The ‘jack of all trades’ concept – the idea that the ability to function in multiple environments can only be achieved by sacrificing maximal performance (MacArthur, 1972) – is commonly invoked in discussing the locomotor performance of wing-propelled diving birds (Elliott et al., 2013; Simpson, 1946; Stettenheim, 1959; Storer, 1960; Thaxter et al., 2010). These species, which include some or all members of the alcids (Alcidae), ducks (Anatidae), petrels and shearwaters (Procellariidae), dippers (Cinclus), and the penguins (Spheniscidae), use their wings to propel themselves underwater. Wing-propelled diving birds which have retained their ability to fly in the air – hereafter, ‘dual-medium’ species (sensu Kovacs and Meyers, 2000) – are fluid generalists. These animals use the same locomotor apparatus to ‘fly’ in both air and water, and are, therefore, expected to fly poorly relative to strictly aerial and strictly aquatic fliers in each environment.

Interestingly, birds in the family Alcidae (puffins, murres, and their relatives) seem to contradict the notion of a trade-off between aerial and aquatic flight performance. As with many dual-medium birds, alcids have high wing-loading (the ratio of body mass to wing area), and therefore display poor maneuverability in aerial flight relative to non-diving birds (Ortega-Jimenez et al., 2011; Shepard et al., 2019). However, the wing-loadings of alcids and other dual-medium birds are nearly indistinguishable from those of volant birds which use their feet for aquatic locomotion (based on data from Alerstam et al., 2007; Bruderer et al., 2010; Spear and Ainley, 1997), indicating that high wing-loading is likely the result of selection by the aquatic environment for large body sizes or low buoyancy (Ponganis, 2015), rather than a trade-off specific to dual-medium flight. The current records for the depth and duration of a single dive by an alcid are 210 m and 224 s, respectively, held by the ~1 kg thick-billed murre (Uria lomvia, Linnaeus 1758), making this alcid, on a mass-specific basis, the deepest and longest-duration diver on earth (Croll et al., 1992). When corrected for body size, alcids exhibit dive durations and depths far greater than even penguins (Halsey et al., 2006).

One possible explanation for the aquatic performance of alcids is that they have mitigated the costs of dual-medium flight. Specifically, by maintaining efficient Strouhal numbers (St) and stroke velocities across air and water, birds in the family Alcidae may lessen the perceivable differences between aerial and aquatic flight, thereby reducing the costs of fluid generalism.

To swim or fly, an animal must impart momentum to the surrounding fluid. Strouhal number (St = fAU⁻¹, where f is wingbeat frequency, A is wing excursion, and U is forward speed) describes the pattern of vortices shed into the fluid wake by a flapping foil as it imparts that momentum (Triantafyllou et al., 1993). Extensive research has determined that peak efficiency (in terms of the power required to flap a foil relative to the thrust output to the fluid) for a simple heaving and pitching foil occurs at around 0.2 < St < 0.4 (Anderson et al., 1998; Triantafyllou et al., 1991; Triantafyllou et al., 1993). Most flapping and swimming animals studied to date fall within or near that range, with the previously studied, strictly aerial birds exhibiting 0.12 < St < 0.47 during cruising flight (Taylor et al., 2003). That most species fall near the efficient range of St suggests that natural selection has tuned the kinematics of animals to fly and swim efficiently (Nudds et al., 2004; Taylor et al., 2003). Thus, alcids could achieve efficient fluid wake production in both air and water by maintaining 0.2 < St < 0.4, and efficiency on par with previously studied single-media species by maintaining 0.12 < St < 0.47, but the ‘jack of all trades’ concept suggests that they may unable to do so given the substantial differences in density and viscosity between the two fluids.

Stroke velocity describes the speed at which the wing is swept through its arc during either the downstroke or the upstroke of the wing. This parameter is likely important in determining the cost of locomotion given that it should be proportional to the contractile velocity of the major flight muscles, the pectoralis and the supracoracoideus (Hamilton, 2006; Tobalske and Dial, 1994; Tobalske et al., 1999). Muscles fibers of a given fiber type and myosin isoform are most efficient at converting metabolic power into mechanical power over a narrow range of contractile velocities (Goldspink, 1977; He et al., 2000; Reggiani et al., 1997; Rome et al., 1988). Thus, it would behoove alcids to operate the fibers in their flight muscles at the contractile velocity which maximizes muscle efficiency, and for that velocity to be shared across aerial and aquatic flight. Otherwise, alcids could maintain two populations of fibers – an aerial set and an aquatic set – but this would add mass to the animal, increasing the cost of aerial flight (Ellington, 1984a). Previous research has demonstrated that diving alcids maintain stroke velocities within a narrow range across dive depths, despite large variations in buoyancy, suggesting that they are responsive to the challenge of maintaining contractile velocity (Watanuki and Sato, 2008; Watanuki et al., 2006). Although researchers have not yet examined myosin isoforms in alcids, the two species of alcids for which histochemical data are available possess only ‘fast’ muscle fibers (Kovacs and Meyers, 2000; Meyers et al., 1992).

Recently, Kikuchi et al., 2015 measured the kinematics of flying and diving rhinoceros auklets (Cerorhinca monocerata) using a combination of videography and accelerometry. The authors used bootstrapping to coalesce measurements from various individuals to determine the range of St exhibited by this species. The results of this study strongly suggest that this small alcid maintains optimal St in air and water. We wanted to extend this work to determine if individuals tune their kinematics to match optimal St on a per-flight basis. Alternatively, it is possible that the average kinematics of this species are simply centered between 0.2 < St < 0.4. These authors also suggest, based on wingbeat frequency, that stroke velocities of rhinoceros auklets are lower in water, but were unable to statistically compare stroke velocities during aerial versus aquatic flight. While wingbeat frequencies are different between aquatic and aerial flight (~2–4 Hz versus 7–11 Hz, respectively), wingbeat amplitude may vary between the two environments, allowing for similar stroke velocities.

To improve understanding of potential evolutionary trade-offs between aerial and aquatic flight, we tested whether alcids exhibit efficient St and maintain consistent stroke velocities when flying in water and air. We used videography to measure the wing kinematics of four species of alcids from three genera. These species differ substantially in body mass (450 g to 1 kg) and represent opposite branches of the alcid phylogeny. In addition to St and stroke velocity, we report a variety of kinematic parameters, including stroke-plane and chord angles relative to the body to contrast how the flight apparatus is used in air versus water and during horizontal versus descending aquatic flight. We hypothesized that alcids maintain efficient St and consistent stroke velocities across air and water, which would allow this group to mitigate the costs of fluid generalism (Figure 1).

Figure 1

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Strouhal numbers (St) for horizontal aquatic flights averaged 0.18 ± 0.02 for common murres, 0.13 ± 0.01 for horned puffins, 0.15 ± 0.01 for pigeon guillemots, and 0.15 ± 0.02 for tufted puffins (Figure 2, blue points). St for descending aquatic flights were significantly greater than those for horizontal aquatic flights (F_1,27 = 145.6, η² = 0.729, p-value = 2.18e-12) with a relatively minor but significant interaction between species and the type of aquatic flight (F_3,27 = 3.59, η² = 0.054, p-value = 0.0264). Within-species post hoc tests indicated that all species exhibited greater St during descending aquatic flights relative to horizontal aquatic flights (p = 0.0478, 4.19e-04, 9.17e-07, 5.72e-07; for species in alphabetical order). St for descending aquatic flights averaged 0.24 ± 0.01 for flights of common murres, 0.21 ± 0.04 for horned puffins, 0.29 ± 0.06 for pigeon guillemots, and 0.29 ± 0.03 for tufted puffins (Figure 2, green points).

Figure 2

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Strouhal numbers of four species of alcid in aerial and aquatic flight.

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St for aerial flights based on the ground speed of the birds averaged 0.17 ± 0.02 for common murres, 0.22 ± 0.14 for horned puffins, 0.49 ± 0.06 for pigeon guillemots, and 0.27 ± 0.02 for tufted puffins (Figure 2, dark red points). Except for the flights of common murres, all birds appeared to be flying in considerable wind based on the size of the waves on the surface of the water. Thus, we also calculated St for aerial flights based on the airspeed characteristic of each species as reported in Spear and Ainley, 1997 (see Materials and methods for details). When estimated from the range of measured cruising flight speeds, St for aerial flights ranged from 0.12 to 0.25 for flights of common murres, 0.13 to 0.27 for horned puffins, 0.18 to 0.27 for pigeon guillemots, and 0.16 to 0.25 for tufted puffins (Figure 2, light red lines).

Downstroke velocities were significantly greater during aerial flights than during aquatic flights for all four species (t-Value = 8.10, 11.5, 6.04, 25.9; df = 16.5, 19.0, 9.48, 16.5; p-values = 3.80e-07, 5.19e-10, 1.55e-04, 8.56e-15; for species in alphabetical order; Figure 3). The same was true for upstroke velocities (t-Value = 10.5, 16.0, 6.83, 26.4; df = 15.0, 18.8, 9.18, 16.1; p-values = 2.67e-08, 2.13e-12, 6.97e-05, 1.09e-14; for species in alphabetical order; Figure 3). Wingbeat amplitudes were greater during aquatic flights across species (F_1,71 = 162.4, η² = 0.597, p-value<2.2e-16; Figure 4) with a relatively minor but significant interaction between species and fluid (F_3,71 = 3.52, η² = 0.039, p-value=0.019). Within-species post hoc tests indicated that all four species exhibited significantly greater wingbeat amplitudes during aquatic flight relative to aerial flight (p-values=1.93e-06,<1.0e-08, 3.29e-04, 2.36e-05). Stroke durations were often 2-3X greater in water as compared to air, as indicated by the differences in wingbeat frequency (Figure 4), leading to significant differences in stroke velocities between fluids.

Figure 3

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Stroke velocities of four species of alcid in aerial and aquatic flight.

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Figure 4

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When horizontal and descending aquatic flights are grouped together, stroke-plane angle (β) was significantly lower (the top of stroke plane is rotated more caudally) during aerial flights relative to aquatic flights (F_1,47 = 41.3, η² = 0.422, p = 6.14e-08; Figure 5). Across species, stroke-plane angle averaged 79 ± 7 deg for aerial flights, 92 ± 7 deg for horizontal aquatic flights, and 93 ± 12 deg for descending aquatic flights. Within aquatic flights, there was no significant relationship between stroke-plane angle and angle of descent (F_1,27 = 0.0755, η² = 0.002, p = 0.786; Figure 5).

Figure 5

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Stroke-plane angle of four species of alcid in aerial and aquatic flight.

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There was a significant relationship between chord angle (α) and angle of descent for upstroke (F_1,30 = 55.7, η² = 0.458, p = 2.55e-08; Figure 6) and downstroke (F_1,27 = 8.17, η² = 0.122, p = 8.11e-03; Figure 6). However, a significant crossed interaction between species and angle of descent for downstroke chord angle (F_3,27 = 7.68, η² = 0.343, p = 7.26e-4), indicates that the main effect of angle of descent on chord angle during downstroke is uninterpretable (i.e. the response depends on the species; Figure 6). However, alcids significantly increased chord angle (thus, the degree of supination) during upstroke as a function of angle of descent.

Figure 6

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Chord angle versus descent angle for aquatic flights of four species of alcids.

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Alcids achieve efficient wake production based on St during both aerial flight (based on airspeed) and during aquatic flight. While St for horizontal aquatic flights often fell below St = 0.2 (Figure 2, blue points), all measured values overlapped with the range for the cruising aerial flight of strictly aerial birds reported in the literature (Taylor et al., 2003). Because stroke velocities were substantially different between air and water (Figure 3), the use of efficient St seems to come at a cost to the contractile efficiency of the primary flight muscles. Alternatively, aerial and aquatic flight may be powered by different sets of muscles, as discussed below.

We interpret the relatively low values of St during horizontal aquatic flight to be a consequence of buoyancy. While swimming horizontally, alcids must counteract buoyancy as it attempts to pull them toward their dorsal side. Buoyancy is especially strong at shallow depths, as air volumes compress with depth (Wilson et al., 1992). To compensate for buoyancy during horizontal aquatic flight, alcids in this study seemed to produce quick, low excursion wingbeats with near-horizontal chord angles (α) on the upstroke (Figure 6). Given that the upstroke produces negative heave (ventrally directed acceleration) in swimming alcids (Watanuki et al., 2006), these kinematics seem to be a strategy used to counteract the strong, dorsally oriented buoyancy experienced during horizontal swimming at shallow depths. In contrast, descending alcids must counteract buoyancy as it attempts to resist their forward motion and are, therefore, not required to produce negative heave via the upstroke. Still, all values of St for horizontal aquatic flight overlapped with the range reported for strictly aerial birds in aerial flight – 0.12 < St < 0.47 – (Figure 1), suggesting that alcids produce wakes of similar efficiency to their fully aerial relatives even while fighting buoyancy.

From previous research, the precise range of St values which confer optimal propulsive efficiency (the proportion of total mechanical energy expended that contributes to useful work) depends somewhat on the kinematics of the flapping foil, but departures from that range can have substantial effects (Anderson et al., 1998; Read et al., 2003). Data comparing St to propulsive efficiency in animals are limited, but Rohr and Fish, 2004 report that a relatively minor shift in St in cetaceans (e.g. from 0.25 to 0.35 in Pseudorca crassidens) can reduce propulsive efficiency by 5–10% (Rohr and Fish, 2004). The paucity of data for animals swimming and flying outside the optimal range of St may be due to the challenge of eliciting inefficient kinematics from animals. Alternatively, because translational velocity is partially determined by wing excursion and frequency, the convergence of St on some range of values may be inevitable. The latter seems unlikely, however, as trout adhere to a narrow range of St despite experimentally-induced disruptions to their kinematics (Nudds et al., 2014).

One limitation of this study is that recordings of aquatic flight were made at shallow depths. However, previous work has indicated that velocity (Lovvorn et al., 2004; Watanuki and Sato, 2008; Watanuki et al., 2006), wingbeat frequency (Watanuki et al., 2006), and wing excursion (Kikuchi et al., 2015) of descending birds remain within a narrow range across depths, suggesting that our results apply to wild alcids. Average velocity and wingbeat frequency of common murres during swimming in this study were 1.63 m s⁻¹ and 2.4 Hz, respectively, whereas Watanuki et al., 2006 report 1.61 m s⁻¹ and 2.6 Hz for wild birds (Watanuki et al., 2006).

In moving between air and water, alcids must cope with a dramatic shift to the forces exerted upon them. For example, a bird in aerial flight must counteract the downward pull of gravity, whereas the same bird in shallow water must counteract the upward pull of buoyancy. Recent work with robotics has revealed that a simple shift in stroke-plane angle (β, Figure 1) can allow for both aerial and aquatic propulsion from the same wing (Izraelevitz et al., 2018). The authors of this study point to alcids as their inspiration for exploring stroke-plane angle in a hybrid, flapping wing, but, to our knowledge, our result is the first to confirm that β varies as predicted by Izraelevitz et al., 2018 as dual-medium birds transition between air and water.

The stroke plane is rotated to a greater degree during aerial flight to values that are consistent with strictly aerial fliers (Figure 5; Tobalske et al., 1999). In other words, during the aerial downstroke, while the wing is being depressed alcids also draw the wing forward. To reset the position, alcids elevate and retract the wing during the aerial upstroke. According to Izraelevitz et al., 2018, this stroke-plane angle helps create the vertical force needed to counteract gravity in air. In water, wherein a bird is actually pulled up by buoyancy rather than down by gravity, the top of the stroke plane rotates cranially (Figure 5), allowing the bird to orient net force production to counteract drag (Izraelevitz et al., 2018). Thus, alcids shift stroke-plane angle to cope with the shift in external forces between air and water.

We found no significant relationship between the angle of descent and stroke-plane angle, suggesting that – while stroke-plane angle varies between air and water – alcids do not seem to further modify β to fine-tune the direction of their force output (Figure 5). Instead, alcids appear to change the orientation of their force output during aquatic flight, at least in part, by increasing upstroke chord angle (α) with angle of descent (Figure 6).

While amplitude was greater in water for all species (Figure 4), as expected, stroke durations were dramatically shorter, causing stroke velocities in aerial flight to be ~2X faster than those during aquatic flight (Figure 3). The work of Kikuchi et al., 2015 suggest a similar result for rhinoceros auklets; however, they report nearly equal wingbeat amplitudes across fluids (87 deg in water, 88 deg in air). Our results may differ because we measured wingbeat amplitude in different ways. Kikuchi et al., 2015 relied on the vertical extent of the wingtip in aerial flight and the estimated half-wingspan. Based on our observations, the excursion of the wingtip may not be a reliable measure for inferring contractile velocity. This is because the distal feathers bend considerably during the end of each half-stroke in air, increasing the perceived wingbeat amplitude. This means that stroke velocity measured via the wingtip in aerial flight is not comparable to that measured at the wrist during aquatic flight.

Assuming stroke velocity is proportional to contractile velocity of the major wing muscles, the pectoralis and supracoracoideus, alcids either contract these muscles at inefficient velocities in one or both fluids or maintain a two-geared system – with one set of muscle fibers used for aquatic flight and another for aerial flight. This is because muscle fibers of a given fiber type and myosin isoform are most efficient over a narrow range of contractile velocities (Goldspink, 1977; He et al., 2000; Reggiani et al., 1997; Rome et al., 1988). Alcids have exceptionally long sterna, perhaps allowing for regional specializations in the pectoralis and supracoracoideus (Hamilton, 2006; Kovacs and Meyers, 2000; Stettenheim, 1959). Alternatively, Kovacs and Meyers indicate that the latissimus dorsi caudalis, which is enlarged in alcids, is positioned to retract the wing as occurs during the aquatic downstroke. Thus, alcids may rely on different muscles for powering the downstroke in each fluid (Kovacs and Meyers, 2000). Additionally, previous histology research has documented two, ‘fast’ fiber-types in the muscles (both with fast myosin but differing slightly in oxidative and glycolytic capacities) of Atlantic puffins (Kovacs and Meyers, 2000). These lines of evidence suggest the presence of a two-geared flight system, the number of myosin isoforms in these muscles in alcids or their contractile properties remain unknown.

By maintaining a two-geared system, alcids would avoid the costs of inefficient muscle contractions but would have increased aerial flight costs due to the additional mass of the ‘aquatic gear’ (Ellington, 1984b). In contrast, maintaining the ‘aerial gear’ may actually benefit aquatic performance, as muscle represents a vital oxygen storage site to diving animals (Ponganis, 2015). Consistent with this hypothesis, the metabolic rate of common murres is high in aerial flight but low in aquatic flight (Elliott et al., 2013). Future research should test whether the pectoralis and supracoracoideus muscles contract at different speeds in aerial and aquatic flight and explore in more detail the variation in myosin composition of those muscles to test for a two-geared system. It would be especially interesting to explore the presence of a two-geared system in dippers (genus Cinclus) – the only dual-medium passerine birds – given that passerines often express only one myosin isoform (Rosser et al., 1996).

All data are available at the following link: https://github.com/alapsansky/Lapsansky_Zatz_Tobalske_eLife_2020 (copy archived at https://github.com/elifesciences-publications/Lapsansky_Zatz_Tobalske_eLife_2020).

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Author details

1. Anthony B Lapsansky

   Field Research Station at Fort Missoula, Division of Biological Sciences, University of Montana, Missoula, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Visualization, Methodology, Writing - original draft, Project administration

   For correspondence

   anthony.lapsansky@umontana.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-7530-7830

2. Daniel Zatz

   ZatzWorks Inc, Homer, United States

   Contribution

   Resources, Data curation, Investigation, Writing - review and editing

   Competing interests

   is affiliated with ZatzWorks Inc. The author has no financial interests to declare.

3. Bret W Tobalske

   Field Research Station at Fort Missoula, Division of Biological Sciences, University of Montana, Missoula, United States

   Contribution

   Conceptualization, Resources, Supervision, Methodology, Writing - review and editing

   Competing interests

   No competing interests declared

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