Cretaceous origins of the vibrotactile bill-tip organ in birds

Abstract

Some probe-foraging birds locate their buried prey by detecting mechanical vibrations in the substrate using a specialized tactile bill-tip organ comprising mechanoreceptors embedded in densely clustered pits in the bone at the tip of their beak. This remarkable sensory modality is known as ‘remote touch’, and the associated bill-tip organ is found in probe-foraging taxa belonging to both the palaeognathous (in kiwi) and neognathous (in ibises and shorebirds) clades of modern birds. Intriguingly, a structurally similar bill-tip organ is also present in the beaks of extant, non-probing palaeognathous birds (e.g. emu and ostriches) that do not use remote touch. By comparison with our comprehensive sample representing all orders of extant modern birds (Neornithes), we provide evidence that the lithornithids (the most basal known palaeognathous birds which evolved in the Cretaceous period) had the ability to use remote touch. This finding suggests that the occurrence of the vestigial bony bill-tip organ in all modern non-probing palaeognathous birds represents a plesiomorphic condition. Furthermore, our results show that remote-touch probe foraging evolved very early among the Neornithes and it may even have predated the palaeognathous–neognathous divergence. We postulate that the tactile bony bill-tip organ in Neornithes may have originated from other snout tactile specializations of their non-avian theropod ancestors.

Comparative morphology and soft tissue histology of the remote‐touch bill‐tip organ in three ibis species of differing foraging ecology

“…Like Glossy Ibises, they have high numbers of foramina which are densely packed together (see du Toit Kiwi follow the trend shown in ibises in terms of the relationship between their bill-tip organ bone morphology and habitat usage (Cunningham, Alley, et al, 2010a). With reference to our study sample, kiwi have relatively high numbers of Herbst corpuscles per pit, and similar foramen size and pitting extent to Hadeda Ibises (Cunningham et al, 2007(Cunningham et al, , 2013du Toit et al, 2020). This further reinforces that this type of bill-tip organ morphology is suitable for remote-touch foraging in drier substrates, and that this has evolved convergently between ibises and kiwi.…”

The True Identity of Putative Tooth Alveoli in a Cenozoic Crown Bird, the Gastornithid Omorhamphus

“…The latter grooves also characterize adult Sylviornis beaks (Mourer-Chauviré and Balouet, 2005) as opposed to juvenile ones (Figure 5B). The remnant pits on the rostral part of adult beaks can be compared with those visible in several extant birds, including those of some ratites which have been interpreted as being related to a sensory bill tip organ (Crole and Soley, 2017;du Toit et al, 2020). The deep grooves in adult Gastornis and Sylviornis are vascular grooves on the surface of the bone that have been interpreted as necessary to maintain and nourish a thick rhamphotheca (Mourer-Chauviré and Balouet, 2005) and their exclusive presence in adults presumably indicates that their formation took place after the cessation of primary bone growth.…”

The Evolution and Fossil Record of Palaeognathous Birds (Neornithes: Palaeognathae)

“…This suggests they could have used their bills for probing the substrate for food items, in a manner more similar to kiwi than tinamous [62]. Additional evidence for this type of foraging behaviour comes from the recognition of mechanoreceptors known as Herbst corpuscles in the rostrum of lithornithids [80], which form a tactile bill-tip organ that picks up mechanical vibrations to detect buried prey.…”

“…Vibrotactile bill tips in Lithornis promiscuus and Paracathartes howardae may have been associated with probe-feeding in the ground, an interpretation congruent with the hypothesis of predominant K-Pg survivorship among non-arboreal taxa. A vibrotactile bill tip organ composed of mechanoreceptors known as Herbst corpuscles embedded within the bone was hypothesized to be a plesiomorphy of Neornithes by du Toit, et al [80], which would support the neornithine MRCA and its immediate descendants as having been ground-foraging birds. Such organs are found in palaeognathous and neognathous probe-foragers, enabling them to locate prey buried in substrate through vibration detection [487,488].…”

“…Such organs are found in palaeognathous and neognathous probe-foragers, enabling them to locate prey buried in substrate through vibration detection [487,488]. In non-probe-foraging palaeognaths, the vibrotactile bill tip organ is vestigial [80,489]. The hypothesis that lithornithids and the palaeognath MRCA were probe-feeders agrees with ideas put forth by Houde [62], who suggested that lithornithids may have preferred to live near water and probed for food using their long beaks, noting the similarity of their jaw apparatus to those of kiwi.…”