High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins

Flight is a key adaptive trait. Despite its advantages, flight has been lost in several groups of birds, notably among seabirds, where flightlessness has evolved independently in at least five lineages. One hypothesis for the loss of flight among seabirds is that animals moving between different media face tradeoffs between maximizing function in one medium relative to the other. In particular, biomechanical models of energy costs during flying and diving suggest that a wing designed for optimal diving performance should lead to enormous energy costs when flying in air. Costs of flying and diving have been measured in free-living animals that use their wings to fly or to propel their dives, but not both. Animals that both fly and dive might approach the functional boundary between flight and nonflight. We show that flight costs for thick-billed murres (Uria lomvia), which are wing-propelled divers, and pelagic cormorants (Phalacrocorax pelagicus) (foot-propelled divers), are the highest recorded for vertebrates. Dive costs are high for cormorants and low for murres, but the latter are still higher than for flightless wing-propelled diving birds (penguins). For murres, flight costs were higher than predicted from biomechanical modeling, and the oxygen consumption rate during dives decreased with depth at a faster rate than estimated biomechanical costs. These results strongly support the hypothesis that function constrains form in diving birds, and that optimizing wing shape and form for wing-propelled diving leads to such high flight costs that flying ceases to be an option in larger wing-propelled diving seabirds, including penguins.

飞行是一项关键的适应性性状。尽管飞行具备诸多演化优势，但多个鸟类类群已丧失飞行能力，其中海鸟类群尤为典型——至少有5个独立演化支系分别演化出了失飞性状。针对海鸟失飞现象，有一项假说认为：在不同介质间移动的动物，需在两种介质的功能最优化之间权衡取舍。具体而言，飞行与潜水过程中的能量消耗生物力学模型显示：若翅膀演化至最优潜水性能，则其在空气中飞行时的能量消耗将极为高昂。目前已有研究对以翅膀飞行或驱动潜水的野生个体的飞行与潜水能耗分别进行了测定，但尚未有同时测定两类能耗的相关报道。兼具飞行与潜水能力的动物，可能正处于飞行与失飞之间的功能边界地带。本研究显示，翼驱动潜水的厚嘴海鸦（Uria lomvia）与足驱动潜水的远洋鸬鹚（Phalacrocorax pelagicus）的飞行能耗，均为脊椎动物中已记录的最高值。鸬鹚的潜水能耗较高，而海鸦的潜水能耗较低，但海鸦的潜水能耗仍高于不会飞行的翼驱动潜水鸟类——企鹅。对于海鸦而言，其飞行能耗高于生物力学模型的预测值；且潜水过程中的耗氧速率随水深增加的下降速率，快于生物力学模型估算的能耗下降速率。上述研究结果强有力地支持了以下假说：潜水鸟类的形态受其功能约束；为适配翼驱动潜水而优化的翅膀形态，会使飞行能耗变得极高，以至于包括企鹅在内的大型翼驱动潜水海鸟，已无法再具备飞行能力。