AMER. ZOOL., 33:151-166 (1993) A Comparative Analysis of Scent-Marking, Social and Reproductive Behavior in 20 Species of Small Cats (Felis) 1 JILL D. MELLEN Conservation Research Program, Washington Park Zoo, 4001 S. W. Canyon Road, Portland, Oregon 97221 SYNOPSIS. Except for lions and cheetahs, members of family Felidae exhibit spatially and temporally dispersed social systems. However, this solitary existence does not preclude possession of a rich repertoire of communication signals. While patterns of communication have been examined in a number of the larger cats {e.g., lions, cheetahs, tigers), those of the smaller cats (<20 kg) remain virtually unstudied. The purpose of this study was to examine behavior in the smaller members of the Family Felidae to determine the level of behavioral uniformity within the family and to ascertain whether systematic behavioral observations could be used as an effective bioassay to monitor reproduction. A comparative examination of the occurrence and rate of scent marking, social behavior (especially behaviors associated with copulation), and other reproductive parameters was made in 20 species of captive, small felids. In general, small felids exhibited remarkable uniformity in their behavioral reper- toire, both with respect to scent-marking and social behaviors. While the frequency of social behaviors differed among species, their appearance and general order of occurrence was similar. This was especially apparent with regard to the copulatory sequence. Detectable behavioral changes occurred in association with reproduction, supporting the concept of using systematic behavioral observations as a viable, non-invasive assay for monitoring reproductive activity. Reproductively active felids scent marked more frequently than reproductively inactive cats. However, no single scent-marking behavior was a good indicator of reproductive activ- ity. Rather, the relative change in rates of behaviors over time was a better indicator of reproduction. As with scent-marking behaviors, a change in the relative rates of some social behaviors was the most reliable indicator of reproductive activity. Comparative behavioral data also show promise for understanding the phylogenetic relationships of three proposed lin- eages within the family Felidae (Panthera, ocelot, and domestic cat). INTRODUCTION although some cat species can be found in Members of the family Felidae comprise nearl y a11 terrestrial habitat types. Except for a unique group of highly specialized carni- lions and cheetahs, most adult felids are vores found on all continents except Aus- intolerant towards adults of the same sex tralia and Antarctica. Characterized by rel- and commonly exhibit a spatially and tem- atively short muzzles, highly sectorial porally dispersed social system (Bekoff et carnassials and sharp retractile claws, cat al., 1984). However, such solitary existence species range in size from small (1.5 kg) to does not Preclude the "asocial" members of very large (300 kg). Felids predominate in the family Felidae from possessing a rich woodland and woodland-fringe terrain repertoire of communicative signals (Ley- hausen, 1965; Eisenberg et al, 1972; Klei- ~ „ , , man and Eisenberg, 1973; Seidensticker et 1 From the Symposium on Basic Behavior Research • \Q~I\\ in Zoos: A Link with the Wild presented at the Annual L~ y .f >' . Meeting of the American Society of Zoologists, 27-30 Detailed field observations ot felld COm- December 1991, at Atlanta, Georgia. munication are limited to a few of the larger 151
Transcript
AMER. ZOOL., 33:151-166 (1993)
A Comparative Analysis of Scent-Marking, Social andReproductive Behavior in 20 Species of Small Cats (Felis)1
JILL D. MELLEN
Conservation Research Program, Washington Park Zoo, 4001 S. W. Canyon Road,Portland, Oregon 97221
SYNOPSIS. Except for lions and cheetahs, members of family Felidaeexhibit spatially and temporally dispersed social systems. However, thissolitary existence does not preclude possession of a rich repertoire ofcommunication signals. While patterns of communication have beenexamined in a number of the larger cats {e.g., lions, cheetahs, tigers), thoseof the smaller cats (<20 kg) remain virtually unstudied. The purpose ofthis study was to examine behavior in the smaller members of the FamilyFelidae to determine the level of behavioral uniformity within the familyand to ascertain whether systematic behavioral observations could beused as an effective bioassay to monitor reproduction. A comparativeexamination of the occurrence and rate of scent marking, social behavior(especially behaviors associated with copulation), and other reproductiveparameters was made in 20 species of captive, small felids. In general,small felids exhibited remarkable uniformity in their behavioral reper-toire, both with respect to scent-marking and social behaviors. While thefrequency of social behaviors differed among species, their appearanceand general order of occurrence was similar. This was especially apparentwith regard to the copulatory sequence. Detectable behavioral changesoccurred in association with reproduction, supporting the concept of usingsystematic behavioral observations as a viable, non-invasive assay formonitoring reproductive activity. Reproductively active felids scentmarked more frequently than reproductively inactive cats. However, nosingle scent-marking behavior was a good indicator of reproductive activ-ity. Rather, the relative change in rates of behaviors over time was a betterindicator of reproduction. As with scent-marking behaviors, a change inthe relative rates of some social behaviors was the most reliable indicatorof reproductive activity. Comparative behavioral data also show promisefor understanding the phylogenetic relationships of three proposed lin-eages within the family Felidae (Panthera, ocelot, and domestic cat).
INTRODUCTION although some cat species can be found inMembers of the family Felidae comprise n e a r l y a11 terrestrial habitat types. Except for
a unique group of highly specialized carni- lions and cheetahs, most adult felids arevores found on all continents except Aus- intolerant towards adults of the same sextralia and Antarctica. Characterized by rel- a n d commonly exhibit a spatially and tem-atively short muzzles, highly sectorial porally dispersed social system (Bekoff etcarnassials and sharp retractile claws, cat al., 1984). However, such solitary existencespecies range in size from small (1.5 kg) to d o e s n o t Preclude the "asocial" members ofvery large (300 kg). Felids predominate in t h e family Felidae from possessing a richwoodland and woodland-fringe terrain repertoire of communicative signals (Ley-
hausen, 1965; Eisenberg et al, 1972; Klei-~ „ , , man and Eisenberg, 1973; Seidensticker et
1 From the Symposium on Basic Behavior Research • \Q~I\\in Zoos: A Link with the Wild presented at the Annual L~ y .f >' .Meeting of the American Society of Zoologists, 27-30 Detailed field observations ot felld COm-December 1991, at Atlanta, Georgia. munication are limited to a few of the larger
ocelot ASDM [historical data only] 0.00San Diego [historical data only] 0.00Sacto [historical data only] 0.00
ocelot Cincin 17 Oct-28 Oct 88 3.25Cincin 17 Oct-28 Oct 88 4.17
domestic cat San Diego 30 Mar-9 Apr 88 6.00
Panthera Pt. Lympne 2 Apr-15 Apr 89 3.00
Panthera Sacto 3Mar-18May85 31.75
domestic cat WPZ 3 Jan-30 Aug 87 168.40
Total Number of Hours 685.02
m
3
oo•n
1 From Waynes a/., 1989.2 Brkfld = Chicago Zoological Park, Brookfield, IL; NZP = National Zoological Park, Washington, D.C.; WPZ = Washington Park Zoo, Portland, OR; Sacto
= Sacramento Zoo, Sacramento, CA: ASDM = Arizona-Sonora Desert Museum, Tucson, AZ; San Diego = San Diego Zoo, San Diego, CA; Cincin = CincinnatiZoological Garden, Cincinnati, OH; Pt. Lympne = Pt. Lympne, Kent, England.
TABLE 2. Marking behavior for male and female captive small felids.
cat species: lions (Schaller, 1972), cheetahs(Caro and Collins, 1987), tigers (Sunquist,1981; Smith et al, 1989), cougars (Seiden-sticker et al, 1973). Additional data havebeen obtained via observations of captiveanimals: snow leopards (Freeman, 1983),tigers (Kleiman, 1974), and cheetahs (King,1983). Substantially less information existsabout the smaller members of the familyFelidae. "Small cats" are denned here asthose species with an adult body weight ofless than 20 kg (Emmons, 1991, p. 62). Thenocturnal pattern of activity, the use ofdensely vegetated habitat, wide-rangingmovements, and often wariness because ofintense hunting pressures preclude obtain-ing this information in situ for most felids,and especially the small cats.
The purpose of this study was to examinebehavior among the smaller members of theFamily Felidae to determine the level ofbehavioral uniformity within the family andto ascertain whether systematic behavioralobservations could be used as an effectivebioassay to monitor reproduction. Toinvestigate these questions, comparativeexamination of the occurrence and rate ofscent marking, social behavior (especiallybehaviors associated with copulation), andother reproductive parameters was madeacross 20 of the 29 species of captive smallfelids. This number represents all but 3 ofthe species of small cats currently held inNorth American and European zoos.
METHODS
Data were collected on a total of 134 indi-viduals (65 males, 69 females) representing20 Felis species from eight zoological insti-tutions. Information on species and numberof animals observed as well as where, when,and how long each was observed is includedin Table 1. Other information on subjectsand their respective captive environmentsare detailed in Mellen (1989, 1991, 1992).
Behavioral data were collected via directobservation using all occurrences of selectedbehaviors sampling methods (Altmann,1974). Behaviors associated with scentmarking, drawn from Mellen (1988), weredefined as follows:
cheek rubbing: cheek of cat is rubbedagainst an inanimate object
156 JILL D. MELLEN
"sharpening" claws: claws of front pawsare used to scratch a surface (usually wood)
urine marking: cat urinates on verticalsurface; tail is usually held straight up andsometimes the distal third is vibrated orappears to quiver; behavior sometimesincludes scraping substrate with hind feet
jlehmen: open-mouth grimace followingthe sniffing of an object or cat.
Other solitary behaviors included:
head rubbing: head (forehead region) ofcat rubbed against an inanimate object
neck rubbing: cat vigorously rubs/scrapeslateral portions of neck against an inanimateobject or along substrate.
Social behaviors included the following:
spit/hiss/growl vocalizations: cat orientsto another cat and emits a spit/hiss/growlvocalization
strike/strike at with paw: cat strikes orstrikes at (i.e., no contact is made) anotherwith its paw
mounting: for the male, mount is dorso-ventral with nape bite and straddling of thefemale with both front feet and hind feet:"pelvic" thrusting, stepping with hind feet,and/or intromission may occur; for thefemale, lordosis posture, treading with hindfeet, deflecting tail to one side, and "copu-latory cry" may occur
lordosis: female lowers her forequarterswhile elevating her hindquarters; tail is oftenmoved to one side
social head rubbing: head (foreheadregion) is rubbed against another cat
social grooming: one cat licks and/or nib-bles on the fur of another cat
anogenital sniffing: cat sniffs the anogen-ital region of another cat
social sniffing: cat sniffs any region otherthan the anogenital region of another cat
following: cat follows within two bodylengths of other cat for a distance of at leasttwo body lengths
displacing: cat directly approaches anothercat (within one body length) and within fiveseconds of the approach, the second catmoves away at least one body length
approaching: cat directly approachesanother cat (within one body length) andthe cat approached does not move away
chasing: one cat runs at or after anothercat
face-off: both cats simultaneously face oneanother (usually both are in a sitting posi-tion); cats are within one to two body lengthsof each other and stare directly at each other;this behavior is usually preceded and/or fol-lowed by an agonistic interaction; durationis variable (10 sec to 2 min).
Behavioral observations were made dur-ing regular visitor hours at each zoo, between09:00 and 17:00 local time. This time framewas chosen because a major purpose of thisstudy was to determine if behavioral obser-vations could be used as an effective assayfor monitoring reproductive functions.While these predominantly nocturnal/cre-puscular cats may have exhibited a sub-stantial portion of their behavior at night,the author wanted to determine if behaviorsexhibited by the cats during regular zoohours (the time period when most zoo per-sonnel/volunteers/students are present tomake such observations) could be used todetect reproductive activity.
Data on reproductive parameters, lengthof estrus, gestation, mean litter size, sex ratioof litter, etc.) were obtained by reviewingmedical, keeper, and ISIS (InternationalSpecies Information System) records.
RESULTS
Behaviors associated with scent markingA summary of data on behaviors asso-
ciated with scent marking are presented inTable 2. Average rates for each behavior arepresented for those cats that were studiedfor at least 8 weeks. Some behaviors asso-ciated with scent marking were noted out-side of a formal observational setting (andthus not quantified); their occurrence isindicated by a plus (+) sign.
Cheek rubbing.—Most species of catsobserved in the present study cheek rubbed(Table 2) and the rate at which cheek rub-bing occurred was about equal for both malesand females (Fig. la). In general, cheek rub-bing occurred more frequently amongreproductively active pairs (Fig. la).
Head rubbing. —No trends were apparentwith regard to the relative rates of head rub-bing between the sexes or between repro-
FIG. 1. Average rates of selected scent-marking behaviors which allow for comparisons of those individualsthat demonstrated reproductive activity to those individuals that were not reproductively active. Bold printindicates data from those pairs in which the female was in estrus during some portion of the observation set.m = male; f = female; 1 = Pallas' cat (Brkfld); 2 = sand cat (Brkfld); 3 = sand cat (WPZ); 4 = fishing cat (WPZ);5 = Temmincks' golden cat (WPZ); 6 = jungle cat (Sacto); 7 = serval (WPZ); 8 = serval (NZP, Sacto); 9 =caracal (Sacto); 10 = caracal (Sacto); 11 = Geoffrey's cat (WPZ); 12 = Geoffrey's cat (NZP); 13 = Canadianlynx (Sacto); 14 = domestic cat (WPZ).
ductively active versus inactive individuals(Fig. lb). When data from Table 2 are com-pared to those compiled by Wemmer andScow (1977), head rubbing was observed inrelatively fewer species in the present study.However, Wemmer and Scow (1977)describe head rubbing, including recumbenthead rubbing, to be evoked by strong, novelodors such as carrion, vomit, feces of strangeanimals, and catnip. Since the pairs observedin the present study had little exposure tonovel odors, the probability of observingthese behaviors may have been reduced.
Neck rubbing.—Neck rubbing is similarto Wemmer and Scow's description (1977)of recumbent head rubbing and wasobserved in apparent response to the urine
marks of a mate. This behavior also wasseen frequently in both males and femalesexamined in the present study during intro-ductions of pairs and when a female was inestrus (see Mellen, 1989).
"Sharpen" claws. — This behavior wasobserved in most species examined in thepresent study (Table 2; Fig. lc). Sharpeningclaws occurred at a somewhat higher ratein males than females and its relative occur-rence does not seem to be related solely toreproductive activity. It was a frequentlyobserved behavior, seen both as a compo-nent of scent-marking behavior (e.g., occur-ring in the same areas as urine marking) andas apparent "displacement" when an estrous
TABLE 3. Occurrences of social behaviors in small felids.oo
Sex Spit Hiss Growl Strike at
Strikewithpaw Bite Mount
Napebite Lordosis
Socialhead rub
Socialgroom
Ano-gemtal
sniffSocialsniff Follow Displace
Ap-proach Chase Face off
Asian CatsPallas' cat
sand cat
fishing cat
Temminck's golden cat
jungle cat
rusty-spotted cat
Indian desert cat
African Catsserval
caracal
black-footed cat
African golden cat
South American CatsGeoffrey's cat
jaguarundi
ocelot
Pampas cat
malefemalemalefemalemalefemalemale
malefemalemalefemalemalefemale
malefemalemalefemalemalefemalemalefemale
malefemalemalefemalemalefemalemalefemale
o
tfl
i
REPRODUCTIVE BEHAVIOR OF CAPTIVE FELIDS 159
HE
• 5 5
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1-5*
cd
E
§.-§
II l
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o cE .2< • §
eo
.
2 E<- o
I'
female repeatedly and vigorously threat-ened a male.
Flehmen.—Observations made during thepresent study support the general patterndescribed elsewhere (e.g., Wemmer andScow, 1977; Wright and Walters, 1980; Hartand Hart, 1985). Typically, a urine mark isapproached, sniffed, and then the cat exhib-its a flehmen response. When a small catflehms, it raises its head and drops its lowerjaw so that the mouth is half open. The catappears almost immobilized, has a staringlook, and breathes slowly. In this study, bothsexes of most species were observed to flehm(Table 2) but males exhibited a consistentlyhigher rate than females (Fig. Id). Males ofmost species examined showed a rise in therate of flehmen during those periods whencopulations were observed.
Urine marking.—Males of all speciesobserved and females of most speciesobserved urine marked, i.e., sprayed urineon a vertical surface (Table 2; Fig. le). Malesof most species sprayed urine at a higherrate than did females. A notable exceptionwas female servals.
In the present study, two behaviors per-formed often in association with urinemarking or spraying were as follows: 1)scraping with the hind feet, and, 2) "tailquiver." Table 2 identifies which speciesexhibited each of these behaviors. Whenspraying urine, virtually all species observedraised their tails vertically while spraying.In some species, the terminal third of thetail sometimes twitched or quivered duringthe spraying.
Social behavior of captive small felidsCats communicate with one another via
a combination of visual, auditory, andolfactory signals. The previous section onscent-marking behaviors addressed someaspects of olfactory communication. Audi-tory communication was not examined inthis study because observations often weremade through glass barriers or in situationswith substantial background noise that pre-vented collection of systematic data onvocalization. (See Peters and Wozencraft,1989, for a review of vocal communicationin felids.) However, visual communicationwas measured with respect to selected social
160
Asian CatsPallas' catsand catfishing catTemminck's golden catjungle catrusty-spotted catIndian desert cat
African Catsservalcaracalblack-footed catAfrican golden cat
South American CatsGeoffroy's catjaguarundiocelotmargayPampas cat
European CatsScottish wildcatSiberian lynx
North American CatsCanadian lynx
Worldwide Distributiondomestic cat
JILL D. MELLEN
TABLE 4. Reproductive data for captive small felids.
' Mount with intromission; n = number of observations.2 Mounts observed but no apparent intromission.3 Period of interest by male &/or period of rubbing/rolling/> vocalization by female.4 Measured from the first day mounting was observed during each of two consecutive estrous periods.5 Calculated from last day of observed mounts.6 See Mellen, 1989.7 n = number of litters.8 Males.females.sex unknown.9 Females' date of birth to birth of 1st litter produced; male's date of birth to 1st litter sired.
behaviors. Because the goal of the presentstudy was not a systematic evaluation ofvisual communication modes, but ratherwhether measurable changes in thesebehaviors might indicate reproductiveactivity, discussion of social behaviors willbe limited to that context.
Social behavior represents only 1-2% ofthe time budgets of small cats in captivity(Mellen, 1989), so the rates of occurrenceof various social behaviors were very low.Table 3 lists the social behaviors observedduring the present study with an indicationof whether or not each species exhibited eachbehavior. These data are meant to provide
an overview of the occurrence of selectedsocial behavior among these species of catsand to demonstrate the relative uniformityof these cats' behavioral morphology.
Reproductive data for captivesmall felids
The study of captive animals facilitatesthe determination of a wide variety ofreproductive parameters that would be dif-ficult, if not impossible, to gather in situ. Inthe process of gathering behavioral data ateight zoological institutions, the author hadan opportunity to glean information regard-ing a wide variety of reproductive param-
eters from zoological records. Table 4 con-tains a compilation of selected reproductivedata obtained during the present studyincluding length of estrus, gestation, meanlitter size, sex ratio of litters, and age at firstmaturity. The data in Table 4 are originaland do not synthesize published informa-tion.
Copulatory behavior.—The copulatorybehavior of small cats shows marked sim-ilarities among the species that have beenstudied. Their copulatory pattern has beendescribed as one with "no lock, no intra-vaginal thrusting, ejaculation on a singleinsertion, and multiple ejaculations"(Dewsbury, 1972; Lanier and Dewsbury,1976).
In this study, nine species of small catswere observed to copulate. The typical cop-ulatory sequence recorded was as follows:the male approached the female, graspedher by the nape, mounted by straddling the
female first with the front feet and then withthe hind feet. The female responded to thenape bite by adopting a lordosis posture andmoving her tail to one side; the femalesometimes also treaded with her hind feet.At this point, the male occasionally beganstepping with his hind feet, often simulta-neously rubbing against the female's flanks.The latter may induce the female to adjustor to exaggerate her lordosis posture. Themale then began "pelvic" thrusting. (Lanierand Dewsbury [1976] term this behavior"extra-vaginal pelvic thrusting" and believeit to function in detecting the vaginal ori-fice.) In the present study, "pelvic" thrust-ing typically lasted one-five min. In mostinstances, the male maintained a firm graspon the female's nape throughout the mount.Intromission is apparently signalled by a"copulatory cry" given by the female; thisvocalization was typically a low, barelyaudible growl. Five to ten seconds after the
162
Asian CatsPallas' catsand catfishing catTemminck's golden catjungle catrusty-spotted catIndian desert cat
African Catsservalcaracalblack-footed catAfrican golden cat
South American CatsGeoffrey's catjaguarundiocelotmargayPampas cat
European CatsScottish wildcatSiberian lynx
North American CatsCanadian lynx
Worldwide Distributiondomestic cat
JILL D. MELLEN
TABLE 4. Extended.
Young rearedby mother
in captivity?
yesyesyesyesyesyes
yesyesyesyes
yesyesyesyesyes
yesyes
—
yes
2nd generationyoung produced
in captivity?
yesyesyesyesyesyes
yesyesyesno
yesyesyes
yes
yes-
-
yes
Data based upon:
7 litters to 5 pairs of 4.4 cats25 litters to 6 pairs of 5.5 cats13 litters to 4 pair of 4.4 cats9 litters to 2 pairs of 2.1 cats1 litter to 1 pair of 1.1 cats9 litter to 3 pair of 3.3 cats
16 litters to 3 pairs of 3.3 cats
15 litters to 5 pairs of 3.5 cats8 litters to 5 pairs of 4.5 cats9 litters to 4 pair of 3.4 cats
14 litters to 3 pairs of 2.3 cats12 litters to 4 pairs of 4.3 cats28 litters to 9 pairs of 7.8 cats17 litters to 3 pairs of 3.3 cats13 litters to 3 pairs of 3.2 cats
10 litters to 3 pairs of 2.3 cats9 litters to 1 pair of 1.1 cats
0 litters to 1 pair of 1.1 cats
8 litters to 8 pairs of 2.8 cats
female emitted this vocalization, she threwthe male off her back, often threatening him,and began vigorously rolling on her back.Rolling on the back typically lasted five tothirty seconds. Both the male and femaleusually then groomed their own anogenitalregions. Numerous mounts were observedin the present study, but it was assumed thatintromission occurred only when mountswere followed by a "copulatory cry" androlling by the female.
The most reliable indicator of estrus and/or reproductive activity identified in thisstudy was a change in the relative rates ofsome behaviors. Figures 2 and 3 illustratethis observation.
DISCUSSION
While the initial intent of this study wasto determine whether systematic behavioralobservations could serve as an effective assayfor monitoring reproductive activity, this
very applied research question also resultedin the acquisition of substantial basic infor-mation about the behavior of a wide rangeof felid species. Discussion of of thesebehaviors in the context of previously pub-lished information is presented below.
Behaviors associated with scent markingUrine, feces, and glandular secretions
presumably carry chemical information.Scent-marking behavior may function notonly to deposit information-laden odors, butthe scent may be delivered in such a way asto be visually conspicuous, e.g., scrapingwith hind feet (Wemmer and Scow, 1977).
Cats presumably rub saliva onto inani-mate objects during cheek rubbing (Ewer,1973; Fox, 1974; Wemmer and Scow, 1977).They also cheek rub against objects whichhave previously been sprayed with urine(Wemmer and Scow, 1977). Male domesticcats can differentiate phases of the estrous
REPRODUCTIVE BEHAVIOR OF CAPTIVE FELIDS 163
Sacramento Male Caracal (L&R Pair) Sacramento Female Caracal (L&R Pair)
•- Cheek Rub
-o- Sharpen Claws
• • Flehmen
o- Mark
a
1e1
r
4 ,
35
3
2.5
2
1 5
1
0 5 .
Di
• • M mount F
•o- Ma/gsnittF
• - MtoJIF
•o- M approaches F
Sacramento Female Caracal (L&fl Pair)
2 3 4 S 6 7 8 9 10 11 124 Weeks A
FIG. 2. Rates of selected behaviors exhibited by a pair of reproductively active caracals (Felis caracal). Arrowsindicate those weeks in which reproductive activity was observed, a/g sniff = anogenital sniffing; foil = following.
cycle of females from cheek gland secretions not as a "marking" behavior (i.e., laying(Verberne and DeBoer, 1976). Reiger(1979) down a scent), but rather to pick up scentand Reiger and Walzthonz (1979) contend from the substrate. They further suggest thatthat cheek rubbing in the Felidae functions cheek rubbing serves as a visual display.
WPZ M a * Sand CM WPZ FsrnaJ* Sand Cat
- ChMkRub
- Rahman
- Mark
2 3 4 5 6 7 8 9 10
A WMkl 4
WPZ Mart Sand Cat WPZ Fcmala Sand Cat
t
«- Haad Rub-lnan
o- RoflonBack
• - Vocalization
t tFIG. 3. Rates of selected behaviors exhibited by a pair of reproductively active sand cats (Felis margarita).Arrows indicate those weeks in which reproductive activity was observed, a/g sniff = anogenital sniffing; foil =following; Head Rub-lnan = head rubbing an inanimate object.
164 JILL D. MELLEN
Data from the present study suggest thatcheek rubbing serves all three functions; todeposit a scent (saliva), to pick up scent (bycheek rubbing against urine marks), and asa visual display (males frequently orientedto estrous females and repeatedly cheekrubbed). See also Mellen (1989).
Claw "sharpening" probably does notfunction to "sharpen" claws per se, butrather may facilitate removal of loosenedclaw sheaths and may also serve to leave avisual signal by modifying or disturbing thesubstrate (Wemmer and Scow, 1977). Datafrom the present study support this inter-pretation.
The flehmen response, its relationship tothe vomeronasal organ (VNO), and the roleof the VNO have been systematically inves-tigated in domestic cats (Verberne, 1976).Cats utilize the VNO, an accessory olfactorysystem, through the flehmen response toexamine urine (or other substances) for thepresence of nonvolatile chemical sub-stances. Flehmen and the use of the VNOsystem appear to be involved in confirmingor refining olfactory discrimination by theprimary olfactory system.
A flehmen response may be universalamong the Felidae (Ewer, 1973). In thisstudy, both sexes of most species wereobserved to exhibit a flehmen, providingsupport for Ewer's suggestion. Male domes-tic cats are reported to flehm more fre-quently than females (Hart, 1985); the pres-ent study demonstrated that in virtually allpairs observed, the male's rate of flehmenwas higher than the female's. This studyalso indicates that the occurrence of fleh-men is a good indicator of reproductiveactivity; males of most species studiedexhibited a sharp rise in the frequency offlehmen responses two to three days priorto when copulations were observed.
In felids, the most conspicuous scent-marking behavior is performed by sprayingurine against vertical objects (Fiedler, 1955;Verberne, 1976; Schaller, 1972; Verberneand Leyhausen, 1976; Leyhausen, 1979). Inthe present study, males typically sprayedurine at a higher rate than did females.Although urine appears to be used to marka felid's territory, the urine spot itself seemsnot to be a deterrent. Instead it provides
temporal information and may reduce theprobability of confrontation (Hornocker,1969; Schaller, 1972; Fox, 1974; DeBoer,1977).
Wemmer and Scow (1977) suggest thatthe tail is raised just prior to spraying tohelp direct and position the spray. They fur-ther add that quivering or twitching of theend of the tail may serve as a visual signalor may simply be an automatic manifesta-tion coupled with urine emission. Duringthe present study, the tail quiver was notobserved to accompany every bout of spray-ing. The cats instead exhibited a tail quiverduring sprays that appeared particularly"vigorous" in execution.
Detectable behavioral changes in scentmarking occurred in association with repro-duction, supporting the concept of usingsystematic behavioral observations as a via-ble, non-invasive assay for monitoringreproductive activity. In general, reproduc-tively active felids display a higher rate ofscent-marking behavior. However, no sin-gle scent-marking behavior was a good indi-cator of reproductive activity. Rather, therelative change in rates of some behaviorsover time were the best indicators of repro-duction. When plotted over time, somescent-marking behaviors or some combi-nations of those behaviors typically showeda dramatic increase in association with thoseperiods when copulations were observed.The scent-marking behaviors that showedincreases in association with reproductiveactivity differed with species, sex, and indi-vidual.
Social behavior of small catsWhile small felids vary widely in the hab-
itats they use and the prey items they exploit,these cats are remarkably similar with regardto the behavioral mechanisms they use tocommunicate with conspecifics. The rela-tive frequency of social behaviors differed,but their appearance and the general orderof occurrence was similar among the speciesobserved. For example, the copulatorysequence among the felid species observedin the present study is similar to other felidspecies, including the larger cats (Ewer, 1973;Lanier and Dewsbury, 1976; Leyhausen,1979). As with scent-marking behavior, no
REPRODUCTIVE BEHAVIOR OF CAPTIVE FELIDS 165
single social behavior measured could reli-ably predict copulation, but when the changein relative frequencies of these social behav-iors were plotted over time, selected socialbehaviors were observed to increase simul-taneously in association with observed cop-ulations. In this study, the most reliableindicator of estrus and/or reproductiveactivity was a change in the relative ratesof some behaviors.
Behavioral patterns associated with thethree lineages ofFelidae
Comparative behavioral data also showpromise for understanding the phylogeneticrelationships of three proposed lineageswithin the family Felidae. When behaviorsof small cats are examined in the context ofthese three proposed lineages, i.e., Panth-era, ocelot, and domestic cat (Collier andO'Brien, 1985), some intriguing patternsemerge. One example involves the behaviorscraping with the hind feet which wasobserved in most species within the ocelotand Panthera lineages, but was seen in onlyone species within the domestic cat lineage,Pallas' cat. Pallas' cat is a species that mayrepresent the sister group of the remainderof the domestic cat lineage (see Wayne etai, 1989).
A second example involves the occur-rence of a nape bite during copulation. Tra-ditionally, one of the most pronounceddichotomies between "large" and "small"cats has been the absence of the nape biteduring copulation in the large cats. Indeedwithin the domestic cat lineage, the napebite often seems to be necessary for themale's ability to safely and successfully cop-ulate (personal observation). In this studymales of two species (the male ocelot [ocelotlineage] and male Temminck's golden cat[Panthera lineage]) displayed an interme-diate behavior: each was observed to ini-tiate a mount with a nape bite, but releasethe grip on the female's nape during themount, grasping the nape again at or nearthe time of intromission. It has been spec-ulated that the absence of the nape bite inthe larger cats (e.g., lions, tigers, jaguars) isdue to the potential risk of injury to thefemale by the male's extremely large canineteeth (Lanier and Dewsbury, 1976; Wem-
mer and Scow, 1977). The absence of a sus-tained nape bite during the mount in thegolden cat may represent a transitional statebetween the sustained nape bite found inthe domestic cat lineage and the lack of anape bite in the Panthera lineage. The inter-mediate condition displayed by the ocelotposes intriguing problems that beg a moredetailed phylogenetic analysis. These exam-ples indicate that a thorough examinationof comparative behavioral data might con-tribute significantly to hypotheses devel-oped using recent molecular data (Wayneet. al, 1989) and help elucidate the rela-tionships of groups within the family Feli-dae.
ACKNOWLEDGMENTS
Eight zoos provided me with the oppor-tunity to study their collections of small cats:Brookfield Zoo, Sacramento Zoo, NationalZoological Park, Washington Park Zoo,Arizona-Sonora Desert Museum, San DiegoZoo, Cincinnati Zoo, and Port Lympne Zooin England. T am grateful to the curators,researchers, and administrators of each ofthese zoos who ultimately made these stud-ies possible. I thank the Chicago ZoologicalSociety and the Friends of the National Zoofor the summer stipends that supported mywork. A grant from the Institute of MuseumServices allowed me to study collections ofsmall cats at Arizona-Sonora DesertMuseum, San Diego Zoo, Cincinnati Zoo,and Port Lympne Zoo. I gratefully acknowl-edge this assistance. I thank Drs. Sue Ellis-Joseph, John Seidensticker, and Marc Hayesfor the careful reviews and insightful com-ments on the various drafts of this paper. Iam especially indebted to John Seiden-sticker of the National Zoo who has beenvery influential in my way of thinking aboutfelids. And finally, I want to express mygratitude to all the keepers who graciouslyanswered my innumerable questions abouttheir cats, helped me in the acquisition ofmy data base, and shared their insights onthese enigmatic animals.
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