Inner-Ear Morphology of the New Zealand Kiwi (Apteryx mantelli) Suggests High-Frequency Specialization

Abstract

The sensory systems of the New Zealand kiwi appear to be uniquely adapted to occupy a nocturnal grounddwelling niche. In addition to well-developed tactile and olfactory systems, the auditory system shows specializations of the ear, which are maintained along the central nervous system. Here, we provide a detailed description of the auditory nerve, hair cells, and stereovillar bundle orientation of the hair cells in the North Island brown kiwi. The auditory nerve of the kiwi contained about 8,000 fibers. Using the number of hair cells and innervating nerve fibers to calculate a ratio of average innervation density showed that the afferent innervation ratio in kiwi was denser than in most other birds examined. The average diameters of cochlear afferent axons in kiwi showed the typical gradient across the tonotopic axis. The kiwi basilar papilla showed a clear differentiation of tall and short hair cells. The proportion of short hair cells was higher than in the emu and likely reflects a bias towards higher frequencies represented on the kiwi basilar papilla. The orientation of the stereovillar bundles in the kiwi basilar papilla showed a pattern similar to that in most other birds but was most similar to that of the emu. Overall, many features of the auditory nerve, hair cells, and stereovilli bundle orientation in the kiwi are typical of most birds examined. Some features of the kiwi auditory system do, however, support a high-frequency specialization, specifically the innervation density and generally small size of hair-cell somata, whereas others showed the presumed ancestral condition similar to that found in the emu.

Is Cerebellar Architecture Shaped by Sensory Ecology in the New Zealand Kiwi <b><i>(Apteryx mantelli)</i></b><b>?</b>

“…Another factor that could influence the size/structure of the central zone is that it also receives acoustic and possibly trigeminal inputs [Snider and Stowell, 1944;Whitlock, 1952;Voogd and Barmack, 2006]. Kiwi have evolved a sensitivity to a specific high-frequency band [Corfield et al, 2011[Corfield et al, , 2012 and have a highly specialized beak (see below) which may require additional processing in the cerebellum. However, we require a better understanding of how the input to the central region is used in specific motor and nonmotor systems in birds before we can comment on how these systems influence the cerebellum.…”

“…Kiwi have evolved an impressive arsenal of sensory specializations to occupy a nocturnal ground-dwelling niche, with increased sensitivities to specific sound frequencies [Corfield et al, 2011[Corfield et al, , 2012, a long beak with a cluster of touch-sensitive mechanoreceptors at its tip [Cunningham et al, 2013], and an acute sense of smell [Cunningham et al, 2009;Castro et al, 2010;. In contrast, kiwi have evolved a much reduced visual system [Craigie, 1930;Martin et al, 2007].…”

Anatomical Specializations for Enhanced Olfactory Sensitivity in Kiwi, <b><i>Apteryx mantelli</i></b>

“…Indeed, all olfactory structures in kiwi are large and well developed: they have a high number of functionally intact olfactory receptor genes in their genome [Steiger et al, 2008[Steiger et al, , 2009 and they have adaptations such as a long beak with nostrils at its tip. Therefore, together with their specialized auditory and tactile systems [Corfield et al, 2011[Corfield et al, , 2012aCunningham et al, 2007Cunningham et al, , 2009Cunningham et al, , 2013, kiwi appear to have evolved an olfactory system well tuned to utilizing olfaction to function in their nocturnal and ground-dwelling niche. This reliance on olfactory rather than visual information is reminiscent of the situation of many nocturnal mammals.…”

“…are entirely ground dwelling and uniquely adapted for their nocturnal activities in native forests of New Zealand. Kiwi have a specialized auditory system, possibly tuned to locating prey using auditory cues [Corfield et al, 2011[Corfield et al, , 2012a, and have developed whiskerlike facial bristles to help navigate a nocturnal environment , together with a highly regressed visual system [Martin et al, 2007]. In addition, kiwi have a long, slightly curved beak, with nostrils at the tip and a specialized bill tip organ, all used to locate and extract hidden invertebrate prey including earthworms and beetle larvae from soil, leaf litter, rotting wood, and damp sand [Colbourne, 1983;Cunningham et al, 2007Cunningham et al, , 2009Cunningham et al, , 2013Martin et al, 2007;Potter, 1989;Reid et al, 1982;Taborsky and Taborsky, 1995;Watt, 1971].…”

A unique cellular scaling rule in the avian auditory system

“…In addition, we expect that the number of hair cells and nerve fibers in the inner ear will be positively correlated with neuron numbers in the cochlear nuclei. In chicken, the ratio of hair cells to nerve fibers is close to 1 (Corfield et al 2012a;Köppl et al 2000); therefore if the size of NM or NL is dependent on the amount of auditory input, we would expect the ratio of hair cells to brain neurons in these regions in galliforms to be also close to 1.…”