The Anatomy of the bill Tip of Kiwi and Associated Somatosensory Regions of the Brain: Comparisons with Shorebirds

Abstract

Three families of probe-foraging birds, Scolopacidae (sandpipers and snipes), Apterygidae (kiwi), and Threskiornithidae (ibises, including spoonbills) have independently evolved long, narrow bills containing clusters of vibration-sensitive mechanoreceptors (Herbst corpuscles) within pits in the bill-tip. These ‘bill-tip organs’ allow birds to detect buried or submerged prey via substrate-borne vibrations and/or interstitial pressure gradients. Shorebirds, kiwi and ibises are only distantly related, with the phylogenetic divide between kiwi and the other two taxa being particularly deep. We compared the bill-tip structure and associated somatosensory regions in the brains of kiwi and shorebirds to understand the degree of convergence of these systems between the two taxa. For comparison, we also included data from other taxa including waterfowl (Anatidae) and parrots (Psittaculidae and Cacatuidae), non-apterygid ratites, and other probe-foraging and non probe-foraging birds including non-scolopacid shorebirds (Charadriidae, Haematopodidae, Recurvirostridae and Sternidae). We show that the bill-tip organ structure was broadly similar between the Apterygidae and Scolopacidae, however some inter-specific variation was found in the number, shape and orientation of sensory pits between the two groups. Kiwi, scolopacid shorebirds, waterfowl and parrots all shared hypertrophy or near-hypertrophy of the principal sensory trigeminal nucleus. Hypertrophy of the nucleus basorostralis, however, occurred only in waterfowl, kiwi, three of the scolopacid species examined and a species of oystercatcher (Charadriiformes: Haematopodidae). Hypertrophy of the principal sensory trigeminal nucleus in kiwi, Scolopacidae, and other tactile specialists appears to have co-evolved alongside bill-tip specializations, whereas hypertrophy of nucleus basorostralis may be influenced to a greater extent by other sensory inputs. We suggest that similarities between kiwi and scolopacid bill-tip organs and associated somatosensory brain regions are likely a result of similar ecological selective pressures, with inter-specific variations reflecting finer-scale niche differentiation.

Neuronal mechanism for acute mechanosensitivity in tactile-foraging waterfowl

“…Previous studies of the biophysical basis of mechanosensitivity have focused on the density, morphology, and functional specialization of mechanoreceptors in waterfowl (4,6,7,10) as well as other avian (33)(34)(35) and nonavian species (1, 2) with acute mechanosensitivity. To our knowledge, our data demonstrate for the first time that in domestic and wild tactile-foraging ducks, somatosensory neurons themselves are key contributors to enhanced mechanosensitivity.…”

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

“…Online supplementary table S1 also indicates the common name and order of each species. Data were compiled from the studies of Ebinger and Lohmer [1984], Corfield et al [2012b], Boire [1989], Cunningham et al [2013], Pistone et al [2002], Rehkamper et al [1991], Carezzano and Bee De Speroni [1995], Mehlhorn et al [2010], Fernandez et al [1997], and Alma and Bee De Speroni [1992]. Additional data on olfactory bulb size in California quail (Callipepla californica), black-winged stilt (Himantopus himantopus), South Island oystercatcher (Haematopus finschi), ostrich (S. camelus), and red-winged tinamou (R. rufescens) were obtained from the same specimens used in the studies of Cunningham et al [2013] and Corfield et al [2012c].…”

“…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.…”

“…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]. Likely as a result of their many unique sensory adaptations, the brain of the kiwi has also undergone many changes, including an enlarged telencephalon [Corfield et al, 2008] resulting from enlargements to specific telencephalic regions [Corfield et al, 2012b].…”

“…Likely as a result of their many unique sensory adaptations, the brain of the kiwi has also undergone many changes, including an enlarged telencephalon [Corfield et al, 2008] resulting from enlargements to specific telencephalic regions [Corfield et al, 2012b]. In addition, the principal sensory trigeminal nucleus (PrV) and the nucleus basorostralis (Bas) [Cunningham et al, 2013], both of which process tactile information from the beak, are enlarged, whereas there is a reduction of all visual nuclei [Corfield, 2009;Martin et al, 2007].…”