Olfactory epithelium and ontogeny of the nasal chambers in the bowhead whale (Balaena mysticetus)

Abstract

In a species of baleen whale, we identify olfactory epithelium that suggests a functional sense of smell and document the ontogeny of the surrounding olfactory anatomy. Whales must surface to breathe, thereby providing an opportunity to detect airborne odorants. Although many toothed whales (odontocetes) lack olfactory anatomy, baleen whales (mysticetes) have retained theirs. Here, we investigate fetal and postnatal specimens of bowhead whales (Balaena mysticetus). Computed tomography (CT) reveals the presence of nasal passages and nasal chambers with simple ethmoturbinates through ontogeny. Additionally, we describe the dorsal nasal meatuses and olfactory bulb chambers. The cribriform plate has foramina that communicate with the nasal chambers. We show this anatomy within the context of the whole prenatal and postnatal skull. We document the tunnel for the ethmoidal nerve (ethmoid foramen) and the rostrolateral recess of the nasal chamber, which appears postnatally. Bilateral symmetry was apparent in the postnatal nasal chambers. No such symmetry was found prenatally, possibly due to tissue deformation. No nasal air sacs were found in fetal development. Olfactory epithelium, identified histologically, covers at least part of the ethmoturbinates. We identify olfactory epithelium using six explicit criteria of mammalian olfactory epithelium. Immunohistochemistry revealed the presence of olfactory marker protein (OMP), which is only found in mature olfactory sensory neurons. Although it seems that these neurons are scarce in bowhead whales compared to typical terrestrial mammals, our results suggest that bowhead whales have a functional sense of smell, which they may use to find prey.

Morphology of nares associated with stereo-olfaction in baleen whales

“…Determining this is a conservation priority because biofouling on floating plastic debris emits DMS, which may predispose seabirds to plastic ingestion [44]. If some baleen whales are similarly attracted to DMS, it could lead to plastic ingestion or disruption to foraging attempts [45]. Behavioural studies investigating olfaction have focused on humpback whales which respond to odorants [9] and orientate into wind more often than by chance, in the presence of odorants [42].…”

“…The recent finding that tactile hairs may have a role in the sensory ecology of North Atlantic right whales serves to highlight that our fundamental understanding of these sensory processes in whales is still evolving [46]. In addition to orthonasal olfaction, it has been theorized that baleen whales may employ retronasal olfaction, whereby odorants from ingested food or water could be passed from the oral cavity to the nasal chambers [45].…”

“…Determining this is a conservation priority because biofouling on floating plastic debris emits DMS, which may predispose seabirds to plastic ingestion [44]. If some baleen whales are similarly attracted to DMS, it could lead to plastic ingestion or disruption to foraging attempts [45].…”

Comparative embryology of Delphinapterus leucas (beluga whale), Balaena mysticetus (bowhead whale), and Stenella attenuata (pan‐tropical spotted dolphin) (Cetacea: Mammalia)

“…Early during the embryonic period, cetaceans appear similar to other mammals with processes like somite formation, forelimb bud development, and patterning of organ primordia (Štĕrba et al, 2000 ; Thewissen & Heyning, 2007 ). As development progresses, these embryos begin to diverge from this mammotypical plan and take on cetacean‐specific traits including loss of external hindlimbs (Guldberg & Nansen, 1894 ; Ogawa, 1953 ; Sedmera et al, 1997a ; Thewissen et al, 2006 ), the formation of a soft‐tissue fluke for tail‐based propulsion (Buchholtz, 2007 ; Fish, 1998 ; Ryder, 1885 ; Thewissen, 2018 ), blowhole formation on the dorsum of the skull (Farnkopf et al, 2021 ; Haddad et al, 2012 ; H. H. A. Oelschläger, 2000 ; Roston & Roth, 2019 , 2021 ), and hyperphalangy (Cooper et al, 2007 , 2011 , 2017 ; Richardson & Chipman, 2003 ; Richardson et al, 2009 ; Richardson & Oelschlager, 2002 ; Sedmera et al, 1997b ). Although other aquatic mammals such as Sirenia (manatees and dugongs) also lack external hindlimbs and display adaptations for tail‐powered swimming (Buchholtz et al, 2007 ; Domning, 2018 ), only cetaceans evolved a blowhole on the top of their heads and hyperphalangy.…”

“…Other knowledge about prenatal cetaceans is based on material from commercial whaling operations (Guldberg & Nansen, 1894 ; Kükenthal, 1889 ; Ogawa, 1953 ; Roston et al, 2013 ; Roston & Roth, 2021 ; Ryder, 1885 ; Stump et al, 1960 ), collaboration with indigenous communities that harvest cetaceans for subsistence (Armfield et al, 2011 ; Farnkopf et al, 2021 ; Heide‐Jørgensen & Garde, 2011 ; Thewissen et al, 2017 ), strandings (Berta et al, 2015 ; Roston & Roth, 2021 ), and from cetacean bycatch during commercial fishing (Armfield et al, 2011 ; Cooper et al, 2017 ; Moran et al, 2011 ; Roston & Roth, 2021 ; Sedmera et al, 1997a , 2003 ; Štĕrba et al, 2000 ; Thewissen et al, 2006 ; Thewissen & Heyning, 2007 ). Many of these reports focus on morphological descriptions of fetal specimens.…”