Abstract
It is widely accepted that obligate aquatic mammals, specifically toothed whales, rely relatively little on olfaction. There is less agreement about the importance of smell among aquatic mammals with residual ties to land, such as pinnipeds and sea otters. Field observations of marine carnivorans stress their keen use of smell while on land or pack ice. Yet, one dimension of olfactory ecology is often overlooked: while underwater, aquatic carnivorans forage “noseblind,” diving with nares closed, removed from airborne chemical cues. For this reason, we predicted marine carnivorans would have reduced olfactory anatomy relative to closely related terrestrial carnivorans. Moreover, because species that dive deeper and longer forage farther removed from surface scent cues, we predicted further reductions in their olfactory anatomy. To test these hypotheses, we looked to the cribriform plate (CP), a perforated bone in the posterior nasal chamber of mammals that serves as the only passageway for olfactory nerves crossing from the periphery to the olfactory bulb and thus covaries in size with relative olfactory innervation. Using CT scans and digital quantification, we compared CP morphology across Arctoidea, a clade at the interface of terrestrial and aquatic ecologies. We found that aquatic carnivoran species from two lineages that independently reinvaded marine environments (Pinnipedia and Mustelidae), have significantly reduced relative CP than terrestrial species. Furthermore, within these aquatic lineages, diving depth and duration were strongly correlated with CP loss, and the most extreme divers, elephant seals, displayed the greatest reductions. These observations suggest that CP reduction in carnivorans is an adaptive response to shifting selection pressures during secondary invasion of marine environments, particularly to foraging at great depths. Because the CP is fairly well preserved in the fossil record, using methods presented here to quantify CP morphology in extinct species could further clarify evolutionary patterns of olfactory loss across aquatic mammal lineages that have independently committed to life in water.
Highlights
Mammals rely on their sense of smell to varying degrees and their olfactory systems have evolved to operate in distinct ecological contexts
Support for a keen sense of smell in pinnipeds and sea otters comes from field observations of scent-driven behaviors, such as nose-to-nose nuzzling, genital sniffing, alarm responses to upwind biologists, and aversive reactions to con-specific carcass odors (Lowell & Flanigan, 1980; Peterson & Bartholomew, 1967; Riedman & Estes, 1990; Ross, 1970), all of which are observed in terrestrial carnivorans
We found a pronounced loss of olfactory anatomy, a reduction in relative cribriform plate size (RelCP), that mirrors established reductions in olfactory turbinal surface area
Summary
Mammals rely on their sense of smell to varying degrees and their olfactory systems have evolved to operate in distinct ecological contexts. It is thought that foraging pinnipeds use surface odors, such as dimethyl sulfide (DMS), to locate areas of high marine productivity in the same way mysticete whales and sea birds do (Bouchard et al, 2019; Kowalewsky, Dambach, Mauck, & Dehnhardt, 2006; Nevitt, 1999); once underwater, these diving carnivorans can no longer use the landscape of chemical cues relied on by terrestrial species to locate and capture prey (Smith, 1980; Ylönen, Sundell, Tiilikainen, Eccard, & Horne, 2003) For this reason, we pose a first, general hypothesis that aquatic carnivorans rely less on olfaction than closely related terrestrial species and predict that this will be manifested in reduced olfactory anatomy. Studying Carnivora is advantageous, as the group has a fairly well-resolved phylogeny, allowing the application of comparative methods that account for phylogenetic relatedness in our study of ecological influences on olfaction
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