Predation and predatory play behaviour of domestic cats

Anitn. Behv.,

1979, 27, 81-94

PREDATION

AND PREDATORY PLAY BEHAVIOUR CATS

OF DOMESTIC

BY MAXEEN BIBEN Department of Zoology, University of North Carolina, Chapel Hill, N.C. 27514” Abstract. This study investigated the factors controlling behavioural responses of the domestic cat to its prey. Experiment 1 identified three temporally-associated groups of behaviours, and associated these differentially with killing. Cat behaviours were independent of prey activity. Hunger was not a necessary condition for killing. In experiment 2, I manipulated hunger and the size of the prey. 1 found that: (1) The probability of a kill increased directly with hunger. (2) When the prey was large or difficult, the probability of a kill decreased. (3) The probability of killing was predictable if the levels of the factors hunger and prey size were known. (4) When these factors were in conflict, cats tended to play with the nrev before. after. or instead of. killing. The relevance of these results to other studies of the control of brehatory and playful behaviobrs is vdiscussed. The wide range of behaviour patterns occurring in predator-prey encounters provides a useful framework for testing short-term changes in the tendency to kill. Sampling the same individual on different occasions, one might see such different responses as killing, avoidance of the prey, or active, playful behaviour (directed at the prey, but not injuring it). This study is aimed at identifying the factor or factors which control these short-term changes in response. The most extensive previous studies of feild predatory behaviour are those of Leyhausen (1956, 1965, 1973). Leyhausen documented typical predatory sequences of domestic and other cats, where prey was sighted, pursued, captured, killed, and eaten. He also observed instances where cats played with their prey, pursued but did not capture, and killed but did not eat. Leyhausen hypothesized (1965) separate drives for pursuit, capture, killing, etc., operating independently of each other and of the cat’s hunger state. This fits well with earlier theories of Lorenz (1950) concerning the unitary nature of drives, but has since been refuted by studies of other predators. Mueller (1973), for example, found predatory killing by American kestrels to be highly correlated with hunger. Kruuk (1972) reviewed surplus killing by mammalian predators and concluded that hunger triggered the initial (hunting) stages of predatory behaviour but was unnecessary when the prey was at close range, at which point the proximity of the prey was sufficient to initiate capture and killing. Because of the confusion which these contradictory conclusions have

generated, I designed my study to illuminate the factor or factors that control predatory behaviour, and the manner and degree to which they do so. Two experiments are reported here. The first is a normative study identifying the range of behaviour that occurs when a cat encounters prey. The data are then inspected for statistical relationships which provide clues to the differential causation of behaviour patterns. In the second experiment, important factors identified in the first experiment are manipulated to determine how changes in these factors change behavioural response. When the alteration of a single factor in a system results in predictable change in the tendency to show a certain behavioural outcome, then this factor may be said to control that outcome, at least in part. In the predatorprey system studied here, the tendency to kill a certain type of prey is easily altered on a day to day basis by altering the predator’s hunger level. Alternatively, killing tendency also varies if hunger is held constant and the type of prey is changed. It is this ease of manipulation that makes the predator-prey system such a convenient model for the study of control mechanisms. Methods I performed the experiments in two identical 2.77 x 2-87-m controlled-environment rooms constructed of concrete and cinder blocks. The rooms were windowless; a 12-h light/l2 h dark cycle was maintained automatically and the temperature was kept between 20 and 25 C. I restricted observations to the cats’ late afternoon hours, the time when they were always fed and when they might be expected to be active.

*Present address: Smithsonian Institution, National Zoological Park Conservation and Research Center, Front Royal, Virginia 22630, U.S.A.

81

The controlled-environment rooms were empty except for lighting, timing, and temperaturecontrol fixtures mounted high on the walls and ceilings. A litter box. food and water bowls. and a sleeping bench or shelf were provided at or near lloor level. A cat under observation was housed in one of the controlled-environment rooms, which had been equipped with a blind. I introduced prey into the room by sliding back a windowpane and dropping the prey to the floor, or by pushing the blind back momentarily. Experiment 1 Methods Eight cats were used in this initial study. Five were former housepets, obtained from private individuals, and had had ample opportunity foi hunting. At the time of the study these cats (except for one obtained within a month of the study) had been housed in the laboratory (females communally, males caged separately) for periods ranging from 1 to 3 years. The remaining three cats were born and raised in the laboratory, Their contact with each other, with other cats, and with prey was limited. All cats were given occasional opportunities to kill mice, and all had killed at least a few times prior to the experiments. My laboratory-raised cats all became killers after repeated exposures to mice, although their killing behaviour (indeed, all facets of their behaviour) was easily disrupted by placing these cats in a different room or by otherwise altering their surroundings. Two types of prey were used : laboratory mice and young domestic chickens. Mice were of mixed genetic background, weighing between 25 and 35 g when used. Although their exploratory activity varied greatly, they generally showed little fear of or interest in cats. Mice defended themselves only when seized or struck and usually did not avoid the cat after such an encounter. White Rock chicks, a broiler breed, were obtained at 1 day of age from a local hatchery. They were used only from I to 10 days of age. Like mice, chicks showed individual variation in activity, but no fear of cats. There were no hiding places for prey in the test arena and all prey were easy to spot and capture. Recording of Behaviour Patterns In a separate pilot experiment, I observed the mouse-catching of six cats (all used again in later experiments) in the cats’ home cages, the laboratory, and in my home. Using a sampling

method similar to the Focal-Animal Sampling of J. Altmann (1974), I identified 20 categories of behaviour which could be reliably distinguished from one another. In recording these behaviours. I used time-sampling procedures as outlined by Altmann, and Hutt & Hutt (1970). i\ 15-s interval was adequate for the majority of my behavioural categories, most of which lasted longer than 15 s, or were repetitions. One important exception was the killing bite, which sometimes lasted only a few seconds. Killing bites were always scored as occurring at the nearest sampling point. I sampled behavioural ‘states’ (the category of behaviour that was ongoing at the moment the sample was taken) rather than behavioural ‘events’ (the isolated motor pattern occurring at the instant of sampling) in accordance with the suggestions of J. Altmann (1974) for timesampling procedures. In addition to monitoring the behaviour of the cat, I also kept a concurrent record of the prey’s behaviour. Preliminary observations indicated that it was sufficient to record the prey’s general level of activity rather than specific behaviour. I recorded prey activity at 15-s intervals. Experimental Procedure I tested cats daily for 15 consecutive days, after allowing them 5 days to habituate to the test room. Because killing by non-hungry cats (that is, surplus or excessive killing) is an important theoretical consideration in the control of predatory behaviour, I offered cats canned cat food prior to testing, supplementary to their diet of ad libitum dry chow. On the sixth day, after the cat had ample opportunity to eat its fill, 1 removed the food and introduced the first mouse. 1 recorded data on cat and mouse behaviour on a checklist. If no kill occurred within 30 min, I removed the mouse and terminated observations for that day. The cat remained housed in in the test arena for the entire 15 days of testing, to maximize familiarity with the test situation. If a kill did occur, the cat was allowed 15 min to eat the carcass, after which time a second mouse was introduced. I repeated this procedure until a mouse had not been killed for 30 min. I offered mice as prey for the first 10 days, young chicks for the last 5 days. This change was an attempt to counteract any habituation to mice as prey. Although no waning in interest was seen over the IO-day period, with respect to mouse killing, the only two cats who killed

BIBEN:

PREDATORY

chicks did indeed show an increase in killing when the prey switch was made. Results Rehaviour Categories The following inventory of behaviour patterns is an exclusive and exhaustive listing of all behaviour patterns seen in the test situation. Each behavioural category comprised several motor patterns whose concurrence resulted in a characteristic behaviour. Each behaviour category, then, can be described by its component motor patterns, which encompass all parts of the cat’s body. Adapting a scheme used by Hutt & Hutt (1970) for describing motor patterns of small children, I identified each behaviour category in terms of its component visual fixations, postures, locomotion, manipulations and vocalizations. For the sake of brevity, only the definitive motor patterns, those which are diagnostic of the behaviour category, are listed in the following inventory: Killbite: the cat normally injures the prey with a single bite or a series of bites. Toss: the cat flings the prey some distance away, without injuring it. Carry: the cat grips the prey firmly in its mouth, but does not maul or chew it. Mouth: the cat’s muzzle makes contact with, or comes very close to, the body of the prey. Recline: though awake, the cat lies on its side in a relaxed posture. Clutch: the cat grabs the prey with its forepaws, pulling the prey in towards its belly. Then it holds the prey in its forepaws while it kicks rapidly at the prey with its hindfeet. Bat: the cat uses one or both forepaws to deliver a blow strong enough to dislodge the prey or make it cry out. Tap: the cat taps gently at the prey, with its claws retracted. Sometimes the cat arrests the movement of its paw in midair or just short of the prey. Herd: if the prey is still, the cat runs toward, but does not overtake, the prey, which usually causes the prey to run away. If the prey is already moving, the cat runs after it, apparently pacing itself so that it never overtakes the prey, If the prey has stopped running, or if running at the prey does not result in its retreat, the cat taps it gingerly with a raised forepaw. The cat does not, or only just, makes contact with the prey. Spring: the cat’s body is close to the ground, head stretched forward and tail stretched backward. Its foreand hind-legs are slightly flexed. In a quick forward thrust of the body, the cat reaches the prey. Crouch: the cat’s body is flat against the ground, forelegs flexed, with elbows elevated

BEHAVIOUR

IN

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83

over shoulder blades, and forepaws directly underneath. Its tail may twitch gently at the tip. Rear: the cat rises on its hindlegs, extends its forelegs and thrusts its body up, forward, and down. Its hindlegs do not reach as great a height as the rest of its body. Often the cat performs this behaviour next to a wall or in a corner; in these cases, the cat drags its body against the wall as it rises up. Attentive: the cat’s gaze is fixed on the prey and will follow any movements of the prey; no manipulations occur. Cry: the cat makes a typical meow sound, or a louder and more throaty cry, similar to the distress cry of a caged cat. Groom: the cat grooms its fur with its tongue, or scratches with its paw. Other maintenance behaviour: the cat is in the litter pan or at the water bowl. Ignore: the cat is gazing away from the prey. Shuteye: the cat is in a relaxed position and its eyes are closed. Jump: the cat springs upwards against the blind or onto the sleeping shelf. Avoidance: the cat moves back, or walks quickly away from, the approaching prey. Relationship of Hunger to Killing The function of predation is generally considered to be that of food-getting (Lorenz 1966; Denny & Ratner 1970). Several rodent studies have suggested the possibility that killing may be controlled by hunger (O’Boyle 1974; Polsky 1975). Using eating as a measure of hunger, such a system predicts that most kills will be eaten. During the 120 days of observation, a total of 71 kills were made by cats who were foodsatiated immediately prior to the predation test. At the end of each day’s trial, I visually estimated the amount eaten from each carcass. Eighty-four per cent of the kills were wholly or partially consumed, suggesting a strong association between killing and hunger. Although eating was an important consequence of killing, cats often abandoned prey for several minutes after a kill. Some kills were made in the presence of uneaten or only partially-eaten carcasses. Cats often returned to a carcass after several minutes or even an hour to eat more. No attempts to hide or cache the prey were ever seen. Thus, although some kills were eaten quickly and completely, most were eaten only incompletely or after a delay, and can be considered surplus kills made independently of hunger. The case for hunger is at best incomplete. These data suggest that it contributes partially

to the control of killing. but by itself cannot completely explain the incidence of killing. Predictions Based on Prey Activity Before attempting a closer invcstigalioit of the differences between the behaviour patterns performed during killing and non-killing situations, 1 looked at the possibility that these differences might be due to differences in the environmental stimuli impinging upon the cats. The laboratory situation allowed me to control essentially all external factors except prey activity. Motion of the prey often provokes pursuit and, indeed, the structure of the cat’s retina is such that a motionless, cryptic prey might not be detected (Fox 1974). It was often difficult, if not impossible. to determine whether the cat was responding to spontaneous movement of the prey or whether the cat, by approaching or prodding the prey, had itself initiated the activity. In the analysis which follows, I made no attempt to separate these two situations. To get a measure of the association between prey activity and each of the different categories of behaviour recorded for the cat. I looked at contingency tables that showed per cent time spent on a given behaviour plotted against the degree of activity shown by the prey. The large size of the contingency tables precluded the use of ~2 and related measures of association (Hays & Winkler 1971). Instead, I calculated the uncertainty coefficient, a statistic which reflected the proportion by which uncertainty in the dependent variable (cat’s behaviour) was reduced by knowledge of the distribution of the independent variable (prey’s activity). Uncertainty coefficients for all behaviours were generally very low, indicating that prey activity is not a particularly good predictor of the type of behaviour shown by the cat. Cat behaviour patterns in which the prey was unimportant (e.g. groom, shuteye) did tend to be performed more often when the prey was relatively inactive. patterns that actively However. behaviour involve the prey (killbite, carry, crouch) occurred about equally whether the prey was inactive or active. The killing bite itself occurred 20”/ of the time during intervals when the prey showed no activity at all. The low values of the uncertainty coefficients are the basis for my conclusion that changes in the activity of the prey were not sufficient to explain the differences in cat behaviour. Nor were cat behaviour patterns determined by any requirements imposed by the act of capture since cats could (and

occasionally did) capture and kill the prey by simply approaching and biting. Clearly the differences between encounters which end in a kill and those which do not must be due to factors other t ban prey activity. Chmges in the Frequencies of Behaviour Patterns Before a Kill Table I lists the percentage of trial time spent on each behaviour category. These data represent over 4000 min of observation. Cats are divided into two groups in Table I, depending on whether or not they killed during the course of the experiments. ‘Killers’ were cats who killed at least once during the 15 days of experimenting. ‘Non-killers’ were cats who, although they killed in their home cages, failed to kill at all during observations. All killers varied in the number of prey they killed from day to day, ranging from zero to seven per trial. All killers were housepets, while three non-killers were laboratoryraised and the fourth non-killer was a young cat with no known hunting experience. In comparing the percentage of time spent in different activities, it is necessary to keep in mind that some behaviour patterns (like toss) are by nature brief, having definite beginningand ending-points with a few swift motor patterns between. Others, like recline, can be prolonged indefinitely. Every cat spent the greatest proportion of its time in the more inactive behaviour patterns, attentive and ignore. In some categories, large individual differences are seen; to determine whether the distribution of percentages in each behaviour category was significantly different for killers and non-killers generally, I used the Mann-Whitney L’ test (Siegel 1956). The category killbite was, of course, seen only in killers. by definition of that group. The behaviour categories carry, mouth, and toss were all performed significantly more often by killers than non-killers. Although killers and non-killers differ in the types of active bahaviour they show, such a comparison does not provide direct information on whether these differences are actually associated with the act of killing. Accordingly, I examined behaviour occurring during trials ending in a kill, as opposed to behaviour occurring during trials where no kill was made. Comparison of the percentage time spent on each behaviour showed that there were no significant differences between killers and nonkillers, during trials where no kill was made.

BIBEN:

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BEHAVtOUR

IN

CATS

$5

Table I. Percentage of Time Spent in All Behaviour Categories: Killers Compared with Non-killers, Samples

Killers Behaviour category Killbite* Toss* Carry * Mouth” Clutch Bat Tap Herd Spring Crouch Rear Attentive Recline Cry Groom Maiaten. Ignore Shuteye Jump Avoidance *Killers

I

2

0.6 0.5 0.1 0.5 0.0 4.6 5.1 0.5 0.0

0.8 0.1 0.6 5.4 0.1 13.2 0.0 0.3 0.1 0.0 0.0 43.2 I I .4 2.2 5.0 0.3 13.7 0.0 0.0 0.0

8:; 70.9

0.0 0.2 0.X 0.9 II.4 3.6 0.0 0.0 significantly

greater

than

non-killers

Using S-min Interval

Non-Killers 3 I.1 0.6 0.5 I.1 0.1 5.4 2.1 0.0 0.0 0.3 0.3 46.6 I .7 2.1 0.8 I .3 19.3 0.0 0.7 9.2

(P < 0.05,

I

2

0.2 0.2

0.0 0.0

0.0 0.0

1.8 1.2 0.0 13.2 0.0 0.9

0.0 0.4 0.0 2.5 6.0 I ,o 0.0 0.0 0.0 53.1 0.0 13.5 0.7 0.7 15.0 I ,o 0.1 5.9

04 ;:;

0.2 0.3 0.3 3s.n 30.6 2.1 0.3 1.2

15.2 0.0 0.1 0.0 Mann-Whitney

The differences in behaviour seen in Table 1 are due to differences between non-kill and killterminated trials. particularly the final 2 min before a kill. Looking at kill-terminated sequences more closely, I found that bat, mouth, carry, toss, and tap all increased in frequency in the minutes preceding the kill. Other behaviours declined in frequency or showed no change. The increased frequency of certain behaviour patterns before a kill could be easily explained if they were instrumental in hunting or in capture of the prey. On the contrary, bat, mouth, toss, and carry represent missed opportunities to kill: the prey is touched or taken into the mouth, but not bitten. Since these behaviour patterns are not related in any obvious functional manner to the delivery of the killing bite itself, I decided to look at the relationships among the behaviour patterns themselves. Such an analysis might yield clues as to why these behaviour patterns change in frequency before a kill and how they might relate to the control of killing. Temporal Associations of Behaviour Patterns A useful method for determining causation is to find out whether behaviour patterns occur together non-randomly. If so, these behaviour patterns may be controlled by a common factor.

4

4.0 1.5 6.0 0.0 i:S 71.6 0.1 I.1 0.8 0.8 I I.9 0.0 0.2 0.0

3

0.0 0.1 0.0 0.1 0.0 5.4 0.3 0.3 0.0 0.8 0.8 50.7 2.6 I.5 0.6 5.1 ‘7.5 0.0 0.0 4.2

-4

0.0 0.0 0.3 0.8 0.2 x.3 32.2 3.0 04 I4 I4 37.5 0.9 12.6 0.4 0.2 I 4) 04 04 0.0

U test)

To investigate this possibility, 1 divided the data from each day’s trial into .5-min intervals of 20 recordings each. The association between each pair of behaviours (dyad) occurring within a 5-min interval was determined by the use of y,‘. More rigorous measures of association (other than those based on ~2) were not applicable to these data primarily because of the large differences in the frequencies of the behaviour patterns (frequency = number of times a behaviour occurred during a .5-min interval). with many behaviour patterns being quite rare (Slater 1973). Figure 1 shows the direction of relationship and degree of significance of association for all dyads. Behaviour patterns are ranked on Ihe axes in approximate order of effect on. or interest shown to, the prey. Thus, going from left to right (or top to bottom) the prey is killed. buffeted about, watched closely, ignored. and avoided. In Fig. 1, behaviour patterns fall into three fairly discrete groups. Behaviour patterns within a group are related in a positive way to each other, and unrelated or negatively related to behaviour patterns outside the group. The characteristics of the three groups can he summarized as follows : Group I: including killbite, toss, carry, mouth, recline, clutch and bat. All of these behaviour

86

ANIMAL

BEHAVIOUR,

patterns (except recline) are active and involve actual contact with the prey. Group II: including bat, tap, herd, spring, crouch, rear and attentive. All of these behaviour patterns (except attentive) are active and (with the exception of bat) involve limited or no actual contact with the prey. Group III: including cry, groom, other maintenance behaviour, ignore, shuteye, jump and avoidance. These behaviour patterns are relatively inactive and either do not involve. or are attempts to avoid, the prey. Tn the minutes before a kill, group I behaviour patterns increase, while many group II and III behaviour patterns decrease. During non-kill sequences, killers and non-killers did not differ in the behaviour patterns they showed (Table I). Groups I and II provided an important clue for why prey are killed in one situation and not in another, Both groups involved active behaviour focussed on the prey; the major difference was that cats made contact with prey in one case but stopped short of making definite contact in the second case. Two possibilities, working separately or together, which might account for a failure to make contact are (1) lack of experience with prey (not knowing how to seize or kill) or (2) fear of the prey. Lack of experience was not a strong possibility, since. three of the four nonkillers were known to be experienced killers in

Fig. 1. The direction of relationship and degree 01 significance for all non-self dyads show that behaviour patterns fall into three fairly discrete groupings.

27,

1

other contexts. One non-killer was a young cat. and inexperience might well have been a factor in its case. Fear of the prey seemed a more likely reason for failure to make contact with prey animals. The three laboratory-raised nonkillers all showed a high degree of fear in the experimental situation and they might have felt more threatened by prey than usual. In addition to the characteristics noted above. behaviour patterns in groups I and II (with the exception of killbite) show many properties commonly referred to as playful. Because the term play has no generally accepted definition, I used an operational definition for categorizing playful responses to prey. By play, I am referring to behaviour that is active, where the cat’s attention is focussed on the prey, or where the prey is touched, manipulated or approached. but not injured. These behaviour patterns can be considered unnecessary for predation since the prey could easily be killed with minimal preliminaries in this laboratory situation. Instead. cats approached the prey, touched it, and picked Etup in the mouth, but failed to bite. Such bouts of play were often repeated several times before the cat finally killed. However, killing was only rarely an ‘accident’ of vigorous play. In the great majority of cases, the killing bite was distinct from the preceding play activities. Although playful behaviour is not directly involved in killing, the data give evidence of a positive relationship between the two. In the experiments which follow, this relationship, as well as other results of experiment 1 (relationship between hunger and killing, inhibiting effect of fear) are investigated in greater detail. Experiment 2 Methods The design of the laboratory and data-gathering procedures was the same as in experiment 1. 1 recorded cat behaviour patterns on a checklist at 10-s intervals. The activity level of the prey (‘active’ or ‘quiet’) was recorded at 30-s intervals. Eighteen cats were used, including nine housepets obtained directly from private individuals. Two of these nine were cats used in experiment 1 who, because they were still available, were used again. Both were killers. At the time of the study, all housepets had been kept in the laboratory for periods ranging from 1 week to 3.5 years. One cat was a laboratory-raised individual, housed communally for several years. The eight remaining cats were obtained from a local

EIBEN:

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BEHAVIOUR

animal shelter at least one week prior to use in the study. All cats used were mature. Two variables were manipulated: hunger and fear. Hunger was measured by food deprivation. Cats were tested after 48 h of starvation, 24 h of starvation, and after satiation on canned food (in this last case, food was left in during the test). I chose prey size as a convenient measure of fear. Because I was interested primarily in the fear-inducing qualities of the prey, I attempted to control for other preyrelated stimuli. I used laboratory mouse pups, adult mice, and young laboratory rats (SpragueDawley) because, except for size, they are very similar in appearance. Differences between mouse and rat odours were minimized by placing rats in dirty mouse cages prior to experiments. Mouse pups (2 to 3 weeks old) are defenceless and easily killed, and should evoke a minimal degree of fear. Young rats (50 to 150 g), capable of self-defence and relatively difficult for a cat to kill, often require over a minute of constant or repeated biting. Rats are also able to inflict

IN CATS

87

serious wounds on the fact: and limbs of a cal while being attacked. I judged adult mice (25-35g) to be somewhere in the middle in terms of difficulty and fearsomeness. Adult mice are almost always killed by cats with a single bite lasting only a few seconds. Laboratory mice showed little self-defence even when attacked. but will usually retreat from an attacker. Cats were housed in the same room where they were tested, or, if removed temporarily before an experiment. were given several hours to reacquaint themselves with the room. Eighteen cats were given one trial with each of the nine combinations of food deprivation and prey size. I used four experimental schedules (Table II) to minimize order effects. I assigned schedules at random. Results Effect of Food Deprivation and Prey Size on King

The distribution of kills (Table III) was significant, as measured by the Cochran Q test.

Table II. Schedule of Experiments

Day

Hunger levels

Decreasing

Decreasing

Increasing

Increasing

Prey size levels

Increasing

Decreasing

Decreasing

Increasing

Hunger

tr: 12 13 14 I.5 I6 17 I? 20 ?I 22 13 24

Hunger

Prey size

Hunger

Prey size

Hunger

Prey size

F F

3 3 : 6 I x 9

Prey size

& NF $4)

K

y

II

NF NF (48)

NF NF (48)

END

Ii

&

r”T) N\ NF (48) NF cp

NE’ (24, NF NF

(24) NF NF

K R”

END

NF N 1’ (48) I NI)

AI)

Food deprivation (hunger) : F .-= fed to satiation prior to experiment : NF not fed; (24) 24.00 h since last meal: (48) = 48 h since last meal. Prey size: B - baby mouse (mean wt -: 7.98 g, SD 2.85); A adult mouse (mean wt. 30,6lg, SD 3.47); K you11g rat (mean wt. := 87.59 g, SD = 37.84).

88

ANIMAL

BEHAVIOUR,

The Cochran Q (Siegel 1956) is uniquely useful for analysing dichotomous data taken from more than two related groups. Scores for a single cat taken under different treatment conditions are related data. The effects of food deprivation and prey size may be considered separately. Because I was interested in the order of these effects, the most powerful and appropriate statistical test was Page’s L (Page 1963), where the order of effects is predicted and tested. The order predicted for food deprivation was that, as food deprivation increased, the incidence of killing increased. This order was significant (P < 0.001, using 18 replications and three treatment levels) (Table IV). Thus, food deprivation, or hunger, increases the probability of killing, while satiation decreases killing. In addition, killing latency was negatively correlated with subsequent carcass consumption (u = -0.7064). This is a further confirmation of the cat’s reduced likelihood of killing when not hungry: cats not only kill fewer prey when not hungry, they also take longer to do it. The order predicted for prey size was that, as prey size increased, the incidence of killing decreased. This order was also significant (P < 0.05) using 18 replications and three treatment levels) (Table V). Thus, small prey increase the probability of killing

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I

while large prey decrease it. In these experiments, all prey were easily accessible and cats were able to seize and bite the prey almost immediately. Under the usual field conditions, the prey would undoubtedly escape if it was not quickly killed. If only those kills in which the killing bite is initiated during the first 1.5 min of the trial are counted, the order trends noted above become even more pronounced. To distinguish between the effects of several days of starvation, as compared to several days since making a kill, I correlated killing with both of these factors. The following are the relevant correlation coefficients (Pearson product-moment) : Correlation of killing and hunger (hours since last meal) : Correlation last kill) : rkilling

of killing and time (hours since time

=~

0.4770

6.86, cJ/’

(t

160, P :.< 0.001) Correlation of hunger and time : I'hunger . time -z 0.2288 P < 0.005)

(f z 2.97.

df

160,

While killing and hunger are correlated positively, killing and time are negatively correlated.

Table III. Incidence of Killing Under the Nine Experimental Treatments (1 = Killed, 0 = Not Killed; Significance of Differences Amongst Treatments: P < 0.001, Cocbran’s Q = 356)

Cat

Experimental schedule*

Column totals

Hunger Prey Size

(48)

(24)

F

(48)

(24)

F

(48)

(241

F

B

B

B

4

A

A

R

R

R

16

IO

10

15

14

II

IO

10

tl

*I = Decreasing hunger, increasing prey size; II =-- Decreasing hunger. decreasing prey size: III decreasing prey size: IV ~:: increasing hunger, increasing prey size.

ROM totals

Increasing hunger

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89

This reflects the fact that time (since last kill) could not be less than the time since the last meal (the measure of hunger)but could be, and often was, much greater if the cat did not kill for several trials or if it did not kill at all. Partial correlation coefficients (Hays & Winkler 1971), showing the degree of relationship between two variables when the effects of a third are removed, were derived to determine if controlling for the differences in time would change the relationship between killing and hunger: ~killinc! = 0’4050 . hunger . time . time . hunger = - 0.5618 ~killin$ hunger . time . killing = 0.4006 Killing and hunger remain positively correlated when controlling for time. The negative correlation between killing and time becomes even larger, indicating that when hunger is controlled, the likelihood of killing decreases very definitely with time since the last kill. The negative relationship between killing and time points out an important characteristic of the predatory behaviour observed in this study: the large degree of individual variation seen in cats. My subjects ranged from total non-killers to cats who killed at almost every opportunity, with most cats falling somewhere between these extremes. Thus the negative correlation between killing and time: cats who had killed recently were probably ‘good’ killers and likely to kill

again, while a cat who had not killed for several days was probably a cat who seldom killed. Experiential differences, particularly those provided by the mother, are thought to be the basis for inter-individual variability in the tendency to show killing behaviour (Kuo 1931; Leyhausen 1965; Fox 1974). However, at least one of my subjects who rarely killed had been provided with prey by its mother, and even stray or feral cats were sometimes poor killers. M. West (personal communication) observed feral mothers with litters, surviving entirely on gleanings from garbage cans. Pooling the data for all cats, as was done here, points up trends that transcend individual variation. This does not mean that this variation should be ignored when predicting the behaviour of any individual. Knowing the cat’s past hunting history, as well as its hunger state and the type of prey involved. affords a greater degree of accuracy.

Table IV. Incidence of Killing at Different Levels of Hunger (All Prey Sizes Combined)

Table V. Incidence of Killing at Different Levels of Prey Size (All Levels of Hunger are Combined)

Predicting the Outcome of Predatory Encounters

A convenient model for predicting the probability of killing, as suggested by these data. would use information about cats’ state of hunger and the size or fearsomeness of the prey involved. 1 performed a multiple regression analysis to determine how much of the variance in the killing response could be explained by the variance in the two factors, food deprivation and

Hunger Cat

F

(24)

2

3

i

32

3

0

2

Prey size Row totals

Cat

3

x

2

I

1 2

3

6

1

3

3 2 3

i

3

9

3

8

2 3

2

3

2 0 0

i: 0

ii

6 I

I;:

i 0 3

(48)

3 3

16 7

ii

Column totals

i

27

2 3

30

3 2

9 x 5

3 3 2 3

8 s 0 7

41

11 1 1.i 14 IS 16 17 1x

Column totals

B

3 3 2

A 3 3

1 I

R 3

-

t%< __-. 8

5

2 0

;i

:

3 2

: 8

t!l 0 3

I: 0 0

; 0 fi

3 3 3

I 3 3

7 0 s .y x s 0 7

3 3 2 -3 1

1 3 3 3 2

0 2 -3 0 :

42

30

176

ANIMAL

90

BEHAVIOUR,

27.

I

Table VI. Multiple Regression Statistics for Hunger (Hours of Food Deprivation), Prey Size (Mean Wt. of Prey), and Killing (Percentage of Prey Killed) l.2 -= 0.9548

P

0.001

Regression coefficients B values !ntercept Mean wt. of prey log1 ohrs of food deprivation bin 1 (“/d of prey killed 57.715

0.229

57.715 -0.229 8.603

(mean ML. of prey)

prey size. Table VI gives the results of this analysis. Since a regression analysis is only useful for linear relationships, I employed two transformations to improve the fit. Killing and food deprivation appeared to be related logarithmically (e.g. cats appeared to be only slightly more likely to kill after 2 days without food than after a single day). The killing response itself, since it was expressed as a proportion, was subjected to an arc sin square root transformation to make the sigmoid distribution of variances more linear. With these transformations, the resulting model for predicting the probability of a kill from just the two parameters, prey size and food deprivation, was sufficient to explain 9504 of the variability in the killing response. The standardized B values, which indicate the relative contributions of the two parameters, are useful in comparing variables measured in different units (size in grams and food deprivation in hours). Thus, information on food deprivation and information on prel size make approximately equal contributions to predicting the outcome of a predatory encounter. and information on both together affords the best prediction. Incidence of Playful Responses Another question I wished to answer concerned the occurrence of playful responses to prey: under what conditions do cats play with their prey? I determined the percentage of time spent in playful behaviour (as defined in experiment 1) for each cat, at each treatment level. I applied the Friedman two-way analysis ot variance for related samples (Siegel 1956) to the ranked scores. The percentage of time spent playing differed significantly (P .< 0.01) amongst treatment levels. I used another non-parametric test, the Kendall coefficient of concordance

Sig. level P -.I om1 P .- OaOl P ." 0401

“B’t,::z 0.0 0.727 0.653

X~603(log~,~ hrq of food depr.)

(Siegel 1956), to determine whether cats tended to be consistent in the conditions under which they showed the most: and least play. Cats were significantly consistent ( P -C O*OOl) and the order of treatment levels is shown in Table VII. The three treatment levels during which cats engaged in the least amount of play were those where the cat was hungry or very hungry and the prey was a baby or adult mouse. In these cases, prey were killed quickly and eaten, with very little time spent on play either before or after the kill. On the other hand, cats showed the most play when not hungry and offered mice, or when very hungry and offered rats. These are conflict or thwarting situations since, in the first, the relatively small prey increases the probability of killing, but the low hunger level decreases the probability. In the second, high hunger level increases, while large prey size decreases. the probability of killing. Discussion Any attempt to understand the control of predatory behaviour must first consider the broad range of responses that predators show when encountering prey. In addition to killing, mammalian predators occasionally perform fragmented or low-intensity sequences, some of which may be characterized as playful. Any theory of predation must account for the appearance of playful responses to prey by answering the following questions: ( 1) Is the appearance of playful behaviour independent of the appearance of seriouc predatory behaviour’? (2) If playful and serious predatory responses art: not independent, what conditions determine the appearance of one rather than the other’? The first step in this process is to determine criteria for distinguishing

playful

behaviour

from

serious

BIBEN:

PREDATORY

predatory behaviour. Leyhausen’s (1956, 1973) studies of prey capture in the domestic cat provide an excellent starting point. These observations were carried out in sparsely-planted outdoor cages, in laboratories, and in home environments. A wide variety of prey types was used, including mice, rats, fowl and rabbits. When presented with familiar prey, cats would typically crouch, approach the prey stealthily, moving close to the ground, and make the final leap when within easy reach of the prey. The method of seizing and biting the prey depended to a great extent on the size, shape, and defences of the prey. The length of time spent in the approach to the prey varied according to the distance and the suitability of cover. Cats ran in short bursts, in a crouched position, from one vantage point to another. As it neared the prey, the cat sometimes paused in a crouched posture. Often the cat prolonged this procedure even when within striking range. The killing bite, directed at the nape of the neck, appears to be similar for all felids, both large and small (Ewer 1973). If the prey is too large or too difficult to bite quickly in this manner, the cat often throws itself on its side while repeatedly biting and raking the prey with the claws of the hind feet. This was the way in which rats were killed in the present study. Small prey were killed with nape bites. Once killed, the prey was often dragged to a favourite eating spot. Cats usually did not begin at once to eat their kills; instead, they left the carcass (even, sometimes, a still thrashing but moribund victim) and took a short walk around the area before beginning to eat. Occasionally, domestic cats or captive small felids will dispense with the preliminaries of stalking and ambush, especially under opportune Table VII. Experimental Treatments Ranked in Order of Time Spent in Play during Each Treatment Hunger 03 CF) (48) (48) 03 (24)

(24) (48)

(24)

Prey B A R A R K A B I\

Time spent in play Most 1

Least

BEHAVIOUR

IN CATS

‘)I

conditions. The prey is merely spotted, approached quickly, seized and killed. Prey capture which involves the minimum of movements, energy and time in achieving a goal of food-getting can be considered efficient. Leyhausen referred to such sequences as ‘Ernstgemeinten’, or ‘earnestly meant’. In contrast to these efficient predatory sequences were pre-kill sequences where cats jumped about, tossed prey into the air, or poked at the prey and ran away. Leyhausen gave many examples of domestic cats and other small felids seemingly throwing away opportunities to make a kill; they chased prey but stopped short of overtaking it, or grasped a rat in their mouths but failed to deliver the killing bite. Similar ‘crazy capering’ was described by Leyhausen as a post-kill release of tension after a difficult struggle. In these cases, cats leaped over the carcass, threw it into the air, and dashed madly about with it in their mouths. All of these behaviours patterns were seen both in killterminated and non-kill-terminated encounters. Leyhausen referred to such reactions to prey as ‘playful’ and differentiated playful reactions from serious ones on several points: (1) The components of prey capture appeared in random sequence in play. Behaviour patterns, or parts of behaviour patterns, appeared out of order and functional context. Individual behaviour patterns and sequences were aborted before completion. (2) Components of behaviour patterns were performed with greater intensity than normal. In serious prey capture, excessive movement was minimized since the cat depended on stealth for a successful ambush. (3) Full-intensity killing bites were not seen in play. Cats rarely bit prey to death while playing; rather, there was a definite changeover from playful to serious behaviour before the killing bite. Leyhausen identified three types of play with prey, all of which intergraded with each other and appeared as recognizable categories only under certain conditions: (1) Inhibited play (Gehemmtesspiel): low-intensity performance of prey capture behaviour when predatory responses have been ‘exhausted’. (2) Overflo\+, play (Stauungsspiel): batting the prey across the floor, carrying it in the mouth, and tossing it. The killing bite is actively inhibited and the prey unharmed although the behaviour patterns are true prey capture movements with the proportions exaggerated due to an excess 01’ energy built up because the cat has not killed recently. (3) Relief play (Erleichterungsspiel)

92

ANIMAL

BEHAVIOUK,

leaping over and around the prey performed mainly after a difficult kill, when built-up tension or energy is released. Although play behaviour patterns described by Leyhausen were ones that I observed often in my own cats, my experimental results did not support his assumptions of causality. The behaviour patterns of inhibited play correspond roughly to the behaviours of group II, as described here in experiment I. These behaviours did occur under conditions of inhibition. though this inhibition arose from a conflict between factors (hunger and prey size) that simultaneously tended to increase and decrease the probability of killing, and not from the exhaustion of more serious predatory behaviour patterns. When these factors are controlled for, cats who have killed recently are not more likely to show group II behaviour patterns than are cats who have not killed in weeks. Overflow play behaviour corresponds to those described here as group I behaviour patterns. As with group I1 behaviour patterns, group I behaviour patterns were independent of the recency of killing. I saw no reason to distinguish between play that occurred before a kill and that which occurred after, as Leyhausen had done. In addition to post-kill leaping about, I observed post-kill batting, tossing, mouthing and carrying. Pre- and post-kill play occurred under similar. conflict, conditions in my experiments. Many of the prey’s stimulus properties might still be operative after it is dead, and lack of hunger might contribute to conflict by inhibiting eating. The non-social play of adults (i.e. solitary play or play with objects), as well as that of young, has long been a disturbing concept in theories of behaviour, primarily because of a failure to discover any significant biological function for its performance. Play is often considered to be the only major category of behaviour which has no purpose, one that is performed only when nothing ‘important’ is happening or when no behaviour patterns having an obvious biological purpose have been activated (Bierens de Haan 1952; MeyerHolzapfel 1956). In cases where a purpose has been found, there has beena tendency to reclassify the behaviour as an immature, neurotic redirected substitute, or low-intensity form of anothct behaviour (Kruijt 1964). There is reason to believr that much of the play of adults should be considered separately from that of juveniles. Juvenile play often appears to be a developmental. rather than a

17.

I

motivational, phenomenon. The possibility that juvenile play is a step in the development of mature adult behaviour is a promising line of research. The inefficient behaviour of young animals is often called play when actually the animal may be performing at the maximum efficiency for its level of development (Loizos 1966). The similarity of motor patterns in the play of juveniles and that of adults does not necessarily imply a similar causation for the two. The important question here is not from where the motor patterns are derived (because. indeed, the motor patterns of all types of animal play are probably taken from other contexts (Poole 1966; Hinde 1970) but. rather, what controls the playful expression of predatory behavioui patterns in the adult? All attempts to identify a drive specific fog play have been mconclusive (Mtiller-Schwarze 1968; Chepko 1971) although the opportunity to play can be a potent reward in lever-pressing situations (juvenile chimpanzees: Mason 1967). Often play appears to be a substitute or a displacement behaviour. Bekoff (1972) observed solitary play in dogs in situations where social play was thwarted by non-responsive companions. Observations have also been made of social play occurring when predatory behaviour was thwarted. Haber (in Brown 1972) observed a wolf pack held at bay by a moose. The wolves. apparently intimidated by their powerful prey, engaged in play with each other, within a few metres of the moose, and then retreated. In the Base1 Zoo, juvenile elephants were observed leaping about when their older companions were taken away. Inhelder (1955) attributed this behaviour to anxiety and believed that the playful behaviour was a release for frustration. Thorpe (1966) cited instances of similar behaviour (termed ‘superstitious’) occurring in tense situations. These examples support the idea that play can result from situations where activity is thwarted or frustrated. Play appears in such a context in kittens confronted with their first prey (Leyhausen 1965). Play before the first kill has also been observed in the African dwarf mongoose (I-lelogale undulata wfila) ( Rasa 1973). A young individual who had never pre\iously succeeded in killing entered ;I mouse breeding cage and killed soveral mice. Subscquently given ;I single mouse, the individual responded with play and timid approaches. as ii‘ i: had never killed. Rasa attributed the killing spree to the excitement caused by numerous

BlBEN:

PREDATORY

ileeing mice. where a single mouse was insufficient to overcome inhibition. Killing sprees, where prey are killed and left uneaten, have been reported for many predators (Leyhausen 1956; Tinbergen 196.5; Errington 1967; Kruuk 1972). Explanations for excessive killing based on models where a killing drive is independent of hunger, or models which see killing as an automatic response to the sight of prey, have not been supported by my data. Kruuk (1972) argues that food satiation does not inhibit catching and killing and that, where prey are readily available, excessive kills will be made. However, 1 found that in the present study, where all prey were at hand and unable to escape, catching and killing were inhibited by satiation. The association between killing and hunger is in agreement with neurological data linking killing and eating centres in the lateral hypothalamus (Hutchinson & Renfrew 1966). In most reported cases of excessive killing (killing without eating), the prey were confined, as in a henhouse, or otherwise unable to escape. A likely explanation is that the predator became so excited by numerous or panicky prey that excessive killing occurred. In the same way, excitement generated by play in conflict situations may be important in determining whether a kill will occur. I have shown that cats have a longer killing latency as well as a reduced incidence of killing, in conflict situations and that this extra time is typically spent in play. Wilz (1970) has described a displacement activity of three-spined sticklebacks (Gasterosteus aculeatus) that is instrumental in resolving the conflict situations where it occurs. Play with prey might serve a similar purpose, either by exciting the cat enough to kill or, in the case of dangerous prey, frightening it enough to retreat. Energy models of predation predict that play with prey will occur when energy for eating, killing and serious pursuit have been exhausted, or in response to an independent drive for play (Leyhausen 1965). Neither of these hypotheses is supported by my data. Instead of exhibiting predatory behaviour patterns in the hierarchical manner predicted by an energy model, cats given no more than one opportunity to kill daily (a relatively deprived killing schedule) showed long periods of play before they killed if the prey was large or dangerous. There was no evidence for an independent killing tendency building up over time; rather, killing was under the control of hunger and stimuli from the prey.

BEHAVIOUR

IN.-CATS.

93

In addition, there was no evidence for a play drive building up as a function of time. Cats deprived of prey (and thus of the chance to play with prey) the longest were the least likely to show play because they were sufficiently hungry to quickly kill all but the largest prey. Explanations which predict that killing will occur as a function of hunger alone are insufficient to explain the occurrence of either predatory or play behaviour patterns in these experiments. My cats continued to kill when satiated if the prey was easy and especially if given the opportunity to play first. Thus, satiated cats continued to respond to stimuli (such as small size and vulnerability) from the prey. Play occurred at both high and low levels of hunger, rather than just at low levels as predicted by hunger-regulated models. Acknowledgments 1 wish to thank Dr Helmut C. Mueller for his guidance and encouragement throughout this study. This article is based on a dissertation submitted to the Department of Zoology, University of North Carolina, in partial fulfillment of the requirements for the Ph.D. degree. Funding was provided in part by a training grant from the Neurobiology Program of the University of North Carolina. REFERENCES Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviorrv, 49, 227-267. Bekoff, M. 1972. The development of social interaction, play and metacommunication in mammals; an ethological perspective. Qunrt. Rev. Bin/., 47, 412-434. Bierens de Haan, J. A. 1952. The play of a young solitary chimpanzee. Behoviour, 4, 144-l 56. Brown. D. 1972. Wild Aluskn. New York: Time-Life ‘Books. Chepko, B. D. 1971. A preliminary study of the effects of play deprivation on young goats. 2. Tierpsychol., 28. 5 17-526. Dennv. M. R. & Ratner. S. CL‘. 1970. Comuaratire s ‘Psychology. Homewood, Illinois: Dorsey: Errington, P. 1967. Oj’Predution nnd Life. Ames: Iowa State University Press. Ewer. R. F. 1973. The Carnivores. Ithaca: Cornell Universitv Press. Fox, M. W. 1974. Understanding Your Co/. New York: Coward, McCann Br Geoghegan. Hays, W. L. & Winkler, R. L. 1971. Statistics: Probability, Inf&-ence. and Decision. New York : Holt. Rinehart &’ Winston. Hinde, R. A. 1970. Anitnnl Behaviour. New York: McGraw-Hill. Hutchinson, R. R. & Renfrew, J. W. 1966. Stalking attack and eating behaviors elicited from the same site in the hypothalamus. J. ro/?tp. physiof. P.qxhol., 79, 237-242.

ANIMAL

94

BEHAVIOUK.

Hun, C‘. & Hun, S. J. 1970. Direct Ob.r~rrariorr ~rnr/ .bleasuren,ent of Behorior. Springfield, Illinois : Charles C. Thomas. Inhelder, E. 1955. Uber das Spielen mit Gegenstanden bei Huftieren. Rev. Suisse de 2001.. 62. 240-250. Kruijt, J. P. 1964. Ontogeny of social behaviour in Burmese Red Jungle fowl (G&s &/rr.r spadiceus ). Behaviour, Supplement XII. Kruuk, H. 1972. Surplus killing by carnivores. J. Zoo/. Lond.,

166,

233-244.

Kuo, Z. Y. 1931. The genesis of the cat’s response IO the rat. J. romp. Psycho/., II, l-35. Leyhausen, P. 1956. Verhaltensstudien an Katzen. %. Tierpsychol., Beiheft 2, l-120. Leyhausen, P. 1965. On the function of the relative hierarchy of moods (as exemplified by the phylogenetic and ontogenetic development of preycatching in carnivores). In: Motivation of HUWKUJ and Animal Behaviour: an Ethological View (Ed. by K. Lorenz & P. Leyhausen), 1973. Translated by B. A. Tonkin. New York: Van Nostrand Reinhold. Leyhauscn, P. 1973. Verhaltensstudien an Katzcn. 3. %. Tirrpsychol., Beiheft 2, completely revised edition. l-232.

Loizos, C. 1966. Play in mammals. Symp. zool. Sac. Lo&., 18, l-9. Lorenz? K. 1950. The comparative method in studying innate patterns. Symp. Sot. exp. Biol,, 4, 221-268. Lorenz, K. 1966. On Aggression. Trans. by Majorie Kerr Wilson. New York: Harcourt, Brace & World. Mason, W. A. 1967. Motivational aspects of social responsiveness in young chimpanzees. In : Eari? Behavior (Ed. by H. W. Stevenson, E. H. Hess Pr H. L. Reingold), pp. 103-126. New York: Wiley. Meyer-Holzapfel, M. 1956. Uber die Bereitschaft zu Spiel- und Instinkthandlungen. 2. Tierpsycho/., 13, 442-462.

27.

I

Mueller, H. ( 1973. The predatory behaviour and Buteo platypterus). Miillcr-Schwarze, D. 1968. Behaviour,

31,

rclattonship ot hunger to in hawks (F&o sparverius Anim.

Behav.,

21, 513-520.

Play deprivation

in deer.

145-162.

O‘Boyle, M. 1374. Rats and mice together: the predatory nature of the mouse-killing response. Psycho/. uJl//., 81, 261-269. Page, E. B. 1963. Ordered hypotheses for multiple treatments: a significance test for linear ranks. J. Am. stat. Assoc., 58, 216-230. Polshy. R. I-1. 1975. Hunger, prey-feeding, and predatory aggression. Behav. Biof., 13, 81-93. Poole, T. B. 1966. Aggressive play in polecats. Syrnp. zool.

Sot.

Lond.,

18,

23-44.

Rasa, 0. A. E. 1973. Prey capture, feeding techniques, and their ontogeny in the African Dwarf MonSiegel,

!;osaglee8gale undulata rujirla. Z. Tierpsychol., . S.’ 1956. Non-pammetric Statistics jtir the Behavioral Sciences. New York: McGraw-Hill.

Slater, P. J. B. 1973. Describing sequences of behavior. In: Perspectives in Ethology (Ed. by P. P. C. Bateson & P. Klopfer), pp. 131-153. New York: Academic Press. .Thorpe, W. H. 1966. Ritualization in ontogeny: 1. Animal Play. Phi/. Trans. Roy. Sot. Lond., B. 451, 311-319. Tinbergen, N. 1965. Von den Vorratskammern des Rotfuchses (Vulpes vulpes L.). Z. Tierpsychol., 22, 119-149. Wilz. K. J. 1970. Causal and functional analysis of dorsal pricking and nest activity in the courtship of the three-spined stickleback (Gasterosteus aculeatus). ,4nin7. Behav., 18, 115-124. (Received 8 December 2nd revision 23 June

1976;

revised

1977; MS. number:

4 April

1977 :

~1965)