Aquatic birds have middle ears adapted to amphibious lifestyles

Abstract

Birds exhibit wide variation in their use of aquatic environments, on a spectrum from entirely terrestrial, through amphibious, to highly aquatic. Although there are limited empirical data on hearing sensitivity of birds underwater, mounting evidence indicates that diving birds detect and respond to sound underwater, suggesting that some modifications of the ear may assist foraging or other behaviors below the surface. In air, the tympanic middle ear acts as an impedance matcher that increases sound pressure and decreases sound vibration velocity between the outside air and the inner ear. Underwater, the impedance-matching task is reversed and the ear is exposed to high hydrostatic pressures. Using micro- and nano-CT (computerized tomography) scans of bird ears in 127 species across 26 taxonomic orders, we measured a suite of morphological traits of importance to aerial and aquatic hearing to test predictions relating to impedance-matching in birds with distinct aquatic lifestyles, while accounting for allometry and phylogeny. Birds that engage in underwater pursuit and deep diving showed the greatest differences in ear structure relative to terrestrial species. In these heavily modified ears, the size of the input areas of both the tympanic membrane and the columella footplate of the middle ear were reduced. Underwater pursuit and diving birds also typically had a shorter extrastapedius, a reduced cranial air volume and connectivity and several modifications in line with reversals of low-to-high impedance-matching. The results confirm adaptations of the middle ear to aquatic lifestyles in multiple independent bird lineages, likely facilitating hearing underwater and baroprotection, while potentially constraining the sensitivity of aerial hearing.

Figure 1

(a) Three-dimensional rendering of a typical terrestrial bird ear built from a micro-CT scan of a rock dove Columba livia, highlighting the tympanic membrane (orange), the trifurcated and cartilaginous extracolumella (blue), the columella bone (black), the inner ear (grey), the round window (white arrow) and cochlear aqueduct (black arrow). (b) Hypothesized anatomical differences between a bird ear typical of terrestrial species and thus adapted for aerial hearing (top row) versus one adapted for underwater hearing (bottom row). From aerial to aquatic, we expect (i) a reduction of the tympanic membrane-to-columella footplate area ratio (shown as a reduction in tympanic membrane area), (ii) a reduced offset (thin grey line) of the columella from the center of the eardrum, resulting in a smaller lever ratio (l₁ and l₂ indicate the lever arms), (iii) a flattened tympanic membrane, quantified as the height of the umbo and the angles at the periphery relative to the base plane of the tympanic membrane, (iv) a reduced area of the round window to raise total inner ear impedance, (v) a shorter extrastapedius, here used as a proxy of overall extracolumella stiffness (dotted line), (vi) hypertrophication of the columella, and (vii) enlargement of the cochlear aqueduct (represented by a curved indentation). (c) Summary of hypothesized differences in the ear of terrestrial (left) vs aquatic birds (right), combined with expectation of reduced cranial air and connectivity, interaural canal and interbullar passage between the two ears.

Figure 2

Phylogeny of species included in this study, labelled by four ecological groupings (terrestrial, surface-foraging, plunge-diving, and underwater pursuit) (inner ring), and classification of dive capability with highest point scores corresponding to deepest divers (outer ring). The phylogeny was constructed using a backbone based on published trees and species-level relationships using a ‘Hackett Stage 2’ phylogeny available online (www.birdtree.org).

Figure 3

(a) Loading plots for pPC1 and pPC2 (TM stands for tympanic membrane) with inset bar plot of percent variance explained for first six principal components. (b) Scatterplot of pPC1 and pPC2 grouped by ecological groups. Several extreme scores are highlighted: owls (Bubo africanus and Tyto alba) on the negative pPC1 end and Phalacrocorax cormorants (P. lucidus, P. capensis, P. neglectus) on the positive pPC1 end. (c) Scatterplot of pPC1 and pPC2 grouped by dive score with increasing value of pPC1 indicating smaller values of most morphological measurements for a given head mass. (d) Scatterplot of pPC1 and pPC2 grouped by orders with at least one underwater-pursuit species. The diversity within Charadriiformes is highlighted by low pPC1 scores in two terrestrial species (Burhinus capensis, Vanellus coronatus) and high pPC1 scores in three diving species (Alca torda, Fratercula arctica, Cepphus grylle). Silhouette images provided by PhyloPic’s database (http://phylopic.org/), see electronic supplemental materials S8 for detailed credits.

Figure 4

Relative sizes of auditory structures, adjusted for head mass and phylogenetic relatedness and grouped by ecological group (a) and order (b). Data are residuals of univariate PGLS regressions relating head mass with each respective ear measure, both as log-transformed variables. Negative values (left of the black vertical lines) indicate smaller values than expected for the bird’s head mass, and positive values indicating greater values than expected. Box plots show the distributions of residuals by ecological group in (a) and individual data points represent different species in (b). Colors indicate ecological groups (white for terrestrial, orange for surface-foraging, black for plunge-diving, blue for underwater-pursuit). (i) tympanic membrane area, (ii) columella footplate area, (iii) tympanic membrane-to-columella footplate area ratio, (iv) columella offset from center of tympanic membrane, (v) umbo height, (vi) tympanic membrane angle, (vii) round window area (RW), (viii) cochlear aqueduct area (CA), (ix) extrastapedius length, (x) columella length, (xi) columella volume (xii) cranial air volume. An asterisk is present if the best-supported model for that ear measure included ecological group. In panels xiii and xiv, bar plots indicate the proportions for three levels of cranial air connectivity for the interaural canal and interbullar passage, respectively (white for air-filled connection, grey for connection present but filled with soft tissue, black signifies no pneumatic opening in the bone).