Water or land: are the middle ears of aquatic birds designed to hear in both?

Sound originating on land can be heard underwater but the intensity is much lower as sound waves reflect at the surface of the water. The concept of resistance or impedance of different media is key to understanding how efficiently sound waves can reach the inner ear of animals. In air, the middle ear of vertebrates functions as an amplifier of the sound pressure reaching the inner ear, travelling from air to the fluid of the inner ear. By contrast, in water, the ear needs to amplify the vibration velocity of sound, rather than pressure, and the impedance of the inner ear is typically slightly lower than the surrounding water. Therefore, the directionality of the impedance mismatch is reversed in air versus water. Depending on the hearing requirements of vertebrates and their lifestyles in water and air, adaptations of the middle ear to underwater hearing may constrain hearing sensitivity on land, assuming no other compensatory mechanisms. 

Figure: Exemplars of the species from South Africa included in this study illustrating the broad range of hearing requirements among birds: A. the Cape gannet (Morus capensis) nests in very large and dense colonies but also plunge-dives into water at incredible speeds to forage, creating great strain on the ear; B. the Knysna turaco (Tauraco corythaix) resides in thick evergreen forests in pairs or small groups and uses beautiful songs to communicate with conspecifics; C. the African penguin (Spheniscus demersus) is a pursuit diver, foraging in the open sea but breeds in colonies on land. Several species of penguins have been shown to emit vocalizations underwater, and these are typically associated with fish foraging events [2]. 

Birds represent a great study group to test these ideas because they encompass a tremendous diversity of lifestyles, with differing degrees of amphibious activity. In addition, land-water transitions have occurred several times in distinct groups and several lineages include both aquatic and terrestrial species, or species with different degrees of aquatic exposure (shallow foragers versus underwater-pursuit foragers). There is also increasing evidence that at least some aquatic birds use sound as a reliable sensory signal for detecting prey or communicate with conspecifics. Several species, including ducks, cormorants and penguins, have been shown to respond to sound cues underwater. In addition, a recent study [1] showed that the hearing sensitivity of a cormorant species in water was higher than in air, revealing several specializations of the middle ear to underwater hearing, similar to turtles and aquatic frogs. 

Several mechanisms have been proposed to optimize sound waves reaching the inner ear by modifications of the middle ear (for low frequency sounds, see [3]). For aquatic birds presented with a unique impedance-matching situation underwater, ear anatomy might deviate from the ‘typical’ design, which is well suited for hearing airborne sound. For example, a smaller ratio between the eardrum and the footplate of the columella (the principal ossicle of the ear of birds) would reduce the increase in pressure expected from aerial hearing. Other modifications, such as a more centrally placed columella tip and a more flattened tympanic membrane, are predicted to increase vibration velocity in water. While some of these structural changes may affect sound transmission in the ear, certain modifications can be related to protecting the ear from barometric pressure during diving. For example, stiffer and thicker eardrums can protect the ears from increasing water pressure but a higher stiffness may compromise hearing sensitivity in air. 

We tested these predicted structure-function relationships by scanning heads of naturally deceased birds from 127 species, representing 26 taxonomic orders, and measured specific ear structures expected to affect underwater and aerial hearing. Our results revealed several adaptations of the middle ear to aquatic lifestyles, which recurred in multiple independent bird lineages. Therefore, these findings suggest key modifications that facilitate hearing underwater and protection of the ear from increased pressure in aquatic birds.

Support from the Human Frontier Science Program was essential to support the unparalleled collection of fresh specimens from many locations and sources in South Africa, the sub-Antarctic, Southern Atlantic and Northwestern Europe. We collaborated with researchers from multiple institutions in South Africa and the British Antarctic Survey (UK) to make this happen. The HFSP-funded CTs scans of all the birds taken at nano and micro-scales and the associated comparative analysis have provided a unique opportunity to test several hypotheses relating to structure-function relationships at large scales. As we have uncovered modifications of the middle ear of birds relating to underwater and aerial hearing, we also examine in our next publication, how specific morphological traits of the middle ear of birds relate to their hearing range and sensitivity, with special attention to low frequency sounds.