Contrasting Patterns of Sensory Adaptation in Living and Extinct Flightless Birds

Peter Johnston,Kieren J Mitchell

doi:10.3390/d13110538

Abstract

Avian cranial anatomy is constrained by the competing (or complementary) requirements and costs of various facial, muscular, sensory, and central neural structures. However, these constraints may operate differently in flighted versus flightless birds. We investigated cranial sense organ morphology in four lineages of flightless birds: kiwi (Apteryx), the Kakapo (Strigops habroptilus), and the extinct moa (Dinornithiformes) from New Zealand; and the extinct elephant birds from Madagascar (Aepyornithidae). Scleral ring and eye measurements suggest that the Upland Moa (Megalapteryx didinus) was diurnal, while measurements for the Kakapo are consistent with nocturnality. Kiwi are olfactory specialists, though here we postulate that retronasal olfaction is the dominant olfactory route in this lineage. We suggest that the Upland Moa and aepyornithids were also olfactory specialists; the former additionally displaying prominent bill tip sensory organs implicated in mechanoreception. Finally, the relative size of the endosseous cochlear duct revealed that the Upland Moa had a well-developed hearing sensitivity range, while the sensitivity of the kiwi, Kakapo, and aepyornithids was diminished. Together, our results reveal contrasting sensory strategies among extant and extinct flightless birds. More detailed characterisation of sensory capacities and cranial anatomy in extant birds may refine our ability to make accurate inferences about the sensory capacities of fossil taxa.

Highlights

The concept of the complementary use of avian senses—and trade-offs among them— provides a framework for the inference of sensory function and sensory ecology in both living and extinct taxa [1]
We explore the sensory anatomy of representatives from these four lineages of flightless avians—kiwi, the Kakapo, moa, and elephant birds—with a view to better characterising their patterns of sensory use and specialisation
We present new findings that add to existing evidence on sensory function in flightless bird taxa, focusing on olfaction, vision, and hearing, and consider how these senses may be integrated. We focus on these four taxa—moa, kiwi, elephant birds, and Kakapo as they form or are parts of island radiations on New Zealand and Madagascar, and we can make comparisons among them with the analytical methods and new data that we present

Summary

Introduction

The concept of the complementary use of avian senses—and trade-offs among them— provides a framework for the inference of sensory function and sensory ecology in both living and extinct taxa [1]. There has been increasing interest recently in ‘avian palaeoneurology’—the inference of sensory and other function from the shape of the brain as a whole and from brain components related to specific functions [2], for fossil taxa (e.g., [3,4]). Of particular importance for improving our understanding are flightless birds, many of which appear to have evolved unusual combinations of sensory capacities. Detailed study of the sensory structures of flightless birds—both living and extinct—may help to illuminate the full diversity of possible avian sensory patterns, and the trade-offs involved in their evolution. Two lineages of flightless palaeognathous birds evolved in New Zealand—the extant kiwi (Apteryx) and the recently extinct moa (Dinornithiformes). Molecular phylogenetic work has revealed that kiwi and moa are only distant relatives [5,6,7,8], with the kiwi being the sister group of the extinct elephant birds (Aeyornithidae) from

Methods

Results

Discussion

Conclusion