Zoo Biology 18:415–420 (1999)

© 1999 Wiley-Liss, Inc.

First Documentation of Flehmen in aCommon Hippopotamus (Hippopotamusamphibius)Thomas A. Zapico*

Department of Biological Sciences, University of Denver; Department of ConservationBiology, Denver Zoological Foundation, Denver, Colorado

A male common hippopotamus (Hippopotamus amphibius) was observed givinga flehmen grimace on 14 occasions in July and August of 1998 at the DenverZoo. Twelve instances of flehmen occurred after anogenital investigation of thefemale as she was exiting the pool. The two other instances of flehmen occurredin the terrestrial portion of the enclosure after the male examined samples of thefemale’s freshly voided urine. The frequency of flehmen increased as the femaleapproached estrus. Flehmen in common hippos may be an example of an evolu-tionary remnant. Zoo Biol 18:415–420, 1999. © 1999 Wiley-Liss, Inc.

Key words: hippo; vomeronasal organ; evolutionary remnant; overt estrus

*Correspondence to: Thomas A. Zapico, 12185 West 7th Place, Golden, CO 80401-5915. E-mail:tjzapico@gateway.net

Received for publication June 29, 1999; Accepted October 28, 1999.

Flehmen is a behavior exhibited by some felids and most ungulates [Dagg andTaub, 1970; Doving and Trotier, 1998; Estes, 1972, 1991; Hart and Leedy, 1987;Ladewig and Hart, 1980], including swine [Martys, 1977 as cited in Hart, 1983], andis characterized by an open mouth and a retraction of the upper lip forming a gri-mace [Estes, 1991; O’Brien, 1982]. Typically, the head is extended and is either heldhorizontally or is elevated [Estes, 1972; Hart, 1983]. Most frequently, males willperform flehmen to the urine presented by conspecific females or immediately afteranogenital investigation of females [Dagg and Taub, 1970; Estes, 1972, 1991]. Themost important function of flehmen simply may be to close the external nares byrostral muscle flexion, which would allow the vomeronasal organ (VNO) exclusivereception of metabolites of sexual hormones [Estes, 1972, personal communication].O’Brien [1982] suggested that flehmen aids in the conveyance and analysis of non-volatile steroid metabolites contained in female urine. Estes [1972, 1991] suggestedthat flehmen and the VNO function together in the detection of estrus through

416 Zapico

chemosensory analysis of urine, signaling the male to begin courtship rituals andmating behaviors. Using a tracer dye, Ladewig and Hart [1980] experimentally dem-onstrated that transport of chemical stimuli from the oral cavity to the VNO via thenasopalatine ducts might be facilitated by flehmen. Tongue manipulation of chemi-cal stimuli against the nasopalatine ducts prior to flehmen has been observed in bulls,providing further evidence that flehmen and the nasopalatine ducts may functiontogether to deliver stimuli to the VNO [Jacobs et al., 1980]. Flehmen is also givenby some female ungulates; however, it is not given as frequently as in males. Femalesable antelope (Hippotragus niger) may use flehmen as a mechanism of manipulat-ing birth synchrony [Thompson, 1991, 1995].

Little is known about the behavior of the common hippopotamus (Hippopota-mus amphibius) in the wild or in captivity. Only recently have studies revealed infor-mation on hippo behavior and communication in the wild [Barklow, 1997; Karstadand Hudson, 1986; Klingel, 1991]. Studies of the reproductive biology of hipposhave revealed anatomical composition of sex organs, age of sexual maturity, repro-ductive seasonality, and duration of gestation and lactation [Dittrich, 1976; Kayanja,1989; Laws and Clough, 1966]. In addition, Krueger [1997] documented underwatercourtship behaviors in captivity. Furthermore, observations of captive hippos havesuggested that the length of overt estrus is approximately 3 days [Krueger, personalcommunication; personal observation]. However, no documentation of flehmen orother sociosexual investigatory behaviors in hippos can be found in the literature.Previously, Estes [1991] stated that male hippos do not perform flehmen to urinepresented by females and hypothesized that the hippo VNO might be designed towork like a syringe bulb that would draw in a fresh urine sample voided underwater.Presumably, large nasopalatine ducts would then conduct the sample to the VNO;however, a possible mechanism for transport of the stimuli was not postulated. Estes[1991; personal communication] observed that the hippo VNO and nasopalatine ductsare encapsulated by a thick muscular layer. In addition, hippos use valves to closetheir external nares, possibly eliminating the need for a flehmen grimace [Estes, per-sonal communication].

In July and August of 1998, while collecting data for a study of the effects ofenvironmental enrichment and enclosure size on the behavior of captive hippos, theDenver Zoo’s male hippo was observed giving flehmen to female urine on two occa-sions. I observed the same hippo exhibiting flehmen after anogenital investigation ofthe female on 12 occasions, one of which I was able to photograph in a behavioralsequence.

The male hippo was born in 1956 and purchased by the Denver Zoo in 1958.At the time of the observations, he was receiving oral anti-inflammatories (Banamineand Adequine) for an arthritic condition. The zoo veterinarian informed me that thedrugs would relieve symptoms but not modify behavior. The keepers confirmed theassertion by informing me that the medication seemed to restore the animal’s normalbehavior. In addition, at least one keeper witnessed the male giving flehmen beforethe onset of the arthritis. The Denver Zoo’s female hippo was born in 1979 andpurchased from the Cheyenne Mountain Zoo in 1980. The two hippos have beentogether since 1980 and have produced 12 offspring, eight of which have survived.Their most recent offspring was 3 months old during these observations.

Although the female was lactating, she came into estrus during my observa-tions. Flehmen was observed as early as 7 days before overt estrus, during overt

Hippo Flehmen 417

estrus, and as late as 7 days after overt estrus (see dates of flehmen as related toestrus condition in Table 1). Twelve instances of flehmen occurred as the female wasleaving the pool (Table 1). There the male would follow her partially up the ramp,force his nasal area under her tail and examine her anogenital region. Next, he wouldthrow back his head, curl his upper lip, and expose his canines while moving hisjaws. This position was maintained for approximately 10 to 20 seconds before fi-nally sinking back into the pool (Figure 1A–E). The two other instances of flehmenoccurred in the terrestrial portion of the enclosure (Table 1). Both observations weredocumented on the same day (during overt estrus) as the male examined the female’sfreshly voided urine (Table1). After sniffing the urine, the male threw back his headand showed flehmen for several seconds. This was the only time during the studythat the female was observed urinating. The frequency of flehmen increased withapproaching estrus (Table 1). I also documented three attempted copulations duringthe 3 days of estrus designated by Table 1, although I could not determine whetherpenetration occurred. The hippos were observed during public viewing hours only,so flehmen and copulation may have occurred during the night as well. It should benoted that the possibility of this behavior being a threat or a display is doubtful.Karstad and Hudson [1986] suggested that hippos perform a full gape to exposetheir tusks and also compare gape breadth to establish rank. Furthermore, the fullgape displays that I have observed do not resemble the lip curl of the presumedflehmen. Additionally, the female seems to be unaware of the flehmen behavior,whereas a directed gape display typically solicits a response and will sometimes leadto a fight, as this female is the dominant animal [personal observation].

If flehmen was used by animals to close their external nares, as Estes [1972]hypothesized, hippos would not need to exhibit this behavior, offering a potentialexplanation of why flehmen has never before been observed in hippos. However, ifflehmen is an evolutionary remnant, this would explain why at least some hipposstill display it. Klingel [1995] suggests that early hippo genera may have been moreterrestrial than the common hippo. If so, these early hippos may have required aflehmen grimace to close their external nares, since the aquatic adaptations found inthe common hippo may not have been completely evolved. As hippos became more

TABLE 1. Location, date, and time of flehmen in a captive male hippo at the Denver Zoo

Date Time Location Estrus

7-22-98 1018 Aquatic No7-23-98 1407 Aquatic No7-25-98 1345 Aquatic No7-27-98 1406 Aquatic No7-27-98 1438 Aquatic No7-27-98 1503 Aquatic No7-28-98 1400 Aquatic No7-28-98 1421 Aquatic No7-29-98 0823 Terrestrial Yes7-29-98 1112 Terrestrial Yes7-30-98 1500 Acquatic, photographed Yes8-6-98 1514 Aquatic No8-7-98 1418 Aquatic No8-7-98 1442 Aquatic No

Note that frequency of flehmen increases as estrus approaches.

418 Zapico

Fig. 1. Sequence of anogenital investigation and flehmen performed by a male hippo at the DenverZoo on July 30, 1998. A: Female begins to exit pool, male follows. B: Male investigates anogenitalarea as female exits. C: Male begins giving flehmen as upper lip curls and exposes upper canines.(Figure 1 continued).

A

B

C

Hippo Flehmen 419

aquatic and developed the ability to close their external nares, the need for flehmenwould not be as great, but also may not have been selected against. The only otherextant hippo species, the pygmy hippopotamus, Hexaprotodon (= Choeropsis)liberiensis, appears to be more terrestrially adapted, as well as more primitive thanthe common hippo [Eltringham, 1993; Estes, 1991]. Furthermore, the pygmy hippogives a flehmen grimace [Schneider, 1934 as cited in Estes, 1972]. Presumably, mosturine testing in common hippos occurs underwater [Estes, 1991], rendering flehmenobsolete. However, in some situations hippos may test urine on land, eliciting aflehmen response. The scarcity of such situations may be another reason that flehmenhas never before been observed or documented in hippos. Additionally, if the behav-ior is not expected owing to what has appeared in the literature, an observer whodoes not consider flehmen in hippos as a possibility might well not recognize it.

Fig. 1. (continued). D: Flehmen continues; lip curl is more prominent. E: Male sinks into pool whilecontinuing flehmen. Female appears indifferent and begins to feed.

D

E

420 Zapico

ACKNOWLEDGMENTS

I thank the Department of Conservation Biology at the Denver Zoo for gener-ously funding my study. The staff and hippo keepers at the Denver Zoo provided mewith important information including histories of each hippo. Richard Reading, BrianMiller, and three anonymous reviewers contributed valuable comments on a previ-ous draft of this manuscript. In addition, I thank my colleague, Steve Kreuger of theToledo Zoo, for his support and suggestions for further hippo studies.

REFERENCES

Barklow WE. 1997. Some underwater sounds ofthe hippopotamus (Hippopotamus amphibius).Marine Freshwater Behav Physiol 29:237–49.

Dagg AI, Taub A. 1970. Flehmen. Mammalia34:686–95.

Dittrich L. 1976. Age of sexual maturity in thehippopotamus (Hippopotamus amphibius). IntZoo Yrbk 16:171–3.

Doving KB, Trotier D. 1998. Structure and func-tion of the vomeronasal organ. J Exp Biol201:2913–5.

Eltringham SK. 1993. The pygmy hippopotamus(Hexaprotodon liberiensis). In: Oliver WLR, edi-tor. Pigs, Peccaries, and Hippos. Gland, Sweden:IUCN. pp 55–60.

Estes RD. 1972. The role of the vomeronasal or-gan in mammalian reproduction. Mammalia36:315–41.

Estes RD. 1991. The behavior guide to Africanmammals. Berkeley, CA: University of Califor-nia Press. 611 p.

Hart BL. 1983. Flehmen behavior and vomerona-sal organ function. In: Muller-Schwarze D,Silverstein RM, editors. Chemical signals in ver-tebrates 3. New York: Plenum Press. pp 87–103.

Hart BL, Leedy MG. 1987. Stimulus and hormonaldeterminants of flehmen behavior in cats. HormBehav 21:44–52.

Jacobs VL, Sis RF, Chenworth PJ, Klemm WR,Sherry CJ, Coppock CE. 1980. Tongue manipu-

lations of the palate assists estrous detection inthe bovine. Theriogenology 13: 353–6.

Karstad EL, Hudson RJ. 1986. Social organiza-tion and communication of riverine hippopotamiin southwestern Kenya. Mammalia 50:153–64.

Kayanja FIB. 1989. The reproductive biology ofthe male hippopotamus. Symp Zool Soc Lond61:181–96.

Klingel H. 1991. Sizing up a heavyweight. IntWildlife 21: 4–11.

Klingel H. 1995. Fluctuating fortunes of the riverhippopotamus. Nat Hist May:46–57.

Krueger SK. 1997. Hippopotamus underwater be-havior and communication. Animal Keepers Fo-rum 24:108–10.

Ladewig J, Hart BL. 1980. Flehmen and vomero-nasal organ function in male goats. PhysiolBehav 24:1067–71.

Laws RM, Clough G. 1966. Observations on re-production in the hippopotamus (Hippopotamusamphibius). Symp Zool Soc Lond 15:117–40.

O’Brien PH. 1982. Flehmen: its occurrence andpossible functions in feral goats. Anim Behav30:1015–9.

Thompson KV. 1991. Flehmen and social domi-nance in captive female sable antelope, (Hip-potragus niger). Appl Anim Behav Sci 29:121–33.

Thompson KV. 1995. Flehmen and birth synchronyamong female sable antelope, (Hippotragusniger). Anim Behav 50:475–84.