Evolution and Ecology of Silent Flight in Owls and Other Flying Vertebrates.

Owls are famous for their relatively silent flight. Most birds produce an audible signature with every flap of their wings, but the wing noise of many (though not all) owls is low enough that a human often does not hear an owl flying by, even at close range. Why have they evolved to do this? The answer is not entirely clear. Here we explore answers to three intertwined questions about the evolution of silent flight. The questions are: (1) do owls fly silently to reduce self-masking, or for stealth during an ambush? (2) Do wing features that promote silent flight do so by suppressing aerodynamic sound, or by suppressing structural sound, such as made by friction between feathers during flapping? And, (3) has silent flight convergently evolved in flying animals with ecological similarities to owls, such as nightbirds (nocturnal members of Caprimulgiformes), or hawks? Research on this topic has focused narrowly on owls, and many works imply that owls are unique or the only birds to have evolved silent flight (Kroeger et al. 1972; Lilley 1998). Might other flying taxa such as harriers or nightbirds also offer simple, general lessons about silent flight? Our purpose in asking these questions is two-fold. First, we review what is known about the evolution and ecology of silent flight, hunting, and nocturnality. Two disparate fields have extensively studied questions on either side of this topic: Engineers have studied the physical acoustics of owl flight, most often in a simple aerodynamic context such as a dried, spread owl wing placed in a wind tunnel, intended to simulate sounds of gliding flight (e.g., Kroeger et al. 1972). Sensory neurobiologists have studied owl hearing, mainly in Barn Owls (Tyto alba), as a model system of how the brain localizes sound (e.g., Konishi 1973a; Knudsen and Konishi 1979). In between the ground covered by these two fields is the sensory and evolutionary ecology of sound in owl hunting. Here, we explore this space in between aerodynamics and neurobiology. We cover both how and why owls fly silently, since, in functional morphology, how a trait works is linked to why it has evolved. Our purpose is to point out tractable questions about silent flight that a biologist should be able to answer. Second, we examine a few of the assumptions about owl flight that are currently widespread in the literature. Some of the terminology and ideas that we revisit have their origin in Graham’s (1934) foundational paper, “The silent flight of owls.” This is the landmark paper on this topic: Graham appears to have been the first to establish the owl wing morphologies associated with the acoustics of owl flight. While most of his ideas about mechanism have stood the test of time, a few are wrong or oversimplified. For instance, his term “trailing edge fringe” has misled subsequent authors for reasons we describe below. Current owl flight literature implies the mechanisms by which owl wings reduce noise in flight are aerodynamic mechanisms, caused by noise made by air flowing over the wing. For example, a recent review of owl wing features focused almost exclusively on postulated aerodynamic mechanisms (Wagner et al. 2017), and scarcely mentioned that there is another explanation for two wing features, the velvet and the vane fringes, given in books on raptor biology (e.g., Duncan 2003; Peeters 2007) or feather anatomy (Lucas and Stettenheim 1972). Below we develop this alternative and the empirical support for it, a version of which was originally proposed by Graham (1934), which we call the structural noise hypothesis. The central idea is that feathers make substantial frictional sound when they rub against each other (Lucas and Stettenheim 1972) and impact sounds during other physical interactions such as in impacts against other structures such as dry grass. Owl diversity and phylogeny Owls (clade Strigiformes) are a natural (monophyletic) group (Fig. 1A). Owls have two major subclades, the barn owls (Tytonidae, ∼20 spp.) and “true” owls (Strigidae, ∼200 spp.) (Uva et al. 2018). Tytonids are medium to large (187–1260 g), and generally have a mammalian diet (Bruce 1999). Strigids vary by two orders of magnitude in size, from the 40 g Elf Owl (Micrathene whitneyi) (Holt et al. 1999a) to the Eurasian Eagle Owl (Bubo bubo), which can weigh up to 4 kg (Holt et al. 1999b). All owls are predators of other animals, which they hunt on the wing. Small owl species tend to eat insects, whereas large species eat mammals, fish, birds, or a mix. Most are nocturnal or crepuscular, and a few are diurnal. This diurnal/nocturnal divide does not always cleanly separate owls into visually hunting versus acoustically hunting species. Species hunting in daylight, such as Snowy (Bubo scandiacus) or Great Gray Owl (Strix nebulosa) may nevertheless be entirely reliant on acoustic cues to detect prey, when they hunt prey under a layer of snow or other visual barrier (Chamberlin 1980). Hearing is acute in some owl species, and many species have specializations associated with hearing, such as an enlarged facial disc and asymmetrical ears (section “Facial disc”). Owls have evolved specialized wing features that are related to sound production while hunting (section “How do owls have silent flight?”). Open in a separate window Fig. 1 Phylogenetic distribution of dorsal velvet, fringed vanes, and leading-edge comb. A) Phylogeny of major owl genera (modified from Wink et al. 2009). Red: leading-edge comb extends >1 mm from surface of P10 (as measured at the midpoint of the comb) in at least one species within each clade. Red dash: leading-edge comb present but extends <1 mm at midpoint of the comb. B) within extant flying vertebrate clades (phylogeny from Prum et al. 2015). Clades with at least one species with a character are marked (i.e., out of ∼5000 passerine species, since the two Stelgidopteryx spp. have a comb-like structure, the entire clade is indicated as short comb present). Black: no data; true absence data are lacking.