play behaviour during early ontogeny in free-ranging dogs (canis familiaris)
TRANSCRIPT
Applied Animal Behaviour Science 126 (2010) 140–153
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Applied Animal Behaviour Science
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Play behaviour during early ontogeny in free-ranging dogs(Canis familiaris)
Sunil Kumar PalKatwa Bharati Bhaban, Katwa, Burdwan 713130, West Bengal, India
a r t i c l e i n f o
Article history:Accepted 21 June 2010
Keywords:Canis familiarisSocial investigationPlay-fightingAggressive playObject playPseudo-sexual play
a b s t r a c t
Twenty-four free-ranging dog puppies belonging to six litters were observed from birth to13 weeks of age to study the play behaviour in early ontogeny. Only a single annual breedingcycle with synchronized breeding season was recorded in this study. Mean litter size was6.67 ranging from 5 to 8 with a male-biased sex ratio of 1.22:1. Social investigation wasfirst observed with 3 weeks of age, and then subsequently developed other play behaviours(play-fighting, play-mounting, aggressive play, objects play and pseudo-sexual play). Thelitters were significantly different from each other in relation to the number of total playbouts (�2 = 475.42, d.f. = 5, P < 0.005). The puppies within the litters as well as among thelitters were significantly different from each other in relation to the frequency of play bouts.There was a positive correlation between the frequency of play bouts and the number ofthe puppies within the litters (r = 9970, P < 0.005). All the play behaviours showing weekly
variations increased with the age of the puppies, but it suddenly decreased in weeks 9or 10, and continued thereafter. Male puppies initiated playful interactions with a greaterfrequency than did female puppies. Except in the case of aggressive play, male puppiesinitiated play more often with female puppies and vice versa showing the evidence ofinter-sexual play in free-ranging dogs. Intra-sexual dominance relationships among thelittermates developed between 5 and 13 weeks of age.1. Introduction
Although there are many important life stages, the keysensitive period in a dog puppy’s development is gener-ally accepted to be the 10-week period from 3 weeks to3 months of age. This 10-week period is the primary sen-sitive period of canine development. This time period isgenerally referred to as the ‘socialization period’ for this iswhen species-typical social skills are learned most rapidly(Bekoff, 2001). Even though some authors consider play
to be functionless behaviour (e.g., Bierens de Haan, 1952),other researchers agree that play facilitates animals tolearn valuable social skills (Biben, 1998) or to strengthen(Bekoff, 1984) or test social bonds (Zahavi, 1977; Pozis-E-mail address: [email protected].
0168-1591/$ – see front matter © 2010 Elsevier B.V. All rights reserved.doi:10.1016/j.applanim.2010.06.005
© 2010 Elsevier B.V. All rights reserved.
Francois et al., 2004), as training for cognitive (Bekoff, 1984;Spinka et al., 2001) or motor development (Byers, 1998),to develop the emotional flexibility needed for dealingwith unexpected situations (Spinka et al., 2001) or as away to assess their own capabilities relative to conspecifics(Thompson, 1998; Smith et al., 1999; Palagi, 2004). Palagi(2007) hypothesizes that play behaviour is an ontogenetictrait in many mammalian species and is widely believed tohave an important role in the assembly of adult behaviour.When animals live together in groups, social rules evolve toreduce conflict and facilitate cooperation. They can share inthe work of defending territories (Pal et al., 1998a) and car-
ing for their young (Pal, 2008). According to Bekoff (1972),Fentress et al. (1987), McLeod and Fentress (1997) playcontributes to the formation of dominance relationshipswithin litters; and a social hierarchy reduces fighting overaccess to important resources that are in short supply, such
S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153 141
Table 1Neighbouring dog groups observed between March 2008 and April 2009.
Dog code Group Sex Age Present in the groups Remark
From To
HM1 HIG Male Adult March 2008 April 2009HM2 HIG Male Adult March 2008 April 2009HM3 HIG Male Juvenile March 2008 April 2009HF1 HIG Female Adult March 2008 April 2009HF2 HIG Female Juvenile March 2008 May 2008 DeathMM1 MIG Male Adult March 2008 April 2009MM2 MIG Male Adult March 2008 April 2009MM3 MIG Male Juvenile March 2008 Jul. 2008 EmigratedMF1 MIG Female Adult March 2008 April 2009MF2 MIG Female Juvenile March 2008 April 2009MF3 MIG Female Adult Dec. 2008 April 2009 ImmigratedLM1 LIG Male Adult March 2008 April 2009LM2 LIG Male Juvenile March 2008 April 2009LF1 LIG Female Adult March 2008 April 2009LF2 LIG Female Juvenile March 2008 April 2009SM1 SM Male Adult March 2008 April 2009SM2 SM Male Adult March 2008 April 2009SM3 SM Male Adult March 2008 Oct. 2008 DeathSM4 SM Male Juvenile March 2008 April 2009SM5 SM Male Juvenile March 2008 April 2008 DeathSF1 SM Female Adult March 2008 April 2009SF2 SM Female Adult March 2008 April 2009SF3 SM Female Adult Dec. 2008 April 2009 ImmigratedSF4 SM Female Juvenile March 2008 April 2009 DeathNM1 NM Male Adult March 2008 April 2009NM2 NM Male Adult March 2008 April 2009NF1 NM Female Adult March 2008 April 2009NF2 NM Female Adult March 2008 April 2009NF3 NM Female Juvenile March 2008 April 2009BM1 BS Male Adult March 2008 April 2009BM2 BS Male Adult March 2008 Oct 2008 EmigratedBM3 BS Male Juvenile March 2008 May 2008 Kept as pet
le
le
afs
b1B1B2cmoVT2co
oagodt
BM4 BS Male JuveniBF1 BS Female AdultBF2 BS Female AdultBF3 BS Female Juveni
s food, resting places, and mates. Therefore, it is importantor individuals to engage in at least some play during theocialization period (Bekoff and Byers, 1981).
A number of studies have been done on the playehaviour of mammals (e.g., Bekoff, 1972, 1974a, 1974b,984, 1995, 2001; Bekoff and Byers, 1981; Baldwin andaldwin, 1977; Fagen, 1981; Pederson et al., 1990; Holmes,994; Drea et al., 1996; Spinka et al., 2001; Packard, 2003;urghardt, 2005; Bauer and Smuts, 2007; Tanner et al.,007; Watts, 2007). However, very few studies have beenonducted on domestic dogs, especially on the develop-ent of social relationships during social play in early
ntogeny (e.g., Rheingold, 1963; Bekoff, 1974a; Lund andestergaard, 1998; Lindsay, 2000; Bauer and Smuts, 2007;óth et al., 2008; Ward et al., 2008, 2009; Ward and Smuts,009; Cafazzo et al., 2010). All previous studies have beenonducted in American and European countries, and onwned populations of dogs.
The purpose of this study was to investigate the devel-pment of different types of play behaviour in relation to
ge, nature of play in relation to sex, and also to investi-ate how adult behaviours are developed from the earlyntogeny in free-ranging dog puppies. Development of aominance hierarchy from aggressive play among the lit-ermates was also investigated.Sept. 2008 April 2009 ImmigratedMarch 2008 April 2009Oct. 2008 April 2009 ImmigratedMarch 2008 Aug. 2008 Death
2. Materials and methods
2.1. Study area
The study was carried out in the town of Katwa (lat23◦30′N, long 88◦05′E) in the state of West Bengal, India.The study area (0.5 km2) with a population of approxi-mately 4200 people was on the outskirts of the town andlinked with other parts of the town by a metalled road. Itwas bounded to the North and North-West by wetland; andto the East, South and South-West by paddy fields. The mainbus stand of the town was situated in the study area. Thearea comprised of 20% low-income, 65% middle-class and15% higher-class neighbourhoods. The study area was char-acterized by an abundance of open land with many privatehouses, five garages, one timber yard, and several cowshedsand poultry farms. Interviews with the area residents con-firmed that about 20% of the low-income residents allowedthe female dogs to use their cowsheds or unused poultryfarms for rearing pups.
Six restaurants and two butcheries were located adja-cent to the bus stand. Garbage was the major food resourcefor the dogs and was scattered throughout the study area.However, the restaurants and butcheries near the bus standwere chief food resources for the studied dogs.
aviour S
142 S.K. Pal / Applied Animal Beh2.2. Subjects
The study was carried out on free-ranging dogs (Canisfamiliaris). Six adult bitches from 6 neighbouring doggroups (Table 1) that roamed freely throughout the day andnight, and whose home range and prior reproductive his-tory were known, were selected for this study. Members ofthe dog groups varied from 4 to 8. Groups of two or moredogs were operationally defined with the requirement thatdogs remain together for at least 1 min without exhibitingagonistic or avoidance behaviours (Daniels, 1983). The doggroups were more or less stable throughout the study andwere observed to defend a common territory.
The animals were identified visually by coat colour andpattern and photographed to permit later identification.The sex of the dogs was determined by observing theanimals and their behaviour especially their urination pos-tures (Bekoff, 1979). The sex of the puppies was determinedby observing the penis in the middle of belly (male), andvulva and vagina located just beneath the anus (female).
The dogs were classified as puppies (birth – 3 months),juveniles (3–12 months), adults (1–7 years), and old adults(>7 years). Age of the puppies was determined by visualmeans. Age of the juveniles, adults, and old adults wasdetermined by direct observations, interviews with thearea residents and sometimes according to the eruptionand wear patterns of their dentition (Kirk, 1977).
2.3. Experimental procedure
The study began in March 2008 and continued untilthe end of April 2009. Data were collected using focalanimal sampling (Altmann, 1974). Previously Pal et al.(1998a) reported that bitches seem to be more aggressiveimmediately after parturition to assure adequate nutritionand to protect puppies. Therefore, throughout the studyperiod, the focal bitches were fed bread to make them tameenough to avoid dog biting during data collection on pup-pies. Throughout the study period, the dog groups wereobserved once a week between 06:00 and 08:00 h. The focalbitches were followed daily between 06:00 and 08:00 hand between 16:00 and 20:00 during their gestation. Dateof parturition was confirmed by direct observations of theanimals and interviews with the area residents. After partu-rition, every focal litter was observed three times (morning,noon and afternoon) daily between 06:00 h and 18:00 h.The duration of each observation session was 30 min with atotal of 90 min observation per litter per day. A total of 819 hwas devoted to collecting data on the play behaviour of thepuppies belonging to six litters. Data collection continuedfor the first 13 weeks of rearing.
Litter sizes were based on the first sighting of thepuppies. Pup survival was estimated from the differencebetween the numbers at the first sighting and the numbersobserved during the following weeks.
The seasons were defined as summer,
March–May; monsoon, June–August; late monsoon,September–November; and winter, December–February.Social interaction can be defined as any sort of play thatdeals directly with the socialization of an individual intothe group. In this study, social interactions were divided
cience 126 (2010) 140–153
into 6 categories: social investigation, play-mounting, play-fighting, aggressive play, object play and pseudo-sexualplay.
2.3.1. Social investigationDuring social investigation a puppy contacts a litter-
mate to lick, orally investigate or sniff its head, body, limbsand/or genitals.
2.3.2. Play-mountingIt involves one puppy approaching another from front
or near side and placing its forepaws on the back of anotherpuppy to assume a posture like that exhibited by adultmales during copulation; but without pelvic thrust.
2.3.3. Play-fightingIt includes biting, pawing, rolling over, wrestling, lung-
ing, arching back, standing over a littermate and pushing.
2.3.4. Aggressive playIt includes stalking and chasing, ambushing and attack-
ing; circling the littermate with a stiff wagging tail, raisedhackles, baring teeth, snarling or biting, direct stare withdilated pupils, erect or flattened ears.
2.3.5. Object playIt includes biting or gnawing on objects from which little
or no energy or nutrients could be derived, including plants,sticks, or old dried pieces of bone. Occasionally, runningwith or tugging on sticks, papers shoes etc.
2.3.6. Pseudo-sexual playPseudo-sexual play known as love play is interactions
which resemble sexual behaviour but do not lead to cop-ulation. Common forms of pseudo-sexual play includemounting, licking, clasping and pelvic thrusting from therear.
Dominance is defined as a relationship between indi-vidual animals that is established by force/aggressionand submission to determine who has priority access tomultiple resources such as food, preferred resting spots,and mates (Bernstein, 1981; Drews, 1993). Dominancebehaviour includes upright and stiff body posture with thehead and tail held high and the ears pricked, and growlingor baring teeth at warning other dog (Cafazzo et al., 2010).All these behaviours were also noticed during aggressiveplay; and so, in this study, dominance was measured onthe basis of number of aggressive encounters initiated bythe pups.
When a puppy solicited play towards another, the firstone was considered as ‘initiator’ and the second as ‘recip-ient’. Sometimes more than two puppies actively joinedthe dyads, and in these cases the third or fourth individualwas recorded as ‘initiator’ as well. Individuals that initi-ated dominant or aggressive play towards a littermate wererecorded as initiators, whereas individuals that reacted
submissively to the initiator’s behaviour were recorded asrecipients.The incidence of interventions among the littermatesduring playful interactions (Ward et al., 2009) was noticedin this study but no data were collected.
S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153 143
Table 2Data showing the mating, parturition, litter size and pup mortality.
Female code Month of mating Month of parturition Litter size Total Puppies survived at theage of 13 weeks
Total
Male Female Male Female
HIGF August 2008 October 2008 4 3 7 2 2 4MIGF September 2008 November 2009 3 2 5 2 1 3LIGF September 2008 December 2009 4 3 7 2 2 4SMF October 2008 December 2009 4 2 6 3 1 4
34
22
cwt
el
upemqwtooo
3
3
A
NMF October 2008 December 2008BSF December 2008 February 2009
Total
Social positions of the puppies within a litter may behanged, but the position of an individual in the social rankas determined on the basis of total play bouts initiated by
he individuals.All observations were videotaped following the dogs
ither on foot or by a bicycle using Sony handycam. Sixocal people assisted to collect data.
For statistical analysis, paired and unpaired t-tests weresed to examine the difference between male and femaleuppies in relation to playful interactions. Chi-square mod-ls were used to calculate the seasonal differences inating and pup rearing and also to differentiate the fre-
uency of play bouts among the puppies within a litter asell as among the litters. A Pearson’s coefficient of correla-
ion was used to calculate the correlation between the agef the puppies and the frequency of play bouts. An analysisf variance (ANOVA) was used to test the weekly variationsf different types of play behaviour.
. Results
.1. Reproduction, sex ratio and litter size
All six focal bitches were observed to copulate betweenugust and December showing late monsoon as the period
Fig. 1. Weekly mean (±S.E.) number of total play bou
5 8 2 3 53 7 2 2 4
18 40 13 11 24
of mating (�2 = 97.36, d.f. = 3, P < 0.005) (Table 2). Birthswere recorded between October and February showingwinter as the peak period of pup rearing (�2 = 123.12,d.f. = 3, P < 0.005). Each female produced a single litter peryear. Therefore, 6 litters were produced involving a totalof 40 puppies with a male-biased sex ratio of 1.22:1. Meanlitter size was 6.67 ranging from 5 to 8 (Table 2). The mor-tality rate in the first 3 months was 40%, leaving 24 puppiesthat survived the first 13 weeks of life.
3.2. Playful interactions in relation to age
Twenty-four puppies belonging to six litters (Table 2)were observed from birth to 13 weeks of age. Data, col-lected on the play behaviour of puppies that died beforethe age of 13 week, were excluded in this study. Only onefemale puppy was present in the litter-MIG as well as inthe litter-SM. As they had no female play partners, no dataon female–female play behaviour were available for thesetwo groups.
Throughout the study, a total of 50,040 intra-litter playbouts (all types of play) were initiated by 6 litters involving24 puppies (Table 3). The mean (±S.E.) number of play-ful interactions initiated by the litters varied from 1312.33(±176.31) to 2696.60 (±484.71) (Table 3), and the litters
ts initiated by 6 litters involving 24 puppies.
144 S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153
Table 3Frequency of play bouts recorded on the basis of thrice per day with 30-min duration in each observation period among 24 puppies (13males and 11females).
Initiators Litter code Sex Recipients
HM1 HM2 HF1 HF2 MM1 MM2 MF1 LM1 LM2 LF1 LF2 SM1
HM1 HIG M – 784 1223 845HM2 HIG M 612 – 698 1120HF1 HIG F 580 342 – 551HF2 HIG F 369 635 479MM1 MIG M – 645 920MM2 MIG M 554 – 845MF1 MIG F 522 451 –LM1 LIG M – 841 1125 741LM2 LIG M 568 – 621 1029LF1 LIG F 540 480 – 444LF2 LIG F 465 664 500 –SM1 SM M –SM2 SM M 754SM3 SM M 684SF1 SM F 587NM1 NM MNM2 NM MNF1 NM FNF2 NM FNF 3 NM FBM1 BS MBM2 BS MBF1 BS FBF2 BS F
Initiators Litter code Sex Recipients
SM2 SM3 SF1 NM1 NM2 NF1 NF2 NF 3 BM1 BM2 BF1 BF2
HM1 HIG MHM2 HIG MHF1 HIG FHF2 HIG FMM1 MIG MMM2 MIG MMF1 MIG FLM1 LIG MLM2 LIG MLF1 LIG FLF2 LIG FSM1 SM M 685 725 1352SM2 SM M – 620 725SM3 SM M 636 – 545SF1 SM F 540 469 –NM1 NM M – 878 1325 1096 812NM2 NM M 765 – 785 1174 897NF1 NM F 709 499 – 425 377NF2 NM F 412 674 409 – 314NF 3 NM F 489 554 401 488 –BM1 BS M – 763 1125 645BM2 BS M 688 – 609 955
BF1 BS FBF2 BS FM = male, F = female.
were significantly different from each other in relationto the number of playful interactions (�2 = 475.42, d.f. = 5,P < 0.005). The frequency of play bouts increased with thenumber of puppies within the litters (r = 9970, P < 0.05).
The mean (±S.E.) number of play bouts initiated by thepuppies (n = 24) varied from 452.25 (±77.34) to 1027.25(±116.19) (Table 3), and the puppies were significantlydifferent from each other in relation to the frequencyof play bouts (�2 = 1131.68, d.f. = 23, P < 0.005). Further-740 488 – 526421 665 417 –
more, the individual puppies within the litters (HIG, MIG,LIG, SM, NM, BS) were significantly different from eachother regarding play bouts (�2 = 700.01, d.f. = 3, P < 0.005,�2 = 142.11, d.f. = 2, P < 0.005, �2 = 485.02, d.f. = 3, P < 0.005,
�2 = 358.55, d.f. = 3, P < 0.005, �2 = 1742.54, d.f. = 4, P < 0.005and �2 = 325.62, d.f. = 3, P < 0.005 respectively, Table 3).The weekly mean (±S.E.) number of play bouts initiatedby 24 puppies varied from 18.58 (±2.09) to 542.38 (±39.81)times (Fig. 1), and the weeks were significantly different
S.K. Pal / Applied Animal Behaviour S
Tab
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n(±
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um
ber
ofd
iffe
ren
tty
pes
ofp
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reco
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wit
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ion
per
iod
amon
g24
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pp
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(13m
ales
and
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es).
Typ
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pla
yA
geof
the
pu
pp
ies
(wee
ks)
3rd
4th
5th
6th
7th
8th
9th
10th
11th
12th
13th
Soci
alin
vest
igat
ion
22.3
3±
1.37
49.3
3±
3.19
79.5
4±
4.24
120.
08±
7.33
153.
25±
8.66
224.
08±
12.9
511
6.71
±9.
6764
.50
±5.
0226
.33
±2.
4812
.46
±1.
425.
63±
1.17
pla
y-fi
ghti
ng
11.6
3±
0.86
19.7
9±
1.93
33.3
3±
3.34
51.2
1±
5.01
76.1
7±
6.51
113.
29±
8.82
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3.45
15.0
4±
1.72
6.38
±0.
653.
42±
0.36
Play
mou
nt
10.3
8±
1.46
18.2
9±
2.68
28.0
0±
3.97
42.1
7±
5.16
63.3
8±
8.32
100.
88±
12.1
231
.38
±4.
4116
.38
±2.
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29±
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47A
ggre
ssiv
ep
lay
8.13
±1.
0016
.25
±2.
5625
.71
±3.
4146
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±4.
9410
5.67
±8.
4924
.46
±2.
0211
.08
±0.
945.
46±
0.42
2.79
±0.
22O
bjec
tp
lay
7.21
±0.
6012
.42
±1.
1021
.50
±1.
3435
.79
±1.
6572
.46
±3.
5517
.29
±0.
839.
08±
0.45
5.04
±0.
242.
25±
0.11
Pseu
do-
sexu
alp
lay
7.29
±0.
9212
.25
±1.
5319
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±2.
2233
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±3.
7412
.00
±1.
287.
54±
0.90
4.25
±0.
571.
50±
0.26
cience 126 (2010) 140–153 145
from each other in relation to the number of total play bouts(F = 93.42; d.f. = 10, 263; P < 0.01).
3.3. Different types of playful interaction
From birth to the 13th week of age, six types ofplay behaviours (social investigation, play-fighting, play-mounting, aggressive play, objects play and pseudo-sexualplay) were recorded (Table 4). Of all play bouts (n = 50,040)recorded in this study, 20,982 (41%) were identifiedas social play, 8767 (18%) as play-fighting, 7659 (15%)as play-mounting, 5906 (12%) as aggressive play, 4393(9%) as object play and 2333 (5%) as pseudo-sexualplay. Social investigations occurred more frequently incomparison to other play types (F = 75.28; d.f. = 5, 143;P < 0.01).
Social investigation was first observed at 3 weeks ofage, whereas play-fighting showed up first at week 4and play-mounting by the end of week 4. Both aggres-sive play and object play were first shown by week 5 andpseudo-sexual play by week 6 (Table 4). Weekly mean(±S.E.) number of play bouts varied from 5.63 (±1.17)to 224.08 (±12.95) in cases of social investigation, 3.42(±0.36) to 113.29 (±8.82) in cases of play-fighting, 3.00(±0.47) to 100.88 (±12.12) in cases of play-mounting,2.79 (±0.22) to 105.67 (±8.49) in cases of aggressive play,2.25 (±0.11) to 72.46 (±3.55) in cases of object play, and1.50 (±0.26) to 33.38 (±3.74) in cases of pseudo-sexualplay leading to significant differences from week to week(F = 112.66; d.f. = 10, 263; P < 0.01), (F = 69.69; d.f. = 9, 239;P < 0.01), (F = 31.56; d.f. = 9, 239; P < 0.01), (F = 77.83; d.f. = 8,215; P < 0.01), (F = 222.75; d.f. = 8, 215; P < 0.01), (F = 32.93;d.f. = 7. 191; P < 0.01) respectively (Table 4).
All the play behaviours showed an initial increase in fre-quency from week 3 to 8 or 9 (Table 5). Social investigationincreased up to week 8 (r = 0.9853, P < 0.05), and the fiveother behaviours up to week 9 (play-fighting, r = 0.9694,P < 0.05; play-mounting, r = 0.9562, P < 0.05; aggressiveplay, r = 0.9097, P < 0.05; object play, r = 0.9301, P < 0.05;and pseudo-sexual play, r = 0.9685, P < 0.05). Play behaviourdecreased in all cases after a certain period of time. Socialinvestigation decreased in week 9 (r = −0.9416, P < 0.05),and the five other play behaviours in week 10 (play-fighting, r = −0.9372, P < 0.05; play-mounting, r = −0.9579,P < 0.05; aggressive play, r = −0.99451, P < 0.05; object play,r = −0.9693, P < 0.05; and pseudo-sexual play, r = −0.9939,P < 0.05).
3.4. Playful interactions in relation to sex
Of all playful interactions (n = 50,040), 32,414 (65%)were initiated by the male puppies (Table 3), and malepuppies initiated more playful interactions than did femalepuppies (�2 = 9.00, d.f. = 1, P < 0.005).
Figs. 2–7 show the frequencies of different types ofplay per hour per week. In all types of play behaviour
(social investigation, play-fighting, play-mounting, aggres-sive play, object play, and pseudo-sexual play) malepuppies initiated play with a greater frequency than didfemale puppies (t = 4.64, d.f. = 10, P < 0.0005, t = 3.48, d.f. = 9,P <0.005, t = 3.21, d.f. = 9, P < 0.01, t = 2.66, d.f. = 8, P < 0.025,
146 S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153
Table 5Frequency of different types of play initiated by 24 puppies (13males and 11 females) recorded on the basis of thrice per day with 30-min duration in eachobservation period.
Initiators Different types of play recipients Total
Social investigation Play-fighting Play-mounting Aggressive play Object play Pseudo-sexual play
M F M F M F M F M F M F
HM1 159 684 165 514 105 489 249 120 80 130 26 131 2852HM2 152 889 132 322 87 300 175 100 48 128 18 79 2430HF1 378 208 201 83 98 53 82 136 122 58 41 13 1473HF2 455 213 199 61 159 43 61 105 98 46 32 11 1483MM1 176 468 128 156 101 129 122 75 84 77 34 15 1565MM2 234 571 102 64 51 89 99 30 54 56 14 35 1399MF1 381 – 185 – 125 – 89 – 141 – 52 – 973LM1 205 715 156 348 126 340 242 145 80 169 32 149 2707LM2 175 675 91 377 85 294 124 91 74 91 19 122 2218LF1 424 164 236 61 108 34 96 130 123 40 33 15 1464LF2 612 220 158 59 120 36 108 130 110 45 21 10 1629SM1 586 579 212 214 211 170 276 165 85 101 40 123 2762SM2 478 278 257 116 221 97 245 75 156 87 17 72 2099SM3 695 212 201 98 178 75 151 49 85 55 10 56 1865SF1 756 – 398 – 55 – 134 – 201 – 52 – 1596NM1 224 1367 174 543 123 745 267 256 71 146 19 176 4111NM2 202 1186 152 525 114 598 241 175 42 210 14 162 3621NF1 578 278 145 159 132 121 89 154 175 72 89 18 2010NF2 519 319 143 143 139 110 64 77 148 58 73 16 1809NF 3 503 376 142 161 145 132 90 105 102 94 61 21 1932BM1 379 728 102 268 78 403 155 79 37 131 12 161 2533BM2 314 712 97 250 74 320 148 65 45 97 10 120 2252BF1 542 263 165 62 207 37 70 101 168 49 76 14 1754
24
639
BF2 545 205 190 52 178
Total 9672 11,310 4131 4636 3020 4
M = male, F = female.
t = 2.63, d.f. = 8, P < 0.025, and t = 3.53, d.f. = 7, P < 0.005respectively).
Table 6 shows the mean (±S.E.) number of dif-
ferent types of play behaviour for male and femalepuppies, Except in the case of aggressive play, malepuppies initiated play more often with female puppies(t = 3.18, d.f. = 12, P < 0.005, social investigation), (t = 2.85,Fig. 2. Number of social investigations per hour per puppy (n = 24) recorded on thfrom birth to 13 weeks of age.
66 100 97 27 10 9 1503
3443 2463 2426 1967 805 1528 50,040
d.f. = 12, P < 0.01, play-fighting), (t = 3.04, d.f. = 12, P < 0.005,play-mounting), (t = 2.40, d.f. = 12, P < 0.025, object play),(t = 5.97, d.f. = 12, P < 0.0005, pseudo-sexual play). On
the other hand female puppies initiated play moreoften with male puppies (t = 6.39, d.f. = 18, P < 0.0005,social investigation), (t = 3.99, d.f. = 18, P < 0.0005, play-fighting), (t = 3.63, d.f. = 18, P < 0.0005, play-mounting),e basis of thrice per day with 30-min duration in each observation period
S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153 147
F he basisb
(P
bmtqSbwa(
vaS
Fb
ig. 3. Number of play-fighting per hour per puppy (n = 24) recorded on tirth to 13 weeks of age.
t = 6.19, d.f. = 18, P < 0.0005, object play), (t = 4.23, d.f. = 18,< 0.0005, pseudo-sexual play).
In the case of aggressive play, the mean (±S.E.) num-er of male–male play bouts was 191.85 (±17.37) andale–female play bouts was 109.62 (±17.15) (Table 6);
herefore, male puppies initiated aggressive play more fre-uently with male puppies (t = 7.16, d.f. = 12, P < 0.0005).imilarly, the mean (±S.E.) number of female–male playouts was 86.27 (±6.54), and female–female play boutsas 115.33 (±7.88). Therefore, female puppies initiated
ggressive play more often with the female puppies
t = 2.86, d.f. = 18, P < 0.01).Six puppies – HM1, MM1, LM1, SM1, NM1, BM1 (one indi-idual puppy per litter) initiated 36%, 48%, 37%, 41%, 35%nd 30% intra-litter aggressive play respectively (Table 5).o, the puppies within the litters were significantly differ-
ig. 4. Number of play-mounting per hour per puppy (n = 24) recorded on the basirth to 13 weeks of age.
of thrice per day with 30-min duration in each observation period from
ent from each other in relation to the number of intra-litteraggressive play (�2 = 88.21, d.f. = 3, P < 0.005; �2 = 43.10,d.f. = 2, P < 0.005; �2 = 73.63, d.f. = 3, P < 0.005; �2 = 201.20,d.f. = 3, P < 0.005; �2 = 338.19, d.f. = 4, P < 0.005; �2 = 16.62,d.f. = 3, P < 0.005 respectively).
4. Discussion
The timing of reproduction is an important aspect of thebiology of free-ranging dogs with respect to the numberof breeding periods and the time of year breeding occurs.
Kleiman (1968) reported that domestic dogs breed twicea year, which has been confirmed by a number of authors(Daniels and Bekoff, 1989; Boitani et al., 1995). This con-tradicts previous studies that suggest that the free-rangingdogs in West Bengal breed once a year (Pal et al., 1998b,is of thrice per day with 30-min duration in each observation period from
148 S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153
orded o
Fig. 5. Number of aggressive play bouts per hour per puppy (n = 24) recperiod from birth to 13 weeks of age.Pal, 2001, 2003, 2005, 2008). Domestic dogs are knownto have litter sizes of up to 17, although the usual littersconsist of up to 10 puppies (Kleiman, 1968, Kleiman andEisenberg, 1973). AKC (2009) reported that the numberof puppies in a dog litter varies from 2 to 10, and littersizes in domestic dogs are influenced by several factorsincluding nutrition, breed, age of the bitches etc. The meanlitter size of 6.67 reported in this study is similar to thatreported by Macdonald and Carr (1995), Pal et al. (1999),Pal (2001, 2003, 2005), and AKC (2009) in other studies offree-ranging dogs.
Six types of play-like behaviours (social investigation,play-fighting, play-mounting, aggressive play, object playand pseudo-sexual play) were recorded in this study. Inter-litter as well as intra-litter variations in play behavioursuggest that the frequency of play bouts in puppies depends
Fig. 6. Number of object play bouts per hour per puppy (n = 24) recorded on thefrom birth to 13 weeks of age.
n the basis of thrice per day with 30-min duration in each observation
upon the number of group members as well as litter sexratio, which has also been reported by Caro (1981), Laviolaand Alleva (1995), D’Eath and Lawrence (2004), Nunes etal. (2004) and Ward et al. (2009).
The possibility that free-ranging dogs could form stablesocial groups has been highly debated. According to vanKerkhove (2004), free-ranging dogs exhibit more variabil-ity in social behaviours, with many dogs living in small,loosely structured groups that may be temporary ratherthan stable pack-like groups. However, an interesting fea-ture of this study was that the free-ranging dogs were
observed to live together in small groups over 1 year indi-cating the existence of long-term affiliative bonds amongfree-roaming dogs (Fox et al., 1975; Carr, 1985; Font, 1987;Pal et al., 1998a; Pal, 2003, 2008; Cafazzo et al., 2010),despite the widely held notion that urban stray dogs arebasis of thrice per day with 30-min duration in each observation period
S.K. Pal / Applied Animal Behaviour S
Tab
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cience 126 (2010) 140–153 149
“asocial” animals (e.g., Scott and Fuller, 1965; Beck, 1973;Kleiman and Brady, 1978; Berman and Dunbar, 1983;Daniels, 1983).
In this study, social investigation was observed as thefirst playful interaction among the littermates at 3 weeks ofage (Freedman et al., 1961; Scott and Fuller, 1965; Lund andVestergaard, 1998; Pal, 2008; Ward et al., 2008), and thenother types of play subsequently developed. Social investi-gation occurred more frequently than other types of play,which had also been observed by Drea et al. (1996) andTanner et al. (2007) in spotted hyenas. All types of playreached their peaks during the 8th or 9th weeks of life andthen subsequently decreased. An initial increase followedby a sudden drop of different types play with age has alsobeen previously noted by Freedman et al. (1961), Scott andFuller (1965), Fagen (1981, 1993), Lund and Vestergaard(1998), Pal (2008), Ward et al. (2008) in domestic dogs; andby Tanner et al. (2007) in spotted hyenas. Why does the fre-quency of different types of play increase in early life anddrop after 8 or 9 week of life? Play facilitates the devel-opment of social skills, e.g., by allowing members to learnhow to maintain social bonds, different motor skills andalso the acquisition by puppies of new information abouttheir social and physical environments (Biben, 1998; Lewis,2005; Palagi, 2007). These benefits may be attained mainlyfrom vigorous social play during the early weeks in life.The fact that play rates drop after 8 or 9 week of age sug-gests that the ability to capture new information via playfulinteractions is declining.
For a given species, sex differences in play are expectedto be more prominent when adult females and males dif-fer in physical characteristics (e.g., body size), behaviouralcharacteristics (e.g., involvement in hunting activity,intraspecific fighting, territorial defense) or social prefer-ences (e.g., formation of strong bonds with same-versusopposite sex individuals; Maestripieri and Ross, 2004;Burghardt, 2005). Among canids, males and females showlittle size dimorphism and engage in similar roles (Derixet al., 1993; McLeod and Fentress, 1997). Some researchhas suggested no sex differences in play style (Bekoff,1974a; Biben, 1983; Bauer and Smuts, 2007; Ward et al.,2008). However, among domestic dog puppies, sex differ-ences in play have been reported (Lund and Vestergaard,1998; Pal, 2008). Aldis (1975) reported that play was notless frequent in female than in male domestic dogs. Incontrast, in this study all six types of playful interactionswere more frequent in male than in female puppies. Thissupports the findings of Lund and Vestergaard (1998),Ward et al. (2008). This sex difference in play behaviourhas also been observed in other species, such as cercop-ithecines (Kummer, 1968; Owens, 1975; Symons, 1978),orangutans (Becker, 1984), squirrel monkeys (Biben, 1986,1998), gorillas (Watts and Pusey, 1993; Nowell, 2005),and chimpanzees (Mendoza-Granados and Sommer, 1995).Male puppies play more frequently perhaps to preparethemselves for competition with other males during adult-
hood. Although evidence is scant, female puppies initiatedplayful interactions more frequently with male puppies.These results may suggest that in the case of free-rangingdog puppies playful interactions are mostly inter-sexual,and perhaps playing with opposite sex partners provides
150 S.K. Pal / Applied Animal Behaviour Science 126 (2010) 140–153
ed on th
Fig. 7. Number of pseudo-sexual bouts per hour per puppy (n = 24) recordfrom birth to 13 weeks of age.opportunities for the puppies to learn characteristics ofthe opposite sex and gain competence in interactions withthem later.
Evidence for some species indicates that mammals playmore and initiate play more often with individuals they candominate during play (Owens, 1975; Biben, 1986, 1998).Even so, experiencing subordinate positions during playmay also confer long-term benefits because individualsgain the opportunity to practice defensive strategies thatcould later be used during an actual fight. Most of the play-fightings recorded in this study were initiated by the malepuppies, which seems to agree with the findings of Scottand Marston (1950) and Lund and Vestergaard (1998). Itis well documented in humans that boys engage in moreplay-fighting than do girls (Aldis, 1975; Pelligrini, 1989;Frey and Hoppe-Graff, 1994; Pelligrini and Smith, 1998).The same has been observed in the Giant Panda wheremale cubs spend more time (Synder et al., 2003). Fagen(1981) suggested that sex differences in play-fightingshould be present only when fighting skills are differen-tially important in adult males and females. Accordingto Pal et al. (1998a), fights among the adult dogs arecommon at territorial boundaries and also in the court-ing places, and predominantly occur between males. Theresults of this study suggest that play-fighting at an earlystage in life is important for developing better fightingskills in adult life, this being predominantly true for maleindividuals.
Blackshaw (1985) suggested that formation of a dom-inance hierarchy is a necessary part of achieving a stablesocial environment. In this study, one individual puppy perlitter, perhaps to establish its social rank, initiated aggres-
sive play more often with other litter mates between 5and 13 weeks of age. Pereira (1993) found that in infantring tailed lemurs play was quite symmetrical, but thatin adolescence, play sessions were used to establish dom-inance relationships. Paquette (1994) also found that ine basis of thrice per day with 30-min duration in each observation period
adolescent chimpanzees, asymmetry in play was stronglylinked with ranking position. Based on these observationsin other species, it may be suggested that dominance hier-archy amongst the free-ranging dogs is developed at anearly stage of life, which agrees with what Scott (1962), Fox(1971), Fox et al. (1976), Bradshaw and Nott (1995), Serpelland Jagoe (1995), and Pal (2008) observed as well. The pref-erence for same-sex play initiations in males and femalesduring aggressive play suggests that play may serve astraining for intra-sexual competition between same-sexlittermates. Like wolves (Mech, 1970; Packard, 2003), bothfemale and male domestic dogs form intra-sexual domi-nance relationships (Pal et al., 1998a; Ward et al., 2008),and play may function in the formation of these dominancerelationships (Bekoff, 1972; Fox and Bekoff, 1975). Becausedominance conflicts generally occur between same-sexdogs (Borchelt, 1983; Sherman et al., 1996), same-sex part-ners may play to practice threat and appeasement signalsthat ritualize aggression. Practicing aggressive componentswithin a safe range of intensity could limit the occurrenceof overt aggression later on (Lindsay, 2005). The early onsetand consistent preference for females to initiate play withother females may be one way females learn to moderatesame-sex aggression (Ward et al., 2008)
Predominantly the males were observed to mount (4thweek of litters’ life) even with pelvic thrusting (6th weekof litters’ life), which has been previously noticed byRheingold (1963), Scott and Fuller (1965), De Hasse (1994)and Pal (2008). Tanner et al. (2007) found that rates ofplay-mounting were higher in male than female hyenacubs. Perhaps, to achieve successful mating in adulthood,the male puppies may thus need practice earlier in life
(Hart, 1980; Pal, 2008). Moreover, it may be presumed thatmountings especially the pseudo-sexual plays are inter-sexual, and perhaps to practice the solicitation behaviourin adulthood (Pal et al., 1999) the female puppies mountedthe male puppies.
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Tanner et al. (2007) found no relation between thebject play and tooth eruption in spotted hyenas. But theuppies in this study were observed to bite and gnawbjects like sticks, papers, old scraps of skin etc. by week 5nd thereafter when the deciduous teeth erupt (Shabestarit al., 1967). Therefore, it may be presumed that bitingnd gnawing objects might be associated with the growthf deciduous teeth. Although this type of play does notequire play partner, competition among the littermatesccurred to capture the objects. Occasionally, the pup-ies were observed running with or tugging on sticks,lastics, dried bones etc. Perhaps free-ranging dog pup-ies rely on their mouths for gaining information aboutbjects encountered in their environment. It was also pre-iously suggested by Tanner et al. (2007) in case of hyenaubs.
Social play in animals and, particularly, in the free-anging dogs is of significant interest to ethologists,nthropologists, and psychologists. However, very little isnown about the significance of different types of puppy’slay. The result of Katwa study seems to agree in manyspects with the studies of Rheingold (1963), Lund andestergaard (1998), Ward et al. (2008, 2009) and Cafazzot al. (2010). Although, the sample sizes in this studyere too small, this study suggests that development of
ome physical and social behaviour takes place a little ear-ier in free-ranging dogs than in captive dogs, and adultehaviours are developed based on different types of play-ul interactions from the early ontogeny. I think the naturend purpose of different types of play may vary with theog breeds and also with the status of the dogs (cap-ive dogs and free-ranging dogs). So, I cannot generalizehese findings to larger populations, and further research iseeded.
cknowledgement
I thank Prof. E. Font, M. Spinka and Dr. C. Ward whoead the drafts of this article and improved the quality. I amincerely grateful to the editor and the anonymous refereeor advice and comments on the final drafts of this article.wish to thank Mr. Subhadip Pal and Mrs. Dipti Pal whossisted with field works.
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