Erin Carter
7616892
LISTENING FOR LUNCH:
PREY DETECTION IN THE
HEARING OF BARN OWLS (Tyto alba)
1
The use of different sensory systems in prey detection varies greatly between vertebrate
groups. Mammals, for example, generally rely on well-developed olfaction whereas birds tend to
use visual information in combination with hearing (Beason 2004). While hearing is important in
both lineages, the independent evolution of the two groups resulted in the emergence of similar
and differing inner ear structures (Köppl 2011). Among the birds, owls display the highest
acoustic sensitivity of at least 9 kHz (Wagner et al. 2013) and up to around 10 kHz, comparable
to the hearing of humans and cats (Konishi 1973; Köppl 2011) (Figure 1). Barn owls (Tyto alba)
represent a species that is highly adapted to locating prey using hearing alone, making them the
model for numerous studies on their specialized auditory systems (Payne and Drury 1958;
Konishi 1973; Takahashi 2010; Hausmann et al. 2009; Wagner et al. 2013). This paper will
highlight these acoustic specializations, related to the asymmetry of the ears and facial ruff, inner
ear elements, and silent flight which aid in the optimization of prey capture.
The localization of sound and directional hearing are quite sensitive in owls, despite a
smaller body size and short distance between the ears (Schwartzkopf 1955). The ability of the
barn owl to hunt and capture prey using only auditory cues was shown in early experiments
under complete darkness, where its sense of hearing was isolated from visual, chemical,
magnetic, and electrical senses (Payne and Drury 1958; Payne 1971; Konishi 1973). Payne and
Drury (1958) initially demonstrated that when a mouse was a towing a rustling piece of paper
behind its tail, the owl would strike the noisy paper and not the quietly walking mouse. Thus it
was concluded that the barn owl mainly uses hearing to locate its prey, that vision is not
necessary for hunting, and that it is not capable of detecting prey by body heat or sense of smell
(Payne and Drury 1958; Konishi 1973).
2
Unlike humans and other mammals, the barn owl (and all birds) lack a pinna or external
ear, which is used to increase ear sensitivity and concentrate sound (Beason 2004). However,
barn owls have a non-homologous structure that is similar in function to the pinna; a skin fold
that extends from the forehead and behind the ear opening, carrying the densely packed reflector
feathers of the facial disc (Konishi 1973) (Figure 2). To demonstrate the importance of the heartshaped facial ruff in sound localization, studies where feathers of the ruff are removed were
completed (Konishi 1973; Hausmann et al. 2009). In both cases it was noted that large errors
were made in localizing sound after removal, by landing short of the target, after an initial 10
decibel sound level increase in the Konishi experiement (1973). These results suggest that the
facial ruff acts as a parabolic sound reflector and amplifier of up to 10 decibels towards the ear
openings (Konishi 1973; Wagner et al. 2013). This is accomplished through improving the
azimuthal and elevational sound localization by increasing the difference in arrival time of a
sound between the two ears and interaural intensity differences (Hausmann et al. 2009).
Complimenting the facial ruff in sound localization are the asymmetrical positions of the
external ear openings. In Tyto alba, this asymmetry arises from soft tissues rather than skull
morphology, where the left ear opening and skin flap are higher than the right side (GutiérrezIbáñez et al. 2011) (Table 2). Such an adaptation allows for lateral displacement between the
ears, where a vertical position increases hearing in azimuth and elevation at the external auditory
meatus, but not in the middle and inner ear (Norberg 1968; Payne 1971). Gutiérrez-Ibáñez et al.
(2011) summarizes the differences in symmetrically and asymmetrically eared owl species,
where the latter shows a larger number of cells in the auditory brainstem nuclei as well as larger
auditory pathways.
3
Birds only have a single columella (stapes) versus the three in mammals that serve to
transmit sound vibrations from the tympanum to the oval window of the inner ear or cochlea
(Beason 2004). The cochlea of the owl, where hearing takes place, is relatively straight in
comparison to the long, coiled cochlea of mammals (Beason 2004). This distinction is important
because longer cochlea lengths allow for greater sound reception and better acoustic sensitivity
at a specific range or over a wider range (Beason 2004). This pattern is typically seen in avian
species like the pigeon, where a short cochlea length of 5 mm corresponds to a narrower
sensitive hearing range between 1 to 2 kHz (Schwartzkopff 1968; Smith 1985). Only one tenth
the length of mammals, the cochlea length may be over 1 cm in barn owls, containing ten times
as many hair cells which aid in sound amplification (Schwartzkopff 1968; Smith 1985; Köppl
2011). In addition, owls have the largest tympanic membrane relative to their head size, further
enhancing auditory sensitivity (Schwartzkopf 1955, 1968). Because of this, barn owls and other
large nocturnal owls exhibit both good hearing and a wide range of frequency sensitivities as an
exception in the avian group (Konishi 1973) (Table 1).
Apart from those adaptations relating strictly to the hearing sensory system, T. alba also
relies on features of its wing morphology to indirectly locate prey. The wings of the owl are
highly specialized in that “the leading edge comb-like serrations, the trailing edge fringes on
each feather and their velvet-like upper surface” all contribute to air flow over the wing that
allows for “silent flight” (Bachmann et al. 2007). Reducing flight noise of frequencies more than
2 kHz is imperative as a hunting strategy because this noise is reduced within the owl’s best
hearing range and also within the hearing spectrum of the owl’s prey (Konishi 1973; Bachmann
et al. 2007). As a result, the barn owl is able to use a variety of anatomical features for
4
specialized hearing in combination with its silent flight to hover over a location and listen for its
target without being detected by the prey itself.
5
References
Bachmann, T., Klän, S., Baumgartner, W., Klaas, M., Schröder, W., and Wagner, H. 2007.
Morphometric characterisation of wing feathers of the barn owl Tyto alba pratincola and
the pigeon columba livia. Front. Zool. 4: 23-37.
Beason, R.C. 2004. What can birds hear? USDA National Wildlife Research Centre. Paper 78.
Gutiérrez-Ibáñez, C., Iwaniuk, A.N., & Wylie, D.R. 2011. Relative size of auditory pathways
in symmetrically and asymmetrically eared owls. Brain Behav. Evolut. 78(4): 286-301.
Hausmann, L., von Campenhausen, M., Endler, F., Singheiser, M., and Wagner, H. 2009.
Improvements of sound localization abilities by the facial ruff of the barn owl (Tyto alba)
as demonstrated by virtual ruff removal. Plos One. 4(11): 1-13.
Konishi, M. 1973. How the owl tracks its prey. Am. Sci. 61(4): 414-424.
Köppl, C. 2011. Birds – same thing, but different? Convergent evolution in the avian and
mammalian auditory systems provides informative comparative models. Hearing Res.
273(1–2): 65-71.
Miller, J. D., C. S. Watson, and W. I. Covell. 1963. Deafening effects of noise on the cat. Acta
Oto-laryngol. Supp. 176:1-91.
6
Norberg, Å. 1968. Physical factors in directional hearing in Aeogolius funereus (Linne)
(Strigiformes) with special reference to the significance of the asymmetry of the external
ears. Arkiv. f. Tool. 20:181-204.
Payne R.S. and Drury W.H. Jr. 1958. Marksman of the darkness. Part 2. Nat. Hist. NY. 67: 316–
323.
Payne, R.S. 1971. Acoustic location of prey by barn owls (Tyto alba). Exp. Biol. 56: 535-73.
Schwartzkopf, J. 1955. On the hearing of birds. Auk. 72: 340–347.
Schwartzkopf, J. 1968. Structure and function of the ear and auditory brain areas in birds. In:
A. V. S. de Reuck and J. Knight (Eds.), Hearing Mechanisms in Vertebrates. Little
Brown, Boston, MA.
Sivian, L. J., and S. C. White. 1933. On minimum audible sound fields, J. Acoust. Soc. Am.
4:288-321.
Smith, C.A. 1985. Inner ear. In: A. S. King J. McLelland (Eds.), Form and Function in Birds,
Vol. 3. Academic Press, New York, NY.
Takahashi, T.T. 2010. How the owl tracks its prey - II. J. Exp. Biol. 213: 3399-3408.
doi: 10.1242/jeb.031195
Wagner, H., Kettler, L., Orlowski, J., & Tellers, P. 2013. Neuroethology of prey capture in the
barn owl (Tyto alba L.). J. Physiology-Paris. 107(1–2): 51-61.
7
Table 1. Ranges of hearing sensitivities of owl species with the pigeon (rock dove) (adapted
from Beason 2004)
Species
Lower Limit
(Hz)
Most Sensitive
(kHz)
Barn Owl (Tyto alba)
Eagle Owl (Bubo bubo)
60
Great Horned Owl
60
1
Upper Limit
(kHz)
Reference
12.5
Konishi 1973
8
Trainer 1946
7
Edwards 1943
(Bubo virginianus)
Long Earred Owl (Asio
otus)
100
6
18
Schwartzkopff 1955
Tawny Owl (Strix
aluco)
100
3-6
21
Schwartzkopff 1955
Rock Dove (Columba
livia)
50
1.8-2.4
11.5
Weaver and Bray 1946
7.5
Brand and Kellog 1939a
200
300
1-4
Heise 1953
300
1-2
Trainer 1946
0.05
Kreithen and Quine 1979
8
Table 2. Summary and differences in the details of the type of ear symmetry or asymmetry
found in eight owl species (Gutiérrez-Ibáñez, et al. 2011).
9
Fig. 1. Comparison of the minimum hearing levels between humans, cats, and barn owls,
showing the similar sensitivities of cats and barn owls, where they can hear extremely faint
sounds that man cannot (Sivian and White 1933; Miller, Watson, and Covell 1963; Konishi
1973).
10
Fig. 2. Specialized features on the head of the barn owl. The forward-facing eyes and heartshaped structure of the facial ruff aid and audition for prey capture. The auricular feathers in the
middle ruff (white dot) are less ramified and are sound transparent. The feathers at the border of
the ruff (white triangle) are called reflector feathers and are densely ramified, acting as sound
reflectors (Wagner et al. 2013).