Zoo Biology The Flehmen Response and Pseudosuckling in a Captive, Juvenile Southern Sea Otter (Enhydra lutris nereis) For Peer Review Journal: Zoo Biology Manuscript ID Draft Wiley - Manuscript type: Research Article Date Submitted by the Author: n/a Complete List of Authors: Island, Heide; Pacific University, PsycholoGy WenGeler, Julia; Pacific University, PsycholoGy Claussenius-Kalman, Hannah ; Pacific University, PsycholoGy Keywords: flehmen, pheromone, sea otter, olfaction, stereotypy John Wiley & Sons Page 1 of 37 Zoo Biology Island, 1 Sea Otter Flehmen 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 The Flehmen Response and Pseudosuckling in a Captive, Juvenile Southern Sea Otter 18 For Peer Review 19 20 (Enhydra lutris nereis) 21 22 Heide D. Island* 23 24 Julia Wengeler 25 26 Hannah Claussenius-Kalman 27 28 Department of Psychology, Pacific University, Forest Grove, Oregon 29 30 Manuscript Word Count: 4,589 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 *Correspondence to: Heide Island, Department of Psychology, Pacific University, 2043 College 55 56 57 Way, Forest Grove, OR 97116; Email: island@pacificu.edu; Phone: 503-352-1538 58 59 60 John Wiley & Sons Zoo Biology Page 2 of 37 Island, 2 Sea Otter Flehmen 1 2 3 4 Abstract 5 6 7 A juvenile, female sea otter (Enhydra lutris nereis) was observed in 43 instances of the flehmen 8 9 response over 19 days from May through July of 2015 at the Oregon Zoo. In all flehmen grimace 10 11 observations, the juvenile sea otter engaged in nibbling, nosing, or licking the peri-mammary or 12 13 anogenital areas of a non-lactating, geriatric female sea otter. The stereotypic flehmen behavior 14 15 observed was consisted with the sequences of behavior documented in other mammals, lifting the 16 17 head, elevating the nose to the air, retracting the upper lip slightly, and manipulating her mystacial 18 For Peer Review 19 20 vibrissae back and forth while rapidly inspiring air through her mouth in quick succession, tongue 21 22 extruded. The occurrence of this behavior was not specific to visitor density, visitor impact rating, 23 24 day of the month, time of day, or exhibit zone. However, it did occur more frequently in one area 25 26 of the enclosure. Among the three sea otters (two females, one male) currently housed at the Oregon 27 28 Zoo, the juvenile female’s flehmen response only occurred following interactions with the older 29 30 female and was always preceded by the pseudosuckling or anogenital nosing, licking or nibbling 31 32 33 behavior. 34 35 36 37 Key words: flehmen, pheromone, sea otter, olfaction, stereotypy 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 John Wiley & Sons Page 3 of 37 Zoo Biology Island, 3 Sea Otter Flehmen 1 2 3 4 INTRODUCTION 5 6 7 The flehmen is a behavioral sequence that involves the elevation of the head, retraction of 8 9 the upper lip, and the inhalation of air through the mouth (Estes, 1972). Depending upon the 10 11 species, the tongue may be extended beyond the lips and curled (Poddar-Sarkar and Lal 12 13 Brahmachary, 2014), or pushed against the hard palate (Hart, 1982). Further, the flehmen may be 14 15 accompanied by an oral aspiration (Charpentier, et al 2013), wrinkling of the nose (Weeks, et al. 16 17 2002), or partial closing of the nares (Bailey, 1978). The apparent function of the flehmen grimace 18 For Peer Review 19 20 is to sip the air for semiochemicals, heavy molecules that communicate reproductive status (Estes, 21 22 1972; Sankar and Archunan, 2004), reproductive synchrony (Thompson, 1995), social dominance 23 24 (Thompson, 1991), territory (Begg, et al 2003), maternal behavior (Aron, 1979; Wysocki, 1972) or 25 26 conspecific identification (Swaisgood, et al 1999). The putative pheromones sampled through the 27 28 flehmen are often suspended in biological secretions from anal or sternal glands, vaginal discharge, 29 30 urine, feces, milk, saliva, or other biological fluid (For a thorough review of mammalian 31 32 33 semiochemicals, see Ferrero and Liberles, 2009). Through the flehmen response, air is pulled 34 35 across the tongue into the back of the throat and along the orifices of the vomeronasal organ (VNO) 36 37 (Pageat and Gaultier, 2003). 38 39 The VNO is the chemoreceptive, peripheral sensory organ of the accessory olfactory 40 41 system, thought to be anatomically and physiologically distinct from the main olfactory system 42 43 44 (MOS). Most tetrapod vertebrates possess a vomeronasal organ regardless of their reliance on 45 46 chemosensensory communication, with the exception of cetaceans, sirenians, old world primates, 47 48 and bats (Mackay-Sim, et al. 1985). The VNO consists of two mucus-filled tubes on either side of 49 50 the inferior nasal septum, where olfactory receptor neurons (ORN) line the medial region of the 51 52 VNO epithelium (Hart 1982). Even though the main olfaction system appears to have some 53 54 pheromone receptivity (Kelliher, 2007; Yoon, et al. 2005; Zufall and Munger, 2001) current 55 56 57 wisdom of mammalian pheromone reception posits that the vomeronasal system (VNS) is the most 58 59 60 John Wiley & Sons Zoo Biology Page 4 of 37 Island, 4 Sea Otter Flehmen 1 2 3 4 specialized for semiochemical detection (Buck, 2000; Yu, et al. 2010). During the flehmen 5 6 7 response, semiochemicals are inhaled through the mouth and mix with mucous, passing into the 8 9 VNO triggering chemosensory impulses from VNO olfactory receptor neurons to the accessory 10 11 olfactory bulb (Ladewig and Hart, 1982). Thus the flehmen grimace heightens chemosensation 12 13 among those vertebrates that utilize intraspecific pheromone communication. 14 15 First documented among ungulates and felids (Schneider, 1930 as cited in Bailey, 1978), 16 17 the flehmen response has been observed across broad taxonomic genera. Among ungulates, goats 18 For Peer Review 19 20 (Ladewig and Hart, 1980; Melese-D’Hospital and Hart, 1985), antelope (e.g., Frey, et al. 2007; 21 22 Thompson, 1991; 1995), bovines (Houpt, et al. 1988; Sankar and Archunan, 2004), horses (e.g., 23 24 Christensen, et al 2005; Weeks, et al 2002), tapirs (Tortato, et al 2007), rhinoceroses (Zahari, et al. 25 26 2005), hippopotamuses (Zapico, 1999), and giraffes (Bercovitch, et al 2006) utilize the flehmen 27 28 during social communication. Similarly, the flehmen is widely used within the felid family for 29 30 intraspecific chemoreception of social state, examples include: the domestic cat (Hart and Leedy, 31 32 33 1987), tigers (Poddar-Sarkar and Brahmachary, 2014), panthers (McBride and McBride, 2010), 34 35 leopards (Freeman, 1982), and lions (Powell, 1995). The flehmen response was documented among 36 37 several other terrestrial mammals including pandas (Swaisgood et al 2002), elephants (Rasmussen 38 39 and Greenwood, 2003; Rasmussen et al 2002), lemurs (Bailey, 1977; Evans,1980), and mandrills 40 41 (Charpentier et al 2013). Although domestic dogs (Canidae) and ferrets (Mustelidae) are not 42 43 44 thought to engage in a true flehmen response, other members within their families, like the maned 45 46 wolf (Canidae) (Coelho et al 2012) and the honey badger (Mustelidae) do (Begg, et al 2003). 47 48 In spite of our understanding of olfactory and chemosensory perception among terrestrial mammals, 49 50 the use of olfaction and chemosensation by semiaquatic marine mammals is poorly understood. 51 52 While fully aquatic mammals, like the cetaceans and the sirenians have either reduced olfactory 53 54 tracts or absent olfactory bulbs (Berta, et al, 2006; Mackay-Sim et al, 1985; Yu, et al, 2010) relying 55 56 57 primarily on the sensory modalities of audition and vision; there is evidence for the use of olfaction 58 59 60 John Wiley & Sons Page 5 of 37 Zoo Biology Island, 5 Sea Otter Flehmen 1 2 3 4 in social interaction among the seals, sea lions, and walruses (Dobson and Jouventin, 2003; Miller, 5 6 7 2002). In fact, given the existence of a vomeronasal system, the large size of the ethmoturbinal 8 9 bones, and their ability to modulate the diameter and the opening of their nares, (Sergeant, 1991), 10 11 pinnipeds are thought to have a sharp sense of smell (Schusterman, 1981; Sergeant, 1991; Yu et al, 12 13 2010). 14 15 Harp seal mother and pups have been observed in face-to-face “nosing” behavior, which 16 17 may be a form of scent marking since the sebaceous glands below the eye secrete an oil that retains 18 For Peer Review 19 20 a unique odor (Sergeant, 1991). The acceptance of pups by their mothers using the mutual naso- 21 22 nasal contact has also been observed in fur seals (Phillips, 2003; Dobson and Jouventin, 2003). 23 24 Further, sniffing the facial regions between mother and pup may aid in detecting secretions from the 25 26 sweat glands, located between the mystacial vibrissae, thereby reinforcing the maternal bond (King, 27 28 1991; Mackay-Sim et al. 1985). In the event the mother and pup separate, Wyatt (2014) observed 29 30 cow harp seals facing the wind to use airborne scent trails of the pup to recover their young. During 31 32 33 mating season, sea lions as well as some species of seals (e.g., harp seals and ringed seals) emit a 34 35 strong odor during rut, likely serving to identify territory during male-male competition (Sergeant, 36 37 1991). Moreover, both male and female pinnipeds nose anogenital and perineal regions during 38 39 breeding and pupping season (Sergeant, 1991).
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