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

Abstract

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 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

Discrete somatotopic representation and neural response properties in hummingbird and zebra finch forebrain nuclei

“…We hypothesized that feathers of the wing, including those associated with filoplume and leading edge feathers would show particular innervation by mechanosensory end organs. Herbst corpuscles (avian specific homologs of Pacinian lamellated corpuscles of mammals and other vertebrates) have been associated with the non-feathered skin of the beak in ducks 14 , kiwis 15 , and shore-foraging birds 16,17 that appear to localize prey using vibration detection via specialized sensory pits at the rostral margins of the beak. Along feather-covered surfaces, Herbst corpuscles are associated with the follicles of facial bristle feathers 18 , conspicuous whisker-like feathers that appear from margins of the mouth and above the eyes in diverse lineages of birds including kiwis 19 and owls 20 .…”

Ecomorphological patterns in trigeminal canal branching among sauropsids reveal sensory shift in suchians

“…No such behaviors are identified among lepidosaurs, which are known to prioritize vision and chemosensation when navigating their environments (Cooper, 1994; Schwenk, 1994). Extant avians however are more variable, so taxa representative of specialized trigeminal tactile‐sensory behaviors (i.e., foraging via dabbling or probing, using solely mechanosensory cues; Cunningham et al, 2013; du Toit et al, 2022) and non‐representatives (i.e., visual‐foragers; Martin, 2007; Martin & Coetzee, 2004) were sampled. For fossil specimens, the crocodylian line of archosaurs were targeted because of the condition of extant crocodilians.…”

“…Similarly, it is expected dermatomes are more richly innervated in taxa feeding in aquatic habitats than non-aquatic taxa because previously observed aquatic taxa (e.g., crocodylians, ducks, probing birds) exhibit high densities of trigeminal soft tissue structures indicative of their trigeminal abilities and use specialized, trigeminalinnervated structures to acquire food (Cunningham et al, 2013;du Toit et al, 2022;Leitch & Catania, 2012). Suchia, the lineage of fossil archosaurs including extant crocodylians, proves a useful group in which to evaluate hypotheses of evolving trigeminal tissues with transitions in ecology.…”

“…crocodyliforms, ecomorphology, somatosensation, trigeminal It remains to be understood how these adaptations for cranial sensation evolved among different clades of sauropsids, including specific lineages of lepidosaurs, crocodylians, and birds. Few neontological studies explore patterns of trigeminal nerve diversity among sauropsids (e.g., Crole & Soley, 2014;Cunningham et al, 2013;du Toit et al, 2022;George & Holliday, 2013;Gutiérrez-Ibáñez et al, 2009;Leitch & Catania, 2012;Lessner, 2020). Similarly, few paleontological studies use osteological structures to predict nervous tissue anatomy, limiting investigation to small ranges of extinct dinosaur and crocodylian species.…”

“…Extant crocodylians are known for having highly sensitive snouts covered with integumentary sensory organs (ISOs) In Alligator mississippiensis , this sensory system is specialized for a semiaquatic lifestyle, with the ability to sense minute changes in water pressure, temperature, and pH (Di‐Poï & Milinkovitch, 2013) and optimized to receive and forage using mechanosensory cues of prey items (Leitch & Catania, 2012). Some extant birds are also specialized for trigeminal nerve‐innervated somatosensation, also optimizing structures which receive mechanosensory cues from potential food (Cunningham et al, 2013; du Toit et al, 2022), whereas others rely more heavily on visual cues (Martin, 2007; Martin & Coetzee, 2004). Trigeminal‐supplied bill tip organs are known from multiple families of probe‐ and tactile‐foraging (i.e., dabbling) birds (e.g., Baumel & Witmer, 1993; Berkhoudt, 1980; Cunningham et al, 2010).…”