Theflehmen response (/ˈfleɪmən/; fromGermanflehmen'to bare the upper teeth', andUpper Saxon Germanflemmen'to lookspiteful'), also called theflehmen position,flehmen reaction,flehmen grimace,flehming, orflehmening, is abehavior in which an animal curls back its upper lip exposing its front teeth, inhales with the nostrils usually closed, and then often holds this position for several seconds.[1] It may be performed over a site or substance of particular interest to the animal, or may be performed with the neck stretched and the head held high in the air.
Flehmen is performed by a wide range ofmammals, includingungulates andfelids.[1] The behavior facilitates the transfer ofpheromones and other scents into thevomeronasal organ (VNO, or Jacobson's organ) located above the roof of the mouth via a duct which exits just behind the front teeth of the animal.
The word originates from theGerman verbflehmen'to bare the upper teeth'. It comes from theUpper Saxon Germanflemmen'to lookspiteful'.[2] The word was introduced in 1930 byKarl Max Schneider, director of the Leipzig zoo and an authority on big cats in captivity.[3][4]
This response is characterized by the animal curling back its top lip exposing the front teeth and gums, then inhaling and holding the posture for several seconds.[3] The behavior may be performed over particular locations, in which case the animal may also lick the site of interest, or may perform the flehmen with the neck stretched and head held high in the air for a more generalgustatory or taste-related investigation. The flehmen response can give the appearance that the animal is looking spiteful, grimacing, smirking, disgusted, or laughing. The relationship between emotions and expressions across species isdebated.
The flehmen response draws air into the vomeronasal organ (VNO), an auxiliaryolfactorysense organ that is found in many animals. This organ plays a role in the perception of certain scents and pheromones. The vomeronasal organ is named for its closeness to thevomer andnasal bones, and is particularly well developed in animals such as cats and horses. The VNO is found encompassed inside a bony or cartilaginous capsule which opens into the base of thenasal cavity.[7] Animals that exhibit flehmen havea papilla located behind the incisors and ducts which connect the oral cavity to the VNO, with horses being an exception. Horses exhibit flehmen but do not have an incisive duct communication between the nasal and oral cavity because they do not breathe through their mouths; instead, the VNOs connect to the nasal passages by thenasopalatine duct.[8]
The chemical cue obtained by an animal exhibiting the flehmen response is the presence of a non-volatileorganic compound. In contrast tovolatile organic compounds (VOCs), non-volatile organic compounds are those carbon compounds that do not participate in atmospheric photochemical reactions or evaporate under normal atmospheric conditions.[9] The VNO detects non-VOCs, which must have direct contact with the odor source. Sources of non-VOCs relevant to the flehmen response include pheromones and hormones excreted from the genital regions or urine of animals.
An animal may perform the flehmen response when investigating sites of particular interest, or perhaps (more generally) odors or tastes. In horses, spontaneous flehmen response outside of the normal context can also indicate discomfort.[10]
The primary function of the flehmen response is intra-species communication. By transferring air containing pheromones and other scents to the VNO, animals can gather chemical "messages".[11] These scents tell an animal about other members of their species in some of the following ways:
Identifying reproductive status – male individuals commonly use the flehmen response as an olfactory mechanism for identifying the reproductive state of females of the same species based onpheromones in the female's urine or genitals.[12] This is exhibited in thereproductive behavior of sheep. The ram often exhibits flehmen after sniffing ewes' external genital regions, but this occurs most frequently on the day beforeestrus when the ewes are sexually receptive.[13]
Reproductive synchrony – flehmen behavior also plays a role inreproductive synchrony between females. In thesable antelope, the frequency of flehmen changes seasonally, with the highest levels just prior to conception. Female antelopes associate closely with other females in the same reproductive state. Flehmen rates between females anticipated birth synchrony. Additionally, the level of synchrony was predicted by the frequency of female urine sampling during the previous year. Flehmen is a mechanism used by female sable antelopes to manipulate the timing of both conception and birth of offspring.[14] In the American bison, flehmen behavior in females has also been shown to stimulate the onset ofestrus andcopulation synchronization.[15]
Post-parturition – in horses, mares commonly show a peak in flehmen response during the first few hours after giving birth. Smelling the newborn foal and the amniotic fluids associated with birth often produces the reaction.[16]
Immature animals – in young horses, both colts (males) and fillies (females) exhibit flehmen behavior toward otherconspecifics with neither sex performing the behavior more than the other.[1] However, it has been reported that young colts flehmen up to five times more frequently than fillies, and fillies flehmen more frequently than mature mares.[16][contradictory] Young elephants also have a flehmen response to stimulants. The VNO of newborn elephants displays a structural maturity similar to adults, which supports the conclusion that flehmen at only six weeks of age is used to deliver chemical pheromones to a functional VNO.[17]
The flehmen response is not limited to intra-species communication. Goats have been tested for their flehmen response to urine from 20 different species, including several non-mammalian species. This study suggests there is a common element in the urine of all animals, aninterspecific pheromone, which elicits flehmen behavior. Specifically, chemical pheromone levels of a modified form ofandrogen, asex hormone, were associated with the response in goats.[18]
A wide range of mammals exhibit flehmen including both predatory and non-predatory species.
The response is perhaps most easily observed in domestic cats and horses; both exhibit a strong flehmen response to odors.[19]Stallions usually smell the urine of mares in estrus whereas the male giraffe's flehmen response includestasting the female's urine.[20]Elephants perform a flehmen response but also transfer chemosensory stimuli to the vomeronasal opening in the roof of their mouths using theprehensile structure, sometimes called a "finger", at the tips of their trunks.[citation needed]
^abHart, Benjamin L (1983). "Flehmen Behavior and Vomeronasal Organ Function". In Müller-Schwarze, Dietland; Silverstein, Robert M. (eds.).Chemical Signals in Vertebrates 3. Springer. p. 87.doi:10.1007/978-1-4757-9652-0_5.ISBN978-1-4757-9654-4.
^Briggs, Karen (December 11, 2013)."Equine Sense of Smell". The Horse. RetrievedDecember 15, 2013.
^Volatile Organic Compounds (VOCs): Technical Overview. United States Environmental Protection Agency.[1]. Updated April 10, 2012. Accessed May 9, 2012.
^abHart, Benjamin L.; Hart, Lynette A.; Maina, J. N. (1988-01-01). "Alteration in vomeronasal system anatomy in alcelaphine antelopes: Correlation with alteration in chemosensory investigation".Physiology & Behavior.42 (2):155–162.doi:10.1016/0031-9384(88)90291-0.ISSN0031-9384.PMID3368534.S2CID26589910.
^Sasada, H.; Kanomata, K.; Fukuoka, T. "Flehmen induction with goats by the urine of twenty animal species". 1988. 11th International Congress on Animal Reproduction and Artificial Insemination, University College Dublin, Irelend, June 26–30, 1988. Volume 4. Brief Communications.
Swaisgood, Ronald R.; Lindburg, Donald G.; Xiaoping Zhou; Owen, Megan A. (August 2000). "The effects of sex, reproductive condition and context on discrimination of conspecific odors by giant pandas".Anim. Behav.60 (2):227–237.doi:10.1006/anbe.2000.1464.PMID10973725.S2CID22445240.
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