Escape Flight Performance Research Articles

Divergence of climbing escape flight performance in Morpho butterflies living in different microhabitats.

ABSTRACTHabitat specialization can influence the evolution of animal movement in promoting divergent locomotor abilities adapted to contrasting environmental conditions, differences in vegetation clutter or predatory communities. While the effect of habitat on the evolution of locomotion and particularly escape performance has been well investigated in terrestrial animals, it remains understudied in flying animals. Here, we investigated whether specialization of Morpho butterfly species into different vertical strata of the Amazonian forest affects the performance of upward escape flight manoeuvres. Using stereoscopic high-speed videography, we compared the climbing flight kinematics of seven Morpho species living either in the forest canopy or in the understory. We show that butterflies from canopy species display strikingly higher climbing speed and steeper ascent angle compared with understory species. Although climbing speed increased with wing speed and angle of attack, the higher climb angle observed in canopy species was best explained by their higher body pitch angle, resulting in more upward-directed aerodynamic thrust forces. Climb angle also scales positively with weight-normalized wing area, and this weight-normalized wing area was higher in canopy species. This shows that a combined divergence in flight behaviour and morphology contributes to the evolution of increased climbing flight abilities in canopy species.

Individual risk-taking behaviour in black-capped chickadees (Poecile atricapillus) does not predict annual survival.

Within species, individuals often show repeatable differences in behaviours, called ‘animal personality’. One behaviour that has been widely studied is how quickly an individual resumes feeding after a disturbance, referred to as boldness or risk-taking. Depending on the mechanism(s) shaping risk-taking behaviour, risk-taking could be positively, negatively, or not associated with differences in overall survival. We studied risk-taking and survival in a population of free-living black-capped chickadees (Poecile atricapillus) in which we previously showed repeatable among-individual differences in risk-taking over the course of several months. We found no evidence that variation in risk-taking is associated with differences in annual survival. We suggest that variation in risk-taking is likely shaped by multiple mechanisms simultaneously, such that the net effect on survival is small or null. For example, among-individual differences in energy demand may favour greater risk-taking without imposing an overall mortality cost if higher energy demand covaries with escape flight performance. We propose directions for future work, including using a multi-trait, multi-year approach to study risk-taking, to allow for stronger inferences regarding the mechanisms shaping these behavioural decisions.

A songbird compensates for wing molt during escape flights by reducing the molt gap and increasing angle of attack.

During molt, birds replace their feathers to retain feather quality and maintain flight performance. However, wing gaps inherent of this process can also reduce flight capacities, which could be detrimental when foraging or escaping predators. Still, many bird species will not cease their normal activities when molting. In this study, we investigated whether and how birds adjust their escape flight behavior to compensate for the reduction in performance when flying with wing gaps. Using stereoscopic high-speed videography, we filmed 146 upward-directed escape flights of 19 and 22 pied flycatchers (Ficedula hypoleuca) with and without simulated molt gaps, respectively. We then reconstructed the three-dimensional body and wing movements throughout each maneuver. By comparing flights with and without gaps, we determined how wing molt gaps affected wing morphology and escape flight performance, and how the birds adjusted their flight kinematics in order to negate possible negative aerodynamic effects. Our manipulations resulted in a lower second moment of area of the wings, but flight speed and net aerodynamic force production did not differ between the two groups. We found that in manipulated birds, the size of the gap was reduced as the flight feathers adjacent to the gap had moved towards each other. Moreover, the experimental decrease in second moment of area was associated with an increase in angle of attack, whereas changes in wingbeat-induced speeds were associated with variations in aerodynamic force production. This suggests that the control of escape flight in molting birds might be modular, allowing relatively simple flight control, thus reducing the burden on the neuro-muscular flight control system.

Carrying a logger reduces escape flight speed in a passerine bird, but relative logger mass may be a misleading measure of this flight performance detriment

Abstract The recent boost in bird migration studies following the development of various tracking devices raised awareness of how detrimental attaching devices can be for animals. Such effects can occur during migration, but also immediately post‐release if the device impairs escape flight performance and, consequently, the bird's ability to evade predators. In this study, we investigated the effect of carrying a device on the escape flight speed and aerodynamic force production in a migratory passerine. We recorded upward‐directed escape flights of 15 male blackcaps. Each individual was tested without a tag, and when equipped with three different leg‐loop dummy tags with masses representing around 3%, 5%, and 7% of their body mass. The experiment was designed such that all individuals passed through all treatments in a randomized order. We found that two factors affected flight speed in roughly equal amounts: first, tagged escape flights had lower flight speeds compared to the control flights, irrespective of tag mass. Second, we found an effect of the total mass, that is, the sum of the masses of the individual bird and of the tag, with heavier birds being slower. In contrast, flight speed was not correlated with relative tag mass in percentage of body mass, the metric commonly used in ethical guidelines for tag attachment. Aerodynamic flight force production also depended on total mass, with heavier birds producing higher forces. But these flight forces did not differ between flights with or without a tag. We conclude that, when tagging birds, it is misleading to choose heavy individuals for tagging in order to minimize the tag mass as a percentage of body mass. This is particularly relevant in species for which body mass is not necessarily related to size, like migratory birds that accumulate large fat reserves. The lower escape speed in “tagged” flights could not be explained by differences in net flight force production, because these did not differ between flights with and without a tag. This suggests that the tag also affected pre‐flight take‐off dynamics, possibly due to a leg harness‐induced reduction in leg push‐off performance.

Exploratory behavior is associated with plasma carotenoid accumulation in two congeneric species of waterfowl

Recently, carotenoid pigments have received considerable attention as modulators of animal health and performance. While studies show that elevated carotenoid intake and accumulation can influence activities like parental care and escape-flight performance, little is known of how carotenoid status influences the expression of animal personality traits, which can be energy-demanding and entail survival costs but also rewarding in the context of foraging and mating. We experimentally investigated the effects of carotenoid availability on exploratory behavior and activity level, using adult males and females of two species of waterfowl: mallard (Anas platyrhynchos) and northern pintail (Anas acuta). We assessed behavior using a novel-environment test designed to measure an individual’s response to novel objects and a potential predator threat (fox urine scent). We found that carotenoid availability was positively associated with some aspects of exploratory behavior: birds with higher concentrations of circulating carotenoids entered the test arena sooner and approached and entered predator-scented bedding material more frequently than birds with low carotenoid concentrations. These results suggest that the availability of carotenoid resources can influence personality traits in waterfowl, and we discuss putative physiological mechanisms underlying this effect.

Early life disadvantage strengthens flight performance trade-offs in European starlings, Sturnus vulgaris

Developmental stress has been shown to affect adult flight performance in birds, with both negative and positive effects reported in the literature. Previous studies have used developmental manipulations that had substantial effects on patterns of growth. They have also examined mean levels of flight performance per individual, rather than investigating how developmental stress might alter trade-offs between different components of flight performance. We recorded multiple components of escape flight performance in 20 adult European starlings previously subjected to a manipulation likely to have altered levels of developmental stress. Siblings had been cross-fostered to nests where they were either slightly larger (advantaged treatment) or slightly smaller (disadvantaged treatment) than their competitors. The manipulation had no detectable effect on growth. However, developmental treatment affected performance in escape flights a year later by strengthening the trade-offs between different flight parameters. Disadvantaged birds faced a steeper trade-off between take-off speed and take-off angle, and a steeper trade-off between take-off angle and total time in flight, than advantaged birds. The results suggest that even subtle early life adversity that has no obvious effect on growth or size can leave a lasting legacy in the form of constraints on locomotor performance later in life.

Costs of compensation: effect of early life conditions and reproduction on flight performance in zebra finches

Conditions experienced in early life have been shown to affect the development or programming of physiological processes. While animals may recover from earlier periods of adversity, this process can carry long-term costs. Such long-term effects are likely to be most evident when individuals are placed in demanding situations that require high performance. Escape flight speed in passerine birds is crucial to predator evasion and requires very rapid take-off. Here, we examine whether the ability to maintain escape flight performance during the immediate post-breeding period is influenced by conditions in early life. We manipulated the early life conditions experienced by zebra finches (Taeniopygia guttata) by rearing them on either low or high quality food through the growth period, or by changing conditions halfway through the nestling period, moving from high to low or vice versa. While there was no difference amongst the treatment groups in body size attained by adulthood, amongst the birds that experienced low quality food, the body size of those that were switched to a high quality diet halfway through the nestling growth period recovered faster than those that had low quality food until fledging. We found no differences amongst the dietary groups in flight performance at adulthood prior to breeding, and all groups showed a decline in average escape flight performance over the breeding period. However, the magnitude of the post-breeding decline in flight performance for a given level of reproductive output was significantly greater for those females that had experienced a switch from a low to a high quality diet during the nestling phase. These results suggest that this diet-induced rapid recovery of body size, which may have immediate competitive advantages, nonetheless carries locomotory costs in later life manifest in the capacity to sustain the high performance escape response during the post-reproductive recovery phase.

Body mass variations in disturbed mallardsAnas platyrhynchosfit to the mass‐dependent starvation‐predation risk trade‐off

For passerines the starvation‐predation risk theory predicts that birds should decrease their body mass to improve escape flight performance, when predation pressure increases. To investigate whether this theory may apply to large birds, which manage body reserves differently from small passerines, we experimentally increased the predation risk in mallardsAnas platyrhynchos. Two groups were disturbed at different frequencies during experimental sessions lasting one week, while a control group was left undisturbed. We found that body mass loss and final wing loading were similar in both disturbed groups and significantly differed from the control group. Food intake in disturbed groups was reduced up to day four of the disturbance session and was lower than in the control group. Altogether our results suggest that disturbed mallards may adjust their body mass to reach a more favorable wing loading, supposedly to improve escape flight performance. Nevertheless, body mass loss in our mallards was double than what has been observed in passerines. This greater mass decrease might be explained by different strategies concerning energy storage. Furthermore, in large birds the predation component of the starvation‐predation trade‐off might be of greater importance. Hence, the observed relevance of this trade‐off over a large size range suggests that the starvation‐predation risk theory is of major ecological significance for many animal species.

Antioxidant status, flight performance and sexual signalling in wild-type parrots

During mate choice, individuals are predicted to assess traits that honestly signal the quality of potential partners. Locomotor capacity may be such a trait, potentially signalling condition and ability to resist oxidative damage. In this study, we experimentally manipulated nutritional status: Male wild-type budgerigars, imported from Australia, were provided with either an enhanced (EQ) or reduced quality (RQ) diet varying in vitamin (particularly retinol and α-tocopherol) and mineral levels. Then, we assessed whether this influenced locomotor capacity, i.e. escape flight performance, and sexual attractiveness in male budgerigars Melopsittacus undulatus. Males in the EQ group showed significantly greater total antioxidant capacity and higher blood plasma concentrations of the dietary antioxidants retinol and α-tocopherol, but not carotenoids, than the RQ group. Over 8 weeks of flight training, males on the EQ diet showed significantly greater improvement on the most strenuous flight test than RQ males. In mate choice trials, females preferred EQ over RQ males. EQ males that were relatively fast in escape flight trials were more strongly preferred in the mate preference arena than their RQ competitors. Interestingly, males with high plasma carotenoid levels flew slower and were less attractive than males with low carotenoid levels. This might indicate that carotenoids are not effective antioxidants in birds. Overall, our results show that dietary-derived antioxidants can influence sexual attractiveness and other fitness-related traits through multiple pathways. Locomotor capacity appears to be an honest signal of male condition in birds.

Impacts of dietary antioxidants and flight training on post-exercise oxidative damage in adult parrots

After intense physical activity animals generally experience a rise in metabolic rate, which is associated with a proliferation of pro-oxidants. If unchecked, these pro-oxidants can cause damage to DNA and peroxidation of lipids in cell walls. Two factors are thought to ameliorate post-exercise oxidative damage, at least in mammals: dietary antioxidants and exercise training. So far it is unknown whether birds benefit similarly from exercise training, although a positive effect of dietary antioxidants on take-off flight has been indicated. In this experiment, we maintained captive wildtype budgerigars Melopsittacus undulatus on enhanced (EQ) or reduced quality (RQ) diets differing in levels of the dietary antioxidants retinol, vitamin C and alpha-tocopherol for 12 months. Birds were then regularly trained to perform take-off escape flights, a strenuous and biologically relevant form of exercise. For these adult budgerigars, regular exercise training improved escape flight performance, particularly in males on the EQ diet. In terms of oxidative damage, post-exercise levels of malondialdehyde (MDA), a by-product of lipid peroxidation, were significantly decreased after 9 weeks of flight training than after a single exercise session. Thus, individuals achieved faster escape flights with lower oxidative damage, after training. Also, birds that were fatter for their skeletal size initially had higher post-exercise MDA levels than thinner birds, but this relationship was broken by 9 weeks of flight training. Interestingly, there was no impact of diet quality on levels of MDA, suggesting that improved protection against oxidative damage for all birds was due to an up-regulation of endogenous antioxidant systems. Given their diversity, bird species provide rich research opportunities for investigating the interactions between exercise training, pro-oxidants production and antioxidant defences.

The starvation–predation risk trade‐off, body mass and population status in the Common Starling Sturnus vulgaris

It is theoretically and empirically well established that body mass variation in small birds reflects a trade‐off between starvation risk and predation risk. This occurs because carrying increased fat reserves reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, therefore, the theory of mass‐dependent predation risk could be used to understand how a bird perceives and responds to the risks in its environment, because its mass will reflect the predictability of foraging opportunities and predation risk. Mass in birds may then provide a relatively straightforward way of assessing the foraging environment of birds and so the potential conservation problems a species faces. This study tests, for the first time for any species, how body mass changes in response to changing starvation risk, changing predation risk and changing population status. Common Starling Sturnus vulgaris mass varies as predicted by starvation–predation risk trade‐off theory: mass is lower when foraging conditions are more favourable and when predation risk is increased. The populations that are declining the most strongly have higher mass, which is most likely indicative of a poor foraging environment, leading to lower relative survival. The results suggest that increased mass in Starlings, and possibly in other species, may provide an indication of the poor quality of the foraging environment and/or rapidly declining populations.

Mass-dependent predation risk and lethal dolphin–porpoise interactions

In small birds, mass-dependent predation risk (MDPR) is known to make the trade-off between avoiding starvation and avoiding predation dependent on individual mass. This occurs because carrying increased fat reserves not only reduces starvation risk but also results in a higher predation risk due to reduced escape flight performance and/or the increased foraging exposure needed to maintain a higher body mass. In principle, the theory of MDPR could also apply to any animal capable of storing energy reserves to reduce starvation and whose escape performance decreases with increasing mass. We used a unique situation along certain parts of coastal Britain, where harbour porpoises (Phocoena phocoena) are pursued and killed but crucially not eaten by bottlenose dolphins (Tursiops truncatus), to investigate whether a MDPR effect can occur in non-avian species. We show that where high levels of dolphin 'predation' occur, porpoises carry significantly less energy reserves than would otherwise be expected and this equates to reducing by approximately 37% the length of time that a porpoise could survive without feeding. These results provide the first evidence that a mass-dependent starvation-predation risk trade-off may be a general ecological principle that can apply to widely different animal types rather than, as is currently thought, only to birds.

Diurnal mass gain strategies and perceived predation risk in the great tit Parus major

1 Individual animals optimize their body mass to enhance fitness and mass is expected to be optimized over both short and long time-scales. On the short time-scale small birds increase mass as they build up energy reserves over each day to avoid starving at night. Theory predicts that starvation risk should be minimized by gaining mass at the start of the day thus insuring against unpredictable food supply later. However, if predation risk is mass-dependent due to reduced escape flight performance, birds should delay mass gain until later in the day to minimize predation risk. 2 Regulation of mass change over longer time-scales has been well documented and a number of studies have been able to show that over weeks, months and years mass is regulated consistent with the starvation–predation risk trade-off being mass-dependent. However, it is crucial to mass-dependent predation theory that it functions over shorter time-scales as well and that birds are able to regulate their diurnal mass gain strategies in response to predation risk. This has not yet been investigated and recent studies of flight performance have been unable to show that small-scale mass change (< 10%) over short time-scales (e.g. diurnal mass change) affects escape flight performance as predicted. 3 We used a unique design of automated identification and weighing system that for the first time allowed the diurnal mass gain of individual great tits Parus major to be monitored remotely in the wild. While automatically tracking diurnal body mass changes of individuals we manipulated perceived predation risk by using model sparrowhawks. We were thus able to investigate experimentally the effect of increased perceived predation risk on diurnal mass gain patterns. 4 We show, for the first time, that birds are capable of manipulating their diurnal body mass gain strategy in response to heightened predation risk and that they do so by delaying mass gain until later in the day, as predicted by mass-dependent predation risk theory. Furthermore, the results are consistent with changing flight performance rather than changing exposure time to predators being the driving force for mass-dependent predation risk.

Plumage Condition Affects Flight Performance in Common Starlings: Implications for Developmental Homeostasis, Abrasion and Moult

Variation in length and asymmetry of wing primary feathers can arise from a breakdown of developmental homeostasis, feather abrasion and incomplete growth during moult. Indirect predictions have been made concerning the impact of primary length and asymmetry on the flight ability of birds, but they have not been explicitly tested. Here we provide evidence from both natural variation in primary feather condition and experimental manipulations of primary feather length and asymmetry to indicate that these factors influence aspects of flight performance in the Common Starling Sturnus vulgaris. Damaged and incompletely grown primary feathers reduce escape flight performance. Experimentally reduced primary lengths reduce take-off speed; increased primary asymmetry decreases aerial manoeuvrability. A comparison of the experimental and natural plumage data indicates that birds may be able to adapt to a change in wing morphology, perhaps reducing the effects of feather loss or damage on flight. The results from this study indicate that primary feathers are under strong stabilising selection to maximise developmental homeostasis and reduce feather asymmetry. These findings are also of ecological importance to the damageavoidance and moult strategies of these birds. This is the first experimental evidence to indicate a quantitative reduction in flight performance with feather lengths and asymmetries typical of those observed during flight feather moult and feather damage in any species.