PHEROMONAL DISCRIMINATION OF SEX BY MALE AND

Journal of Chemical Ecology, Vol. 23, No. 12, 1997

PHEROMONAL DISCRIMINATION OF SEX BY MALEAND FEMALE LEOPARD GECKOS

(Eublepharis macularius)

WILLIAM E. COOPER, JR.* and LAURA J. STEELE

Department of BiologyIndiana University-Purdue University Fort Wayne

Fort Wayne, Indiana 46805-1499

(Received October 28, 1996; accepted August 14, 1997)

Abstract—The ability of male and female Eublepharis macularius to discrim-inate among pheromones of males and females and a blank control was inves-tigated. Stimuli were presented on ceramic tiles in the animal’s home cages.Males tongue-flicked at significantly lower rates in response to male stimulithan to female and control stimuli. Males also performed aggressive behaviorstoward male, but not female or control, stimuli, and tail vibrations towardfemale, but not male or control, stimuli. Mean tongue-flick rates by femalesdid not differ significantly among conditions. Discrimination of male phero-mones by females was demonstrated by greater performance of labial-lickingand chin-rubbing in response to male stimuli than to either female or controlstimuli.

Key Words—Pheromone, tongue-flicking, sex recognition, Squamata, Euble-pharidae, Eublepharis macularius

INTRODUCTION

Pheromonally based sex discrimination has been demonstrated in several speciesof squamate reptiles (Duvall, 1979; Cooper and Vitt, 1984a; Mason, 1992;Cooper and Trauth, 1992; Cooper et al., 1994). Male Eumeces laticeps exhibitdifferential tongue-flicking rates to male and female conspecific pheromones(Cooper and Vitt, 1984a) and are able to track females by following pheromonetrails (Cooper and Vitt, 1986a). Male Gerrhosaurus nigrolineatus also tongue-flick at a higher rate to female pheromones than to either male pheromones ordistilled water controls (Cooper and Trauth, 1992), as do male Blanus cinerus

*To whom correspondence should be addressed.

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0098-0331/97/1200-2967$12.50/0 © 1997 Plenum Publishing Corporation

(Cooper et al., 1994). Fewer studies address the ability of female lizards todiscriminate sex from pheromonal cues. Female Eumeces laticeps show no dis-crimination of sex based on tongue-flick rate (Cooper and Vitt, 1984b), althoughthey do detect conspecific pheromones of both sexes. Female Cordylus cordylustongue-flick at higher rates in response to female, but not male, pheromonesthan control stimuli (Cooper et al., 1996).

Evidence from several behavioral studies suggests that pheromonal cuesare important in sex recognition in Eublepharis macularius (Greenberg, 1943;Brillet, 1990, 1993; Mason and Gutzke, 1990). Following surgical exchange ofthe tails of male and female Coleonyx variegatus (close relatives of Euble-pharis), experimental males courted males with female tails and avoided themale tails of experimental females (Greenberg, 1943), leading to the conclusionthat some cue present on the skin relayed information about the sex of theindividual. This was an important finding, but possible tactile sex differencesbetween tails were not ruled out (Cooper and Trauth, 1992).

Male E. macularius react aggressively to other males at any time and courtfemales except when they are preparing to shed their skins. While females areshedding, however, males react agonistically to them (Mason and Gutzke, 1990).This suggests that the separated skin prior to shedding acts as a barrier, makingfemale sex pheromones unavailable for detection (Mason and Gutzke, 1990).Examination of chemical constituents of the dorsal epidermis of male and femaleleopard geckos by gas chromatography revealed distinct sex differences in lipidfractions of high molecular weight (Mason and Gutzke, 1990). Some of thelipids that differ between male and female profiles have been shown to serve assex pheromones in Thamnophis sirtalis parietalis (Mason et al., 1989).

Male E. macularius perform tail-vibrating behaviors when courting females(Brillet, 1991), but not in other contexts. In empty cages that had previouslyhoused conspecific females, males vibrate their tails, indicating recognition offemale pheromones (Brillet, 1990). Experimental males reacted agonisticallytoward anesthetized males, but courted anesthetized females (Brillet, 1993).Males often attempted to copulate with females, implying that these geckos arenot only able to determine the sex of conspecifics in the absence of any behav-ioral cues, but behave as though they were encountering unanesthetized lizards.Chemical cues may have contributed to sex recognition in Brillet’s (1991) study,but were confounded with other cues provided by the lizards.

Brillet (1990) examined lingual responses and other behavioral responsesby males and females to both male and female pheromones. He reported thatthe number of tongue-flicks by males in clean cages did not differ significantlyfrom those in cages previously occupied by males or females. Numbers oftongue-flicks by females did not differ in clean cages and cages previouslyoccupied by females, but Brillet reported that females tongue-flicked at a sig-nificantly higher rate in cages that had been occupied by males than in clean

2968 COOPER, AND STEELE

cages. However, Brillet (1990) accepted P = 0.06 as significant without makingany downward adjustment of a to compensate for the number of significancetests conducted. In addition, the sample sizes were so small (N = 6 in all cases)that statistical power was too low to assure detection of real differences.

Here we report further studies of the ability of male and female leopardgeckos to detect conspecific chemical stimuli derived from both sexes and torespond differentially to male and female stimuli based solely on chemical cuesdeposited on a substrate. These abilities were studied experimentally by record-ing lingual and other behavioral responses to chemical stimuli presented onceramic tiles.

METHODS AND MATERIALS

Subjects and Maintenance. Adult male (N = 15) and female (N = 28)leopard geckos were obtained from captive-bred research colonies and kept inan AALAC-accredited animal care facility. They were housed in translucentplastic containers (45 x 25 x 30 cm), each having a plastic shelter site andwater bowl. Water was available ad libitum, and animals were fed crickets twotimes weekly. Any crickets not immediately eaten were left in the cage. Roomtemperature was maintained at 27°C, with a 12L: 12D photoperiod. All exper-iments were performed between 19:00 hr and 24:00 hr under red light tominimize potential disturbance to these nocturnal lizards due to the investigator’spresence and to observe responses during the normal feeding period.

Experimental Design and Analysis. Experiments were conducted to deter-mine whether or not male and female E. macularius detect conspecific phero-mones and discriminate between pheromones of males and females presentedon tiles. Pheromonal stimuli were obtained by placing an unglazed ceramic tile(15 x 15 cm) at the center of one end of each animal’s cage for a minimum oftwo weeks to allow thorough marking. Just before the beginning of a trial, thetile, shelter, and water bowl were removed from the cage of the animal to betested and placed on the cage lid. After being lightly brushed to remove exces-sive soiling, an experimental tile was placed in the test animal’s home cage inthe same position as the one removed. In the control condition for responses totiles, the tile was a clean, unmarked tile. For the trials requiring marked tiles,the tile was taken from the cage of one of the other individuals in the laboratorypopulation.

In two similar experiments testing tongue-flicking and other behavioralresponses of adult males and females, male pheromones or female pheromoneson ceramic tiles and clean ceramic tiles were presented to lizards sequentiallyin randomized blocks designs in which each individual was tested in all threeconditions. Order of stimulus presentation was completely counterbalanced for

DISCRIMINATION OF SEX BY GECKOS 2969

the 15 males to prevent sequential bias. In the experiment on female responses,trial sequences were completely counterbalanced for 24 females. For the remain-ing four females, the sequences were randomized with the constraint that allthree stimuli occurred at least once in the first, second, and third trials.

After placing a tile in the animal’s cage, the investigator moved to a seat1 m away. Tongue-flicks were recorded for 5 min, beginning with the firsttongue-flick directed to the tile. The occurrence of other behaviors was recordedbeginning as soon as the tile was placed in the cage until the end of the trial.If the animal failed to tongue-flick the tile in 10 min, the tile was removed andthe animal was tested at a later date. Animals were tested only once per day.

At the conclusion of a trial, the experimental animal’s tile, shelter, andwater bowl were replaced in its cage. If the animal’s tile was used as the stimulusin a trial with another gecko, it was replaced by a clean, blank tile that was leftto be marked for two weeks for use in future trials. This method allowed tilesto be continuously present in the cages, except during brief intervals before theanimals were tested. Each tile was used once, then washed by hand with Alconoxand dried.

In the experiment on male response to pheromones, several behaviors wererecorded: (1) tongue-flicking; (2) cloacal rubbing—a substrate-marking behaviorin which the animal presses the cloacal region to the substrate while moving(Brillet, 1990; Mason and Gutzke, 1990); (3) stilting—behavior whereby theanimal lifts its entire body off the substrate by extending all four legs, archesits back, and often waves and coils its tail (Mason and Gutzke, 1990); (4) tailvibration—rapid vibration of the distal third to half of the tail performed onlyin response to female stimuli while the body and head are held rigidly still(Brillet, 1990); and (5) biting—biting or attempting to bite the experimenterimmediately after the trial while the experimental tile was being retrieved andobjects were being returned to the cage.

Behaviors recorded in the experiment on female responses to pheromoneswere tongue-flicks, labial-licks, and chin-rubs. Labial-licks are lingual protru-sions in which the tongue wipes the labial scales about the mouth rather thanbeing directed to the air or substrate. Although labial-licks were included in thetotal tongue-flick count, their occurrence was recorded because their functionmay differ from tongue-flicks directed to substrates (DePerno and Cooper, 1996).Chin-rubbing is pronounced rubbing of the chin and throat area along the sub-strate, in this case the cage floor or tile. Only its presence or absence wasrecorded.

Nonparametric ANOVAs were conducted due to significant heterogeneityof variance (Hartley’s Fmax tests) (Winer, 1962). Friedman two-way analysis ofvariance was used to determine whether differences between the three conditionswere significant. When main effects were significant, multiple comparison pro-cedures (Zar, 1984) were used to determine whether tongue-flick rates differed


between pairs of conditions. Differences in frequency of the other behaviorswere analyzed using sign tests and binomial tests (Siegel, 1956). All statisticswere assessed at a = 0.05, and probability values are two-tailed unless other-wise stated.

RESULTS

Male Responses. Mean tongue-flick rates of males were highest towardcontrol stimuli and lowest toward male stimuli (Table 1). Variances of numbersof tongue-flicks differed significantly among conditions (Fmax = 12.34; df = 3,14; P < 0.01). Mean tongue-flick rates by male E. macularius differed signif-icantly among conditions (x 2 r = 12.4; df = 2; P < 0.006, Table 1). Tongue-flick rates were significantly lower to male stimuli than to both female stimuli(P < 0.005) and blank control stimuli (P < 0.025). Tongue-flick rates elicitedby female and control stimuli did not differ significantly (P > 0.05).

Only a few males stilted, and only during trials with male stimuli (Table1). In addition, a few males bit the investigator when the tile was removed atthe end of the trial involving male stimuli, but none bit after trials in the otherconditions (Table 1). Differences between male and other stimulus conditionswere not significant for either of these behaviors alone (P = 0.06, stilt; and P= 0.125, bite; one-tailed sign tests). However, aggressive behavior, either stilt-ing, biting, or both, was performed by five males, all in trials involving male-labeled tiles, but by no male in other trials. Thus, males were significantly morelikely to perform aggressive behaviors in response to male stimuli than to eitherfemale or control stimuli (P = 0.03; one-tailed sign test). This difference is atbest only marginally significant. However, assuming that aggression was equally


TABLE 1. RESPONSES BY 15 MALE Eublepharis macularius TO CONSPECIFIC CHEMICALSAND CONTROL STIMULI

Tongue-flicks/5 minMeanSERange

Stilting (N)Biting (N)Tail-vibrating (N)Cloacal-rubbing (N)

Male

29.64.6

5-64430

14

Female

57.03.7

38-7800

1210

Control

66.812.9

18-194000

14


likely in each of the three conditions, the binomial probability that all fiveinstances of aggression occurred in male trials rather than in the combined othertrials is < 0.004.

Eighty percent of males performed tail vibrations in response to femalestimuli, whereas none vibrated their tails in response to male or control stimuli.Thus, significantly more males performed tail vibrations in response to femalestimuli than to either of the other two stimuli (P < 0.0003 each, one-tailed signtests).

Males rubbed their cloacal regions over the tile and cage bottom in nearlyall trials. There were only seven trials in the entire experiment in which thisrubbing behavior did not occur. Five males did not rub during trials with femalestimuli, and one each did not rub in the male stimulus and control conditions.No individual failed to perform cloacal rubbing in more than one trial. Differ-ences between pairs of conditions were not significant (P > 0.10, sign tests),but the data hint that males may be less likely to perform cloacal rubbing inresponse to female chemical stimuli than to male or control stimuli.

Female Responses. Females tongue-flicked at substantial rates in all con-ditions, with slightly higher rates in response to female stimuli than to the othertwo stimuli (Table 2). Variances of female tongue-flick rates differed signifi-cantly among conditions (Fmax = 3.98; df = 3, 27; P < 0.01). Mean tongue-flick rates by female E. macularius did not differ significantly among conditions(X? = 5.24; df= 2; 0.05 < P < 0.10, one-tailed).

Twenty-four of 28 females performed labial-licking (Table 2), but only twoindividuals did so in all three conditions. Thirteen females labial-licked only inresponse to male stimuli, three only to female stimuli, and none only to controlstimuli. Numbers of females labial-licking varied significantly among condi-tions: more females labial-licked in response to male stimuli than to either femalestimuli (sign test, P < 0.001) or controls (sign test, P « 0.001). There was

TABLE 2. RESPONSES BY 28 FEMALE Eublepharis macularius TO CONSPECIFICCHEMICALS AND CONTROL STIMULI

Tongue-flicks/5 minMeanSERange

Labial-licking (N)Chin-rubbing (N)

Male

46.43.7

23-1062110

Female

53.27.4

15-21171

Control

39.14.4

1-10970

no significant difference in numbers of females labial-licking between the femaleand control conditions (P > 0.10).

Slightly over one third of females rubbed their chins and throats along thetiles in response to male-labeled tiles. One female chin-rubbed on both male-labeled and female-labeled tiles, but none chin-rubbed a control tile (Table 2).Thus, significantly more females chin rubbed in response to male stimuli ineach case (female: P = 0.002; control: P < 0.001; sign tests).

DISCUSSION

Male Responses. Male Eublepharis macularius clearly detected and differ-entiated between male and female stimuli in tests using marked tiles. Detectionis implied by the difference in tongue-flick rates between the male stimulus andcontrol conditions. Discrimination of male from female chemical stimuli is indi-cated by the significantly lower tongue-flick rate in response to male-labeledthan female-labeled tiles. Detection and identification of male chemical stimuliby male E. macularius is confirmed by the aggressive responses—stilting andbiting—limited to the male stimulus condition. Elicitation of male aggressivebehaviors by conspecific male pheromones has also been documented in Sce-loporus occidentalis (Duvall, 1979) and Blanus cinerus (Cooper et al., 1994).

The lower tongue-flick rate to male stimuli than to female and controlstimuli confirms a report that male E. macularius tongue-flick at a lower ratein cages previously occupied by males than in clean cages (Brillet, 1990).Because tongue-flick rates are reduced rather than increased in male E. macu-larius by contact with conspecific male pheromones, identification must occurwithin the first few tongue-flicks, with further tongue-flicks serving perhaps forconfirmation and reinforcement of the original assessment.

In other lizard species, tongue-flick rates are elevated in response to malepheromones (Cooper and Vitt, 1986b; Cooper and Trauth, 1992; Cooper et al.,1994; Dussault and Krekorian, 1991; Duvall, 1979). Reasons for the differencein effect on tongue-flick rate by male pheromones from other species are obscure.Although little is known about the ecology of E. macularius, males of the relatedColeonyx variegatus may occupy the same sites for some time (Cooper et al.,1985a,b) and are aggressive to conspecific males (Greenberg, 1943). Triggeringby pheromones of species-typical aggressive displays and readiness for aggres-sive biting in the nocturnal leopard gecko might be an evolutionary response tothe difficulty of detecting intruding males visually. Readiness for aggression,possibly with improved detection of nonresident males, while in the elevatedstilting posture, interferes with further tongue-flicking of the substrate. Suchstilting (and presumably vigilance) often persisted for much of the trial in themale stimulus condition. Biting in response to male stimuli also suggests that


males are prepared to respond aggressively to a male whose pheromones havebeen detected. Diurnal species, readily able to detect other males visually, arefree to continue lingual investigation of pheromones.

The frequent marking in all conditions may indicate that leopard geckosmark novel substrates in their home ranges. Although differences among con-ditions were not significant, the fact that five of the seven instances in which amale did not perform marking behaviors occurred in response to female chemicalstimuli hints that there may be a somewhat stronger tendency to overmark pher-omonal deposits of other males and to mark unmarked surfaces than to markfemale pheromone deposits. By marking the area, a male may signal his occu-pancy status to intruders of both sexes, allowing nonresident males to avoidinteraction, and nonresident females to detect a potential mate.

Males discriminated female chemical stimuli from male chemical stimuliand control stimuli, but this was demonstrated by species-typical sexual behaviorrather than by lingual responses. Mean tongue-flicking rates did not demonstrateeven detection of female pheromones. Identification of female pheromones bymales is confirmed by the significantly greater number of males that vibratedtheir tails to female stimuli than to other stimuli. These results agree withBrillet’s (1990) finding that males performed tail vibrations almost exclusivelyin cages previously occupied by females, but did not tongue-flick differentiallyin clean cages and those previously occupied by females.

Performance of social behaviors including stilting, severe biting, and tailvibrations appropriate only for stimuli derived from only one sex (Mason andGutzke, 1990; Brillet, 1991, 1993) shows that males detect and respond differ-entially to male and female chemical stimuli even when tongue-flick rates donot differ. Preliminary investigation of conspecifics before performance of thesebehaviors is brief, often limited to single tongue-flicks, which supports thehypothesis based on the current data that chemosensory identification by malesoccurs rapidly. Following identification, performance of social behaviors maysuppress or reduce further tongue-flicking.

Female Responses. Tongue-flick rates yielded no evidence that femalesdetect conspecific pheromones. Brillet (1990) found no difference in tongue-flick rates in response to female stimuli and clean cages, but he reported thatfemales tongue-flicked significantly more in cages previously occupied by malesthan in clean cages. However, he did not test for differences among all condi-tions, accepted P = 0.06 as significant, and conducted many individual com-parisons without adjusting the level of significance. Appropriate procedureswould reveal no significant difference.

The significantly greater numbers of individuals that labial-licked and chin-rubbed when responding to male stimuli than to female or control stimuli showsthat females detected male pheromones. There was no indication that femalesdetected female chemical stimuli. These findings differ from those for Eumeces


laticeps, in which females clearly detected female chemical stimuli but did notrespond differentially to male and female chemical stimuli (Cooper and Vitt,1984b).

Differential labial-licking indicates that females detected male pheromonesand suggests that vomerolfaction or gustation may be involved. Labial-lickingmight allow an individual to glean more information from a sampled stimulusthrough redistribution on the tongue, resulting in contact with taste buds orenhancing the transfer to the vomeronasal organs (DePerno and Cooper, 1996).In addition, any molecules that adhere to the anterior labial scales during tongue-flicking might be sampled by labial-licking. Eublepharis macularius also per-forms labial-licks in response to prey chemicals (DePerno and Cooper, 1996),suggesting that labial-licking may function generally in the sampling of chem-icals that carry information useful to the animal.

The function of chin-rubbing is uncertain, but two possibilities seem worthyof investigation. First, females may deposit pheromones indicating their pres-ence in response to male pheromones. Chin-rubbing behavior has been foundin Sauromalus o. obesus (Berry, 1974) and Sceloporus jarrovi (Simon et al.,1981). Both sexes of 5. o. obesus chin-rub the substrate, and chin-rubbed siteselicit species-typical behavioral displays when encountered by conspecifics. Sec-ond, because physical manipulation of animal chemical deposits releases moresubstance (Alberts, 1992), chin-rubbing may release more pheromones forexamination. There is no evidence of increased tongue-flicking after chin-rub-bing, but chin-rubbing might place chemicals on the labials where they may betransferred to the vomeronasal organs (Graves and Halpern, 1989).

Although there is no strong evidence that females detect female phero-mones, neither is there any strong evidence that they do not. Females are notovertly aggressive toward each other and coexist well in the laboratory whenhoused together (personal observation). A similar lack of overt responsivenessto female pheromones has been reported for female Eumeces laticeps (Cooper,1996), a species also characterized by relatively low levels of interfemale aggres-sion. In contrast, female Cordylus cordylus, which are known to be territorialand aggressive toward other females, discriminate females pheromonally as indi-cated by differential tongue-flicking rates, but do not differentiate male phero-mones from controls (Cooper et al., 1996). The low aggression among femaleE. macularius might explain the lack of evidence for detection of female pher-omones by tongue-flicking or social behavior. Because little is known of thesocial structure of Eublepharis macularius outside captivity, potential benefitsof discriminating female pheromones are unclear.

Geckos have highly developed olfaction as well as vomerolfaction (Gabeand Saint Girons, 1976; Schwenk, 1993). Because tongue-flicking serves tosample chemicals for vomerolfaction (e.g., Halpern and Kubie, 1980; Gravesand Halpern, 1989), chemical discriminations based on olfaction might not be


accompanied by changes in tongue-flicking rates. In the related C. variegatus,recognition of snake predators may be based on olfaction rather than vomerol-faction (Dial et al., 1989). The olfactory response to pheromones might alsoaccount for the low tongue-flick rates of males, especially when responding toother males.

Acknowledgments—This work was partially supported by the School of Arts and Sciences ofIndiana University-Purdue University Fort Wayne. We are grateful to Brian Viets and Gary Fergusonfor supplying specimens and to Carla Barrett for providing animal care.

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PHEROMONAL DISCRIMINATION OF SEX BY MALE AND