deposits have also been found in hooded crows (Corvus cornix; Acquarone et al., 2002), magpies (Pica pica; Cucco et al., 2002) and red crossbills (Loxia curvirostra; Bradley et al., 2020). Furthermore, dietary restriction has also been shown to result in a decrease in resting metabolic rate in ducklings (Anas platyrhyncos domesticus; Moe et al., 2005), decreased the sizes of the stomach, small intestine and liver in migratory birds, e.g. yellow-rumped warblers (Setophaga coronata; Lee et al., 2002), yellow-legged gulls (Larus michahellis; Alonso-Alvarez and Ferrer, 2001) and white-throated sparrows (Zonotrichia albicollis; Pierce and McWilliams, 2004). Meanwhile, our results showed that the total and relative flight muscle mass did not change, but the heart index increased. Such an increase in the relative mass of an oxygen-supplying organ should be advantageous for flight activities. Our results suggest that birds, as high oxygen- and energy-consuming animals, can dynamically adjust trade-offs to preferentially support energy for flight in the short term (3 days) but must reduce overall catabolism with long-term (6 days) resource limitation.

Variations in flight performance

Our results indicate that birds increased flight performance in response to mass reduction induced by short-term dietary restriction (DR3 treatment), supporting the flight efficiency hypothesis. Similarly, a temporary mass loss to reduce flight costs contributes to maintaining a constant flight performance in starlings (Sturnus vulgaris; Wiersma et al., 2005), thick-billed murres (Uria lomvia; Elliott and Gaston, 2005) and other birds (Norberg, 1981; Videler, 1995). Unchanged maximum load capacity following a DR6 treatment can be attributed to mass loss and a decrease in fat contents in muscle and liver that lead to decreased wing loading but the maintenance of flight muscle mass. Our results are consistent with prior findings showing no effect on flight ability as the ratio of flight muscle to body mass changes (Lindstrom et al., 2000; Macleod, 2006; Dietz et al., 2007; Van den Hout et al., 2009). Birds can increase their pectoral muscle size without strength training, unlike mammals (Lindstrom et al., 2000). Our results indicate that birds are capable of maintaining flight ability and enhancing catabolism by mobilizing fat reserves in the liver and flight muscle when they are experiencing a short-term shortage of food resources. Therefore, it seems that maintaining flight ability with decreasing body condition is a positive strategy to increase the probability of immediate survival when individuals encounter environmental stimuli, e.g. the threat of predators (Van den Hout et al., 2009; Walters et al., 2017).

However, after the DR6 treatment, the negative effects on flight were apparent. Our results showed that the maximum take-off speed, maximum range, maximum power speed and flight power decreased significantly. This suggests that the DR6 treatment decreased flight speed and power output, although the maximum load did not change. In addition, the power margin did not change with dietary restriction treatment, indicating that the energy efficiency increased and the birds have sufficient energy reserves to maintain flight performance (Askew and Ellerby, 2007). Therefore, such unimpaired flight capability reflected by maximum lifting load should result from self-mass loss but not due to the increase of flight power output, i.e. such a mass loss derived from depleting fat storage enables them to increase the additional loading mass. Similarly, mass loss in brown-headed cowbirds (Malothrus ater) did not induce an impaired escape ability (Walters et al., 2017). These results indicate that the maximum power output in wild birds depends closely on flight muscle size but less on total mass. Whether reduced body mass is closely correlated with optimal efficiency of mechanical power output (Rayner, 1985; Kvist et al., 2001) remains to be determined.

Variations in flight kinematics

Our results further indicate that it is not necessary for birds to alter flight kinematics to maintain flight performance. When the birds exhibited dramatic physiological changes in the DR6 treatment, the changes in flight behavior helped maximize their flight power output. The increase in wing stroke amplitude and decrease in relative downstroke duration enhanced flight power output following dietary restriction. Changing wing stroke amplitude is the primary way for birds to adjust their dynamics when the wingbeat frequency is fixed (Nudds et al., 2004), and this has been confirmed in aerodynamic experiments on hummingbirds (Altshuler and Dudley, 2003; Altshuler et al., 2004). However, unlike hummingbird, which have a wide variation in wingbeat frequency, other passerines can adjust the curvature of their up-and-down wing strokes to help them break the geometric limits of morphological constraints, to an extent (Berg and Biewener, 2010; Muijres et al., 2012). Therefore, the proportion of downstroke duration over the entire wingbeat process is particularly important for achieving better climbing performance, although this may impose a higher energy requirement on the flight muscles and is not suitable for endurance flight (Altshuler and Dudley, 2003; Usherwood, 2016).

Among the flight kinematic parameters, aerodynamic flight power increased, and body angle decreased significantly when sparrows were challenged by an extra load attached to the tarsometatarsus. Our results are in line with the findings in parrots and pigeons, which show that increased flight power is required for take-off and landing (Berg and Biewener, 2010; Chin and Lentink, 2019). Theoretically, a decrease in body angle enhances vertical flight power output (Berg and Biewener, 2010; Chin and Lentink, 2019).

Variation in stroke plane angle is another effective attempt by birds to relax the morphological limitations on wing stroke amplitude (Nudds et al., 2004), which is useful for maintaining theoretical maximum speed and weight-bearing capacity. Our results indicate that an increase in stroke plane angle counters decreased body condition by regulating the power output direction (Yu and Tong, 2005). Maintaining a constant flight power is essential for possessing steady theoretical maximum power speed and take-off speed (i.e. the ability to escape and foraging were unaffected), which is thought to be an important indicator of maneuverability in flight (Kullberg et al., 2002; Clemente and Wilson, 2016). This is in line with findings in red knots, with increased power output and velocity leading to a reduction in turning radius (Van den Hout et al., 2009). It is also noteworthy that changes in body angle and stroke plane angle create precise control of the direction of lifting force or horizontal thrust (David, 1978; Dial, 2003; Tobalske et al., 2007; Snelling et al., 2012; Chin and Lentink, 2019).

Our results are consistent with previous findings showing that wingbeat frequency is highly conserved, unlikely to be changed even by dramatic changes in body condition within (Kou et al., 2022) or among species, e.g. in song thrush (Turdus philomelos) and European robin (Erithacus rubecula) (Bruderer et al., 2010). Our results confirm that wingbeat frequency and wing stroke amplitude do not provide a complete explanation of the maximum loading limits of wild Eurasian tree sparrows (Wang et al., 2019). Wingbeat frequency in flapping flight determines the amount of power available from each gram of flight muscle, which is also associated with the morphology of the wings, body size and air density (Nudds et al., 2004; Pennycuick, 2013; Bruderer et al., 2010).

Conclusions

Our results showed that the sparrows exhibited a dramatic mass loss in response to dietary restriction after the DR3 treatment and even worse body conditions after the DR6 treatment. Despite the physiological challenges, the take-off flight performance was not significantly affected. To the best of our knowledge, this is the first quantitative research on evaluating the costs and benefits of mass loss concerning flight performance in free-living animals. Notably, wing stroke amplitude and relative downstroke duration were closely associated with dietary treatment but independent of load condition. Mass loss induced by a DR3 treatment may increase maximum load capability, but is unrelated to flight power output. In contrast, mass loss induced by a DR6 treatment did not impair flight performance, although it did decrease power output and thus maximum take-off speed owing to a corresponding adjustment of wing kinematics and decreases in theoretical maximum range speed for promoting energy efficiency in flight. The changes in flight postures (body angle and stroke plane angle) but not wing kinematics (wing stroke amplitude, wingbeat frequency and relative downstroke duration) were an important way to lift extra mass in free-living birds, whereas moderating mass loss induced by DR6 (but not DR3) treatment is a co-regulatory effect of both. Our findings contribute to our better understanding of the flight efficiency hypothesis, i.e. unchanged flight performance appears to be an adaptive way of coping with physiological changes induced by extreme conditions shaped by the tight constraints of better performance for survival.

We thank Dr Joseph Elliot at the University of Kansas for assistance with English language and grammatical editing of an earlier version of the manuscript, and Xiaowen Zhang for drawing the schematic diagram.

Author contributions

Conceptualization: D.L.; Methodology: G.K., Y.W., S.G., Y.Y., Y.S., D.L.; Validation: D.L.; Formal analysis: G.K., Y.W.; Data curation: G.K., S.G., Y.Y.; Writing - original draft: G.K., Y.W., D.L.; Visualization: G.K.

Funding

This study was funded by the National Natural Science Foundation of China (NSFC) through grant 31971413 to D.L. and grant 32171490 to Y.W.

Data availability

All relevant data can be found within the article and its supplementary information.

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Competing interests

The authors declare no competing or financial interests.

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