Birds even smelled like dinosaurs: the evolution of avian olfaction

Evolution in birds of the olfactory bulb, the part of the brain where smell information is processed, passing from a dinosaur (Bambiraptor) through early birds (Lithornis, Presbyornis) to a modern-day bird (pigeon).

Birds have a lousy sense of smell, right? That common perception may apply to some modern-day birds, but that wasn’t always the case. Early birds, frankly, smelled like dinosaurs, meaning that they inherited a pretty respectable sense of smell from their dinosaurian kin. The typical scenario had been that as birds evolved flight, the senses of vision and balance increased and the olfactory sense diminished. Darla Zelenitsky (University of Calgary) and François Therrien (Royal Tyrrell Museum) invited Ryan Ridgely and me to join forces in testing this scenario by studying the evolution of the olfactory bulb, the part of the brain receiving information on odors, across the transition from small theropod dinosaurs to birds. As our new article in Proceedings of the Royal Society B reveals, birds started out with a full sensory toolkit, including a pretty capable sniffer. And we also learned a thing or two about non-avian theropods along the way.

Assembling the team
Collaboration was obvious. François and Darla had done some important work on the olfactory apparatus of theropod dinosaurs, culminating in their excellent 2009 article. Our Ohio team has had NSF funding since 2003 to look at the evolution of the brain and sensory systems of dinosaurs and other archosaurs. So, it was natural to combine our data and expertise to tackle the transition to birds. Teasing apart this transition has been the target of our NSF grants all along, and so Ryan and I had already sampled a number of the key advanced non-avian coelurosaurian dinosaur species (e.g., dromaeosaurs, troodontids) and basal bird species (e.g., Archaeopteryx, Hesperornis, Ichthyornis), as well as some basal members (e.g., Lithornis) of the evolutionary group that includes all modern-day birds (Neornithes).

Brain endocast with inner ear of the basal neornithine bird Lithornis. Inset is Figure 1 from the Zelenitsky et al. (2011) article, showing the measurements taken.

Making sense of avian olfactory evolution
You can check out the published article for details of our findings. Our OU WitmerLab site and Darla’s site both have more information. Basically, our results showed that many advanced non-avian maniraptorans had pretty respectable senses of smell as judged by the sizes of their olfactory bulbs. Bulb size was maintained across the transition to birds, as far as we can tell, and even increased a bit in basal birds. Moderately large olfactory bulbs persist in basal members of Neornithes, the group that includes all modern-day species of birds. Lithornis, a 58-million-year old neornithine perhaps related to ratites and tinamous, gave us our best evidence for early members of the modern radiation, but even among birds living today, many basal (primitive) species (ducks, flamingos) have relatively large olfactory bulbs.

All this suggests that birds inherited a good sense of smell from their ancestors and that a pretty potent sniffer was maintained in many bird groups. Some birds indeed have tiny olfactory bulbs and are not as reliant on odors. A huge group, the perching birds (passerines, such as crows, cardinals, and sparrows), have very small olfactory bulbs, as do parrots. Previously, the assumption had been that birds in general had a weak sense of smell and that a good sense of smell is an evolutionary specialization. Our study reverses that polarity: a good sense of smell is basically an avian trait, itself inherited from dinosaurs. It’s been greatly reduced a few separate times (albeit in one case in an extremely diverse group, passerines), as well as greatly enhanced a few separate times (albatross, turkey vultures).

Simplified diagram of avian evolution illustrating some of the species included in the study.

Olfaction and the not-quite-total extinction of dinosaurs
Nearly all dinosaurs—including birds—went extinct at the end of the Cretaceous. Only “modern birds” (neornithines) survived. What was different about neornithines? The reality is that it’s still generally mysterious why some species survive mass extinctions and others die out, but a common trait of some survivors is that they are generalists that can do many things well. Basal neornithines weren’t the sensory specialists that we once thought. Rather they were generalists that could use all their senses, which may have given them an edge in comparison to other flying vertebrates like others birds or pterosaurs. Being excellent flyers maybe gave them an edge over non-avian dinosaurs, many of which were also sensory generalists. So, the ancestors of modern-day birds could not only fly to search for better conditions, but they had the complete sensory toolkit to find food, mates, and suitable habitats. That may have been enough to tip the scales toward survival. This scenario constitutes little more than speculation at this point—a future research direction—which is why it got about half a sentence in our published article. We know next to nothing about the olfactory capabilities of, say, enantiornithine birds, a diverse group that didn’t survive the extinction. I’m still banking on neornithines being mostly lucky, but it’s worth keeping this hypothesis in mind.

Graphic based on the Schmitz & Motani (2011) Science article showing a nocturnal dinosaur (Velociraptor) and a diurnal pterosaur (Scaphognathus).

Nocturnal dinosaurs: seeing…and smelling?…in the dark
This was a good week for dinosaur sensory biology. A couple days after our article on olfaction came out, Lars Schmitz and Ryosuke Motani’s article on eyeballs, vision, and daily activity patterns came out in Science. They found that many of the same theropods that we found to have moderately large olfactory bulbs also had the eye-socket parameters of nocturnal animals. Many nocturnal animals have a keen sense of smell, and so these results fit nicely. On the other hand, they found that basal birds were probably more active in the daytime (diurnal), whereas we found basal birds to have a sense of smell that was pretty comparable to, if not better than, the non-avian maniraptorans. Our avian samples only share Archaeopteryx, and so it’s hard to know what to make of this difference. To be honest, I trust Lars and Ryosuke’s vision-based assessments of activity patterns much more than assessments based on olfactory capabilities (a good sense of smell can be pretty handy at any time of day). Still, combining data like these is another interesting future direction and has bearing on Ryan’s and my ongoing work on dinosaur brain and sensory evolution. It’s a good time to be a dinosaur biologist!

– Larry Witmer

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