Olfaction at depth: cribriform plate size declines with dive depth and duration in aquatic arctoids

Abstract

It is widely accepted that cetaceans, obligate aquatic mammals with almost no chemosensory input, rely little on olfaction and have lost the adaptive olfactory anatomy and behaviors present in their terrestrial ancestors. There is less agreement, however, on the relative role of a sense of smell in the life of aquatic mammals with residual ties to the land, such as the carnivoran sea otter (Enhydra lutris) and pinnipeds. Field observations of marine carnivorans often stress their keen use of smell for social communication and predator defense during forays onto land. Yet, one critical aspect of the olfactory landscape has been lost to the pinnipeds and otters. In contrast to terrestrial mammals, aquatic carnivorans forage underwater “noseblind” with nares closed and therefore completely without chemical cues. For this reason, we hypothesize that marine carnivorans rely less on the sense of smell than their terrestrial relatives and thus predict that this loss will be manifested in reduced olfactory anatomy. Second, we predict that pinniped species that dive to greater depths and for longer durations will display a greater reduction in olfactory anatomy, as they are further separated from, and likely less reliant on, surface odor cues. To test this, we look to one olfactory skull feature, the cribriform plate (CP), a bone in the posterior nasal cavity that is perforated by passageways for olfactory nerve bundles carrying chemical signals from the periphery to the olfactory bulb of the brain. Because CP size varies with the amount of peripheral olfactory innervation in a mammal's snout, quantifying the CP provides a gauge with which to compare relative olfactory investment across species. Using high-resolution CT scans and 3D imaging software, we performed the first extensive comparative and quantitative study of CP morphology across 28 species of arctoid carnivorans, a clade at the intersection of terrestrial and aquatic life. Overall results show that within this clade, aquatic species have substantially smaller relative CP surface area than terrestrial species. Moreover, within the aquatic arctoid species (pinnipeds and sea otter), we found a significant negative correlation between relative CP size and three variables of diving behavior: mean dive depth, mean dive duration, and maximum dive duration. By contrast, maximum dive depth was not significantly correlated with relative CP size after correcting for phylogenetic effects. Moving forward, we hope to apply our digital methods for quantifying CP morphology to the fossil record to provide insights into the process and rate of evolutionary losses of olfactory anatomy during the transition to an aquatic lifestyle in lineages of arctoids. Support or Funding Information NSF Graduate Research Fellowship Program grant DGE-1144087, Sigma Xi, Department of Ecology and Evolutionary Biology UCLA, UCLA Graduate Division Top: sagittal section of a CT scan of a female elephant seal skull. Individual morphological featured were segmented in Mimics software. Bottom: volumentric rendering of skull and nasal elements. Red: Cribriform plate. Green: olfactory-related ethmoturbinal bones. Blue: respiratory maxilloturbinal bones. Scale bar: 50 mm. This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.