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.
Highlights
One of the most diverse characteristics of birds is the bill
North Island brown kiwi (Apteryx mantelli), bar-tailed godwits (Limosa lapponica), South Island oystercatchers (Haematopus finschi), black-winged stilts (Himantopus himantopus) and masked lapwings (Vanellus miles) are protected in New Zealand and permission to use these specimens for research was obtained under permits NO-16732-FAU, NO-18095-DOA, WC-17552-DOA, WE-333RES, WA-24648-RES, NO-27881-RES from the New Zealand Department of Conservation
Kiwi share with scolopacids a bill-tip organ consisting of mechanoreceptors clustered within sensory pits, and a hypertrophied PrV
Summary
One of the most diverse characteristics of birds is the bill. Bills are uniquely adapted to carry out a multitude of functions, including preening, manipulating objects, fighting, courtship, feeding young and most importantly, the acquisition and handling of food. At least five clades of birds have bills containing high concentrations of these mechanoreceptors: waterfowl (Anseriformes), parrots (Psittaciformes), shorebirds (Charadriiformes, Scolopacidae), ibises and spoonbills (Ciconiiformes, Threskiornithidae) and kiwi (Apterygiformes, Apterygidae) [1,4,5,6,7,8,9,10,11,12,13,14,15,16]. Waterfowl possess parrot-like papillae that emerge from the deep dermis behind the keratinaceous nail of the bill tip, as well as sensory pits containing mechanoreceptors in the distal portions of the bill bones [1,4]. Whether configured within touch papillae or sensory pits, these dense clusters of mechanoreceptors at the bill tips are commonly referred to as a ‘bill-tip organs’ (e.g. [1,7])
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