Nasopalatine Ducts and Flehmen Behavior in the Mandrill: Reevaluating Olfactory Communication in Old World Primates

Abstract

Compared to other modes of communication, chemical signaling between conspecifics generally has been overlooked in Old World primates, despite the presence in this group of secretory glands and scent-marking behavior, as well as the confirmed production and perception of olfactory signals. In other mammalian species, flehmen is a behavior thought to transport primarily nonvolatile, aqueous-soluble odorants via specialized ducts to the vomeronasal organ (VNO). By contrast, Old World primates are traditionally thought to lack a functional VNO, relying instead on the main olfactory system to process volatile odorants from their environment. Here, in the mandrill (Mandrillus sphinx), we document unusual morphological and behavioral traits that typically are associated with the uptake of conspecific chemical cues for processing by an accessory olfactory system. Notably, we confirmed that both sexes possess open nasopalatine ducts and, in response to the presentation of conspecific odorants, we found that both sexes showed stereotyped behavior consistent with the flehmen response. If, as in other species, flehmen in the mandrill serves to mediate social or reproductive information, we expected its occurrence to vary with characteristics of either the signaler or receiver. Flehmen, particularly in a given male, occurred most often in response to odorants derived from male, as opposed to female, conspecifics. Moreover, odorants derived during the breeding season elicited more flehmen responses than did odorants collected during the birthing season. Lastly, odorants from reproductively cycling females also elicited more responses than did odorants from contracepted females. Although confirming a link between the nasopalatine ducts, flehmen behavior, and olfactory processing in mandrills would require further study, our observations provide new information to suggest anatomical variability within Old World primates, calling further attention to the underappreciated role of chemical communication in this lineage.

Mandrills use olfaction to socially avoid parasitized conspecifics

“…Individual odors are likely cues of parasitism because infectious diseases often trigger changes in body odors ( 23 ). Moreover, mandrills often use olfaction to elaborate olfactory-guided behavioral responses ( 24 ), and they also often closely investigate conspecifics’ perianal area. We therefore tested the hypothesis that the observed relationship between grooming behavior and protozoan status in mandrills is mediated by an olfactory mechanism.…”

Facial expression: An under-utilised tool for the assessment of welfare in mammals

“…Play behavior is intrinsically rewarding (Boissy et al, 2007) and has been described as an "opioid-mediated pleasurable emotional experience" (Held and Špinka, 2011, p. 891). Play has both immediate and future benefits for psychological and long-term fitness, and as a contagious behavior can promote welfare at the group level (Bekoff, 2001; (Langner et al, 2010) in a wide range of mammals including marsupials (e.g., wombat, Lasiorhinus latifrons, Gaughwin, 1979) Charpentier et al, 2013), and felids (e.g., puma, Puma concolor, Allen et al, 2014). Recognizing sexual motivation by flehmen expression may also assist with the interpretation of other behavioral changes that occur during reproduction or courting, such as increased locomotion or aggression, which can confound interpretations of welfare (Morgan et al, 2004).…”

“…Pain will be examined in a separate section due to its specific, well-defined contribution to poor welfare states, as well as the comparatively large body of literature on facial indicators of pain. In mammals, facial expressions have been extensively Cabanac and Lafrance, 1990Spotila et al, 1977Wells, 1978;Robertshaw, 2006Gaughwin, 1979Stahlbaum and Houpt, 1989;Weeks et al, 2002;Charpentier et al, 2013Fox, 1970Sandem and Braastad, 2005;Kaiser et al, 2006;Bennett et al, 2012 Sefcek andKing, 2007;Knierim et al, 2007Partan, 2002Parr et al, 2005Parr et al, , 2007Bethell et al, 2012 Baker andAureli, 1997;Sandem et al, 2002;De Marco et al, 2010;Vick and Paukner, 2010Nagasawa et al, 2013Redbo, 1998Mason et al, 2007;Fernandez et al, 2008;Mason, 2010;Fureix et al, 2011;Tan et al, 2013Fox, 1970Waller and Dunbar, 2005;Judge and Bachmann, 2013;Yanagi andBerman, 2014 Craig et al, 1991;Langford et al, 2010;Sotocinal et al, 2011;Leach et al, 2012;Dalla Costa et al, 2014;Wathan et al, 2015;McLennan et al, 2...…”

The flehmen response and pseudosuckling in a captive, juvenile Southern sea otter (Enhydra lutris nereis)

“…Depending upon the species, the tongue may be extended beyond the lips and curled [Poddar‐Sarkar and Brahmachary, ], or pushed against the hard palate [Hart, ]. Further, the flehmen may be accompanied by an oral aspiration [Charpentier et al ], wrinkling of the nose [Weeks et al, ], or partial closing of the nares [Bailey, ]. The apparent function of the flehmen grimace is to sip the air for semiochemicals, heavy molecules that communicate reproductive status [Estes, ; Sankar and Archunan, 2004], reproductive synchrony [Thompson, ], social dominance [Thompson, ], territory [Begg et al, ], maternal behavior [Aron, ], or conspecific identification [Swaisgood et al, ].…”

“…Similarly, the flehmen is widely used within the felid family for intraspecific chemoreception of social state, examples include: the domestic cat [Hart and Leedy, ], tigers [Poddar‐Sarkar and Brahmachary, ], panthers [McBride and McBride, ], leopards [Freeman, ], and lions [Powell, ]. The flehmen response was documented among several other terrestrial mammals including pandas [Swaisgood et al, ], elephants [Rasmussen et al, ; Rasmussen and Greenwood, ], lemurs [Bailey, ; Evans, ], and mandrills [Charpentier et al, ]. Although some antelopes (Alcelaphinidae) do not engage in flehmen behavior [Hart et al, ], nor do domestic dogs (Canidae) and ferrets (Mustelidae) engage in a true flehmen response, other members within their families, like the maned wolf (Canidae) [Coelho et al, ] and the honey badger (Mustelidae) do [Begg et al, ].…”