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

Ibises (order: Pelecaniformes, family: Threskiornithidae) are probe-foraging birds that use 'remote-touch' to locate prey items hidden in opaque substrates. This sensory capability allows them to locate their prey using high-frequency vibrations in the substrate in the absence of other sensory cues. Remote-touch is facilitated by a specialised bill-tip organ, comprising high densities of mechanoreceptors (Herbst corpuscles) embedded in numerous foramina in the beak bones. Each foramen and its associated Herbst corpuscles make up a sensory unit, called a 'sensory pit'. These sensory pits are densely clustered in the distal portion of the beak. Previous research has indicated that interspecific differences in the extent of sensory pitting in the beak bones correlate with aquatic habitat use of ibises, and have been suggested to reflect different levels of remote-touch sensitivity. Our study investigates the interspecific differences in the bone and soft tissue histology of the bill-tip organs of three species of southern African ibises from different habitats (mainly terrestrial to mainly aquatic). We analysed the external pitting pattern on the bones, as well as internal structure of the beak using micro-CT scans and soft tissue histological sections of each species' bill-tip organs. The beaks of all three species contain remote-touch bill-tip organs and are described here in detail. Clear interspecific differences are evident between the species' bill-tip organs, both in terms of bone morphology and soft tissue histology. Glossy Ibises, which forage exclusively in wetter substrates, have a greater extent of pitting but lower numbers of Herbst corpuscles in each pit, while species foraging in drier substrates (Hadeda and Sacred Ibises) have more robust beaks, fewer pits and higher densities of Herbst corpuscles. Our data, together with previously published histological descriptions of the bill-tip organs of other remote-touch foraging bird species, indicate that species foraging in drier habitats have more sensitive bill-tip organs (based on their anatomy). The vibrations produced by prey (e.g., burrowing invertebrates) travel poorly in dry substrates compared with wetter ones (i.e., dry soil vs. mud or water), and thus we hypothesise that a more sensitive bill-tip organ may be required to successfully locate prey in dry substrates. Furthermore, our results indicate that the differences in bill-tip organ anatomy between the species reflect complex trade-offs between morphological constraints of beak shape and remote-touch sensitivity requirements, both of which are likely related to each species' foraging behaviour and substrate usage. Our study suggests that structures in the bone of the bill-tip organ could provide valuable osteological correlates for the associated soft tissues, and consequently may provide information on the sensory ecology and habitat usage of the birds in the absence of soft tissues.