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Comparative Study
, 285 (1890)

Nocturnal Giants: Evolution of the Sensory Ecology in Elephant Birds and Other Palaeognaths Inferred From Digital Brain Reconstructions

Affiliations
Comparative Study

Nocturnal Giants: Evolution of the Sensory Ecology in Elephant Birds and Other Palaeognaths Inferred From Digital Brain Reconstructions

Christopher R Torres et al. Proc Biol Sci.

Abstract

The recently extinct Malagasy elephant birds (Palaeognathae, Aepyornithiformes) included the largest birds that ever lived. Elephant bird neuroanatomy is understudied but can shed light on the lifestyle of these enigmatic birds. Palaeoneurological studies can provide clues to the ecologies and behaviours of extinct birds because avian brain shape is correlated with neurological function. We digitally reconstruct endocasts of two elephant bird species, Aepyornis maximus and A. hildebrandti, and compare them with representatives of all major extant and recently extinct palaeognath lineages. Among palaeognaths, we find large olfactory bulbs in taxa generally occupying forested environments where visual cues used in foraging are likely to be limited. We detected variation in olfactory bulb size among elephant bird species, possibly indicating interspecific variation in habitat. Elephant birds exhibited extremely reduced optic lobes, a condition also observed in the nocturnal kiwi. Kiwi, the sister taxon of elephant birds, have effectively replaced their visual systems with hyperdeveloped olfactory, somatosensory and auditory systems useful for foraging. We interpret these results as evidence for nocturnality among elephant birds. Vision was likely deemphasized in the ancestor of elephant birds and kiwi. These results show a previously unreported trend towards decreased visual capacity apparently exclusive to flightless, nocturnal taxa endemic to predator-depauperate islands.

Keywords: Aepyornithidae; Madagascar; computed tomography; fossils; recent extinction.

Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
Digital endocranial reconstructions of (a,b) elephant bird Aepyornis maximus (MNHN F 1910-12), (c,d) elephant bird Aepyornis hildebrandti, (e,f) kiwi, (g,h) greater rhea, (i,j) the open-dwelling Chilean tinamou and (k,l) the forest-dwelling brown tinamou in (a,c,e,g,i,k) ventral and (b,d,f,h,j,l) left lateral views. Optic lobes are highlighted by dashed lines. Colours: blue, brain; green, inner ear; red, vasculature; yellow, cranial nerves. Abbreviations: I, olfactory nerve; II, optic nerve; III, oculomotor nerve; IV, trochlear nerve; V, trigeminal nerve; VI, abducens nerve; VII–VIII, facial and vestibulocochlear nerves; IX–XI, glossopharyngeal, vagus and accessory nerves; XII, hypoglossal nerve; ca, carotid artery; ce, cerebellum; ff, floccular fossa; ioa, internal ophthalmic artery; ob, olfactory bulb; ol, optic lobe (red dashed outline); pf, pituitary fossa; te, telencephalon; va, vallecula; ve, vestibular organs; w, wulst. Scale bars = 1 cm.
Figure 2.
Figure 2.
GLS regressions of olfactory ratio (olfactory bulb size versus cerebrum size) for palaeognaths (solid) and neognaths (dashed). Neognath data from Bang and Cobb [22]. Lithornis plebius data from Zelenitsky et al. [10]. Colour legend: orange, elephant birds; red, kiwi; yellow, cassowary; pink, emu; purple, moa; cyan, tinamous; green, rhea; tan, ostrich; blue, lithornithid; white, neognaths.
Figure 3.
Figure 3.
Evolution of the sensory ecology of elephant birds and other palaeognaths showing transitions in daily activity patterns (inferred from reconstructions of ancestral relative optic lobe size) and foraging habitat (inferred from reconstructions of ancestral relative olfactory bulb size). Diurnal activity patterns were ancestral for palaeognaths, followed by transition to crepuscularity independently in elephant birds/kiwi, in cassowaries and possibly in some moa. Within the elephant bird–kiwi clade, nocturnality arose independently in the largest elephant birds (Aepyornis) and in kiwi. Open habitat (e.g. grass- and shrubland) was likely ancestral for palaeognaths, followed by transition to forested habitat in the clade including elephant birds, kiwi, cassowaries and emus. Emus likely subsequently transitioned back to open habitat as Australia became deforested leading up to the present. Forested habitat was likely ancestral for tinamous followed by transition back to open habitat in the clade containing the Chilean and red-winged tinamous. Although the heavy-footed moa likely occupied open habitat, other moa taxa occupied forested habitat and it is unclear if open or forested habitat was ancestral for moa. Optic lobe size ancestral state reconstruction (upper tree) is based on electronic supplementary material, figure S7. Olfactory bulb size ancestral state reconstruction (lower tree) is based on electronic supplementary material, figure S5.

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