Investigating the Function of Play Bows in Dog and Wolf Puppies (Canis lupus familiaris, Canis lupus occidentalis)

Publishing Authors : Sarah-Elizabeth Byosiere, Julia Espinosa, Sarah Marshall-Pescini, Barbara Smuts
Friederike Range

Date Published : 29/12/16

Abstract
Animals utilize behavioral signals across a range of different contexts in order to communicate
with others and produce probable behavioral outcomes. During play animals frequently
adopt action patterns used in other contexts. Researchers have therefore hypothesized that
play signals have evolved to clarify communicative intent. One highly stereotyped play signal
is the canid play bow, but its function remains contested. In order to clarify how canid
puppies use play bows, we used data on play bows in immature wolves (ages 2.7–7.8
months) and dogs (ages 2 to 5 months) to test hypotheses evaluated in a previous study of
adult dogs. We found that young dogs used play bows similarly to adult dogs; play bows
most often occurred after a brief pause in play followed by complementary highly active play
states. However, while the relative number of play bows and total observation time was similar
between dog and wolf puppies, wolves did not follow this behavioral pattern, as play
bows were unsuccessful in eliciting further play activity by the partner. While some similarities
for the function of play bows in dog and wolf puppies were documented, it appears that
play bows may function differently in wolf puppies in regards to re-initiating play.
Introduction
Communication can be defined as a multifaceted exchange between senders and receivers
each with their own targets or goals [1]. Within this exchange an individual performs a signal
in order to induce the receiver of said signal to perform a probable pattern [2]. These signals
may be “behavioral, physiological, or morphological characteristics fashioned or maintained
by natural selection [as] they convey information to other organisms” [3, p. 385].
In non-human animals (hereafter animals), signals are often assumed to represent simple
single traits [4]. This oversimplification ignores the fact that signals often occur in complex
contexts and are imperative in animal communication. Individuals must signal that they wish
to initiate an interaction and then negotiate the nature of it [5,6]. This means that senders
must choose an appropriate signal(s) based on context-specific information to ensure a
PLOS ONE | DOI:10.1371/journal.pone.0168570 December 29, 2016 1 / 16
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OPEN ACCESS
Citation: Byosiere S-E, Espinosa J, MarshallPescini
S, Smuts B, Range F (2016) Investigating
the Function of Play Bows in Dog and Wolf Puppies
(Canis lupus familiaris, Canis lupus occidentalis).
PLoS ONE 11(12): e0168570. doi:10.1371/journal.
pone.0168570
Editor: Sergio Pellis, University of Lethbridge,
CANADA
Received: August 25, 2016
Accepted: December 3, 2016
Published: December 29, 2016
Copyright: © 2016 Byosiere et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: Data files used for
the final analysis are available from Figshare at
https://dx.doi.org/10.6084/m9.figshare.4307765.
v1.
Funding: This research was financially supported
by the European Research Council under the
European Union’s Seventh Framework Program
(https://ec.europa.eu/research/fp7/index_en.cfm)
by ERC Grant Agreement n. [311870] and the
Austrian Science Fund (https://www.fwf.ac.at/en/)
project P21244-B17 & P24840. The authors
successful outcome [7]. Furthermore, multiple single signal components may be combined
into a multimodal signal, thereby inducing additional behavioral outcomes (for examples see
[8]). Considering the variety of mediums (such as visual, auditory, and olfactory), intensities,
frequencies, and situational contexts in which signals can occur, proper utilization is highly
complex.
While signals are performed across a range of contexts, their function within play behavior
is particularly fascinating [9]. Within playful interactions, action patterns common to other
contexts such as aggressive and sexual bouts are often performed [6,10–12]. Therefore, these
generalizable action patterns may, on a surface level, appear fundamentally identical while the
communicative intent behind them may vary drastically [13]. Researchers have hypothesized
that animals discriminate between these contexts and maintain a playful atmosphere through
the use of play signals.
Play signals have typically been thought to communicate playful intentions in order to commence,
continue, and recommence social play [5,14,15]. Thus, they may serve as social mediators,
or ways for the signaler to convey his/her intentions in a manner easily interpretable for
the receiver [16]. They can co-occur as modifiers of other behaviors, such as an open mouth
display while charging, or they can be specific actions, like exaggerated bouncy movements
interspersed among other behaviors. Play signals may vary or even evolve within or across
structured play bouts in a way to redefine the appropriate “rules” of play [9,17]. Consequently,
maintaining a playful bout not only requires sophisticated communicative skill, but also communicative
effort, improvisation, strategic timing, creativity, and the capacity to cope with
unexpected events or unpredictable partner reactions [9,18].
Canids, such as dogs and wolves, are unusual in that they exhibit high frequencies of play
behaviors even as adults (for a review of dog play see [19,20]). Furthermore, they exhibit one
of the most stereotyped and easily recognizable carnivore play
position, and that after the bow dogs most commonly showed active behaviors such as mutual
rear-ups and complimentary runaway/chase sequences. Therefore, the authors concluded that
one important function of the play bow is to re-initiate play after a pause [24].
Due to the paucity of research and lack of consensus about the function of play bows in
dogs and other canids, the current study adopted a comparative approach to further clarify the
purpose of this highly stereotyped play signal. Specifically, we aimed to investigate whether the
behavioral patterns observed around play bow signaling in adult dogs developed similarly in
both dog and wolf puppies. In doing so we expand on the study by Byosiere et al. [24] that
assessed a variety of proposed functions such as whether play bows function as visual signals
[11,24], to clarify intentions [26], to resume play, to occupy a better strategic position [16], or
to synchronize behavioral actions [27,28].
Hypotheses and Predictions
To further examine the function of play bows in wolf and dog puppies, behaviors occurring
just before and just after the play bow for both the play bower and the play partner were analyzed
(following the methods of [24]; see Table 1 for a summary of supported hypotheses). The
following hypotheses derive from the studies described in the introduction and predict outcomes
that may not be mutually exclusive (hypothesis 1, 2 and 5), while others may be
(hypotheses 2 and 3).
Hypothesis 1: Play bows as visual signals
1. If play bows function as visual signals, play bows should be limited to times when the
bower and partner are within one another’s visual field (S1 Table).
2. If play bows function as visual signals, play bows performed when the players are not
within one another’s visual fields should occur in association with attention-getting
behaviors, as defined by Horowitz (2009).
Hypothesis 2: Clarification of easily misinterpretable behaviors
If play bows function to clarify behaviors by the bower that are most susceptible to misinterpretation,
the bower should perform more offensive behaviors than the partner before and/
or after play bowing.
Hypothesis 3: Attacking and escaping the play partner
1. If play bows function to obtain an optimal position to better ‘attack’ the play partner, the
bower should perform more offensive behaviors after the play bow than before.
Table 1. Summary of evidence for hypotheses 1–5 in adult dogs from Byosiere et al., (2016).
Hypothesis Adult Dogs
1: Play bows as visual signals Yes
2: Clarification of easily misinterpretable behaviors No
3a: Attacking the play partner No
3b Escaping from the play partner Maybe
4: Re-initiation of play Yes
5: Play bow synchronization Yes
doi:10.1371/journal.pone.0168570.t001
Investigating the Function of Play Bows in Dog and Wolf Puppies
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2. If play bows function to obtain an optimal position to better ‘escape’ the play partner,
the bower should perform more vulnerable/escape behaviors, such as runaway (for definitions
see S1 File), after the play bow than before.
Hypothesis 4: Re-initiation of play
If play bows function to reinitiate play, both the bower and the partner should perform
more pauses and passive non-play behaviors before the play bow than after.
Hypothesis 5: Play bow synchronization
If play bows function to help synchronize play behaviors, the bower and the partner should
perform more synchronous behaviors after the play bow than before.
Materials and Methods
Ethical Statement
No special permission for use of animals (wolves and dogs) in such observational studies is
required in Austria (Tierversuchsgesetz 2012- TVG 2012). The relevant committee that allows
running research without special permissions regarding animals is: Tierversuchs-kommission
am Bundesministerium fu¨r Wissenschaft und Forschung (Austria).
Subjects
Dog and wolf puppies were raised in the same way, hand-reared in peer groups, and bottlefed/hand-fed
by humans from 10 days of age to 4 months. The dogs were mongrels born in
Hungarian animal shelters or at the Wolf Science Center in Ernstbrunn, Austria. All wolves
were born in captivity. Dogs observed in 2014 were born at the center, and spent at least four
hours per day with a trainer and other puppies (without the mother) (see [29] for additional
information). Both species were kept in a similar manner and therefore have the same life
experiences in order to compare the two without fundamental differences in ontogeny.
Dog subjects (Canis lupus familiaris) consisted of 10 dogs. All play interactions involved
dog puppies of 75 to 140 days (2 to 5 months). See Table 2 for demographic and relatedness
information for dogs. Wolf subjects (Canis lupus occidentalis) consisted of 15 timber wolves.
All play interactions involved wolves of 85 to 1254 days (2.7 months to 3.4 years), however
only play bows performed by wolf puppies aged 85 days to 239 days (2.7 to 7.8 months) were
Table 2. Demographic data for dog puppies sampled.
Name Sex Siblings Puppy Pack
Banzai M Enzi, Panya, Pepeo Pack A (2014)
Enzi M Banzai, Panya, Pepeo Pack A (2014)
Gombo M Hiari, Imara, Sahibu Pack A (2014)
Hiari M Gombo, Imara, Sahibu Pack A (2014)
Imara F Gombo, Hiari, Sahibu Pack A (2014)
Nia F Pack B (2011)
Kali F Pack B (2011)
Panya F Banzai, Enzi, Pepeo Pack A (2014)
Pepeo M Banzai, Enzi, Panya Pack A (2014)
Sahibu F Gombo, Hiari, Imara Pack A (2014)
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Investigating the Function of Play Bows in Dog and Wolf Puppies
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analyzed. Therefore a play partner could be an older wolf, however no play bow performed by
an older wolf was included in the analysis.
Additional analyses were conducted and revealed no significant difference in the results
when the adults were removed as partners from the sample.
See Table 3 for demographic and relatedness information for wolves. One set of wolf puppies
was observed in 2009 and one in 2012 [29]. Each pack consisted of six wolf puppies with
both kin and non-kin (no more than two individuals from one litter per pack). Wolf puppies
lived in a single pack for the first four months of life. Next, they were introduced into already
established packs of adult wolves (mixed pack). In 2009, all six puppies were integrated into a
previously established group of three adult wolves. In 2012, the six puppies were separated in
twos and integrated into each of the three mixed packs (Table 3).
Data Collection and Video Coding
Dyadic play bouts were videotaped for research purposes during 2009 and 2012 for wolf puppies,
and 2011 and 2014 for dog puppies by researchers at the Wolf Science Center as part of a
study on wolf and dog play and social behavior. Videos coded for the current study were taken
from a database of already recorded videos. Permission from management at the Wolf Science
Center was obtained to review and analyze previously recorded videos. Some of these videos
and data have been analyzed and published (for descriptive information about these videos see
[29]). Filming for these interactions took place in the animal’s home enclosures, which were
large, fenced outdoor areas; elevated areas used for shelters, as well as trees, brush, and occasionally
fallen tree trunks. Video recordings analyzed for this study did not include any feeding
times. All observations were distributed throughout the day, from roughly 0600 to 2000 hours.
Twenty hours and 39 minutes of video recordings were analyzed for the dog sample, and 16
hours and 53 minutes of video recordings were analyzed for the wolf sample. Videos were
recorded on 62 different days for the dogs and 40 for the wolves. The first two authors coded
the videos; both had previously reached 90% agreement using this coding protocol (see [24]
for a comprehensive review of the methods).
Data was coded in a way so that only the immediate behavior both before and after the play
bow were coded for the bower and the partner. Our rationale was that this was the most direct
Table 3. Demographic data for Timber wolf puppies sampled.
Name Sex Siblings Birthplace Puppy Pack Adult Pack
Amarok M Tala Minnesota Wildlife Connection Pack B (2012) Pack C
Apache M Cherokee Zoo Basel Pack A (2009) Pack A
Aragorn M Shima Herberstein Zoo Pack A (2009), Pack D (2012)
Cherokee M Apache Zoo Basel Pack A (2009) Pack A
Chitto M Una Minnesota Wildlife Connection Pack B (2012) Pack D
Geronimo M Yukon Triple D Farm, Montana USA Pack A (2009) Pack A
Kay F Wamblee Haliburton Forest Canada PackB (2012) Pack C
Kaspar M Herberstein Zoo Pack A (2009), Pack D (2012)
Nanuk M Triple D Farm, Montana USA Pack A (2009) Pack A
Shima F Aragorn Herberstein Zoo Pack A (2009), Pack D (2012)
Tala F Amarok Minnesota Wildlife Connection Pack B (2012) Pack D
Tatonga F Triple D Farm, Montana USA Pack A (2009) Pack A
Una F Chitto Minnesota Wildlife Connection Pack B (2012) Pack B
Wamblee M Kay Haliburton Forest Canada Pack B (2012) Pack B
Yukon F Geronimo Triple D Farm, Montana USA Pack A (2009) Pack A
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way to test the various hypotheses and to compare how bower and partner behavior may have
changed as a result of the play bow. Play bows were only coded when they occurred during a
play bout (defined below), not when they were used to initiate a play bout, and when they met
specific and detailed criteria involving both the type of movement and duration. Play bows
were defined as beginning when an individual’s front legs began to bend, and concluding
when an individual fully extended the elbows back to an upright position, lay down, or
adopted a new position in which the rear was not elevated above the front end. Play bows had
to last at least 1/3 of a second in order to be coded as such [24]. Dyadic play bouts were coded
when play continued for at least 15 seconds. The play bout was considered over after a minute
without either individual in a dyad showing any of the play behaviors listed in S1 File. We
recorded only instances in which play bows occurred during dyadic play bouts. If a third (or
fourth, fifth) individual interrupted the bout for more than 15 seconds, the dyadic play bout
was considered to be over.
During a play bow, we coded the pair as facing one another when each was within the other’s
visual field (S1 Table). Furthermore, behaviors occurring immediately before and immediately
after play bows by both the bower and partner were coded (see S1 File for the ethogram).
These play behaviors (from here on termed behavior codes) were divided into five mutually
exclusive categories: offensive/dominant, vulnerable/escape, pause, synchronous, and miscellaneous
(S1 File) [24]. Offensive/dominant behaviors consisted of mock-attack play behaviors
(e.g., tackle, bites; [30], chases/charges and receipt of formal submission (i.e., muzzle licks;
[31]). Vulnerable/escape behaviors included self-handicapping behaviors, receiving an offensive
behavior (e.g., ‘is tackled’), and running away behaviors. Note that many of the behaviors
shown in these two categories were reciprocal; that is, if one dog showed an offensive behavior,
such as pushing or tackling the other dog, the partner would be coded as receiving a vulnerable/escape
behavior, in this case, being pushed/tackled. Pause behaviors were all behaviors that
involved little movement (i.e., the individual took two steps or less) and that lasted at least 1.5
seconds.
Synchronous behaviors included two types of actions that both players commonly performed
synchronously (e.g. they displayed very similar or identical behaviors overlapping in
time), moving together and rearing up together. Note that we did not include any other behaviors
occurring in synchrony within the analysis. However, we have noted the instances in
which the bower and the partner performed the same behavior. Many of these instances
included relatively stationary behaviors and thus were accounted for in the “pause” behavior
category. All other instances in which the bower and partner performed the same behavior
occurred at extremely low rates (approximately 2% of all behaviors before, and 1.8% after the
bow for dog puppies, and 1.4% before and 2.5% after the bow for wolf puppies). Finally when
two play bows given by different individuals overlapped in time, they were considered synchronous
bows and were used to evaluate hypothesis #5.
Data Analysis
To evaluate hypotheses 2 through 5, a generalized linear mixed model (GLMM) [32] was used
to analyze the proportion of a particular behavior category (Table 3) relative to all other behavior
categories combined (binary model) (for a comprehensive review of the model see [24]).
The model contained fixed effects for role (bower versus partner) and timing (before versus
after the bow), and a fixed effect interaction between role and timing. Random effects for individual
and dyad were also included. Thus, the proportion of a given behavior (P) was modeled
Investigating the Function of Play Bows in Dog and Wolf Puppies
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as:
LogitðPtijÞ ¼ β0 þ b1Role þ b2Time þ b3ðRole TimeÞ þ b0i þ b0ij
Where b denotes a random effect, t denotes timing, i denotes the individual dog, and j denotes
the dyad. Four binary regressions were conducted comparing one behavior category to all
other behavior categories. Results, therefore, represent the change in proportion of a particular
behavior category across time (i.e., before or after the bow) and/or as a function of role (i.e.
bower or partner). Since 4 comparisons, 2 for role and 2 for time, were used per behavior category
analysis, a Bonferonni post-hoc correction of .01 was applied to results for each regression
to reduce the chances of a type I error. Convergence criteria were satisfied for each test conducted
using the logistic binary regression.
Two-tailed one sample t-tests (alpha set at 0.05) were conducted to analyze differences in
observed bite behaviors performed by the bower and the partner both before and after the
bow.
Results
For the dog puppies, we observed 136 play bows by 10 dogs in 26 dyads (2 female-female
dyads, 12 male-female, and 12 male-male) (Table 4). Play bows occurred at a rate of 10.97%
across the observed video time. For the wolf puppies we observed 69 play bows during play by
15 wolves in 25 dyads (4 female-female, 12 male-female dyads and 9 male-male dyads)
(Table 5). Play bows occurred at a rate of 6.81% across the observed video time. The number
of play bows per dyad in the dog puppies varied from 1 to 16, and 1 to 13 in wolf puppies. For
a comprehensive overview of the data output see S2 File.
Hypothesis Testing
Hypothesis 1: Play bows as visual signals. Hypothesis 1a predicted that play bows would
almost always be limited to times when the bower and partner were within one another’s visual
field. This prediction was confirmed for dog puppies: for 135 of the 136 play bows the dogs
could see one another. In this one exceptional instance, the bower performed an attention-getting
behavior by barking as predicted by [11] (Hypothesis 1b).
This prediction was also confirmed for wolf puppies: for all 69 of the play bows the subjects
could see one another. Therefore, hypothesis 1b could not be evaluated for the wolves.
Hypotheses 2 through 5. Percentages for each behavior category were determined before
the play bow and after the play bow for both the bower and the partner (see Figs 1 and 2 for
dog puppies and wolf puppies respectively). All tests of significance are shown in Table 6 for
the dog puppies and Table 7 for the wolf puppies.
Hypothesis 2: Clarifying easily misinterpretable behaviors. Hypothesis 2, based on [26],
predicted that if play bows function to clarify easily misinterpretable behaviors, bowers should
perform more offensive behaviors before and/or after play bows than partners. Results did not
confirm this prediction for either species. For both dog and wolf puppies, no difference in
offensive behaviors by role was observed before the play bow (Table 6, row 3, column C;
Table 7, row 3, column C). Contrary to prediction, after the bow, dog puppy partners showed
more offensive behaviors than the bower did (Table 6, row 3 column D). No difference in
offensive behaviors by timing was observed before the bow for either dog or wolf puppies
(Table 6, row 3, column A; Table 7, row 3, column A). However, dog puppy partners showed
more offensive behaviors after the bow than before (Table 6, row 3, column B).
Due to evidence suggesting that play bows serve to clarify easily misinterpreted aggressive
behaviors by the bower (specifically those associated with bite-shakes; see Bekoff, 1995), the
Investigating the Function of Play Bows in Dog and Wolf Puppies
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frequencies of bite-like behaviors (nips and bites, hereafter termed bites; see S1 File for definitions)
in association with play bows were analyzed. For both dog and wolf puppies, no biteshakes
immediately preceded or followed a play bow by the bower or the partner.
For dog puppies, bite behaviors were performed only 13.6% of the time, occurring only 73
times out of the 544 behaviors for both the bower and the partner before or after the play bow
(39 times by the bower, and 34 times for the partner) (p = 0.53). However, while bowers were
equally likely to perform bite behaviors before (n = 21) and after (n = 18) the bow (p = 0.50),
partners were more likely to perform bite behaviors after the bow (n = 27) than before (n = 7)
(p < 0.01). Of the 276 wolf behaviors recorded for both the bower and the partner before and
after the bow, only 28 (10.14%) were bites. Bowers (p = 0.02) and partners (p = 0.04) were
more likely to perform bite behaviors before the bow than after (bower before, n = 13; bower
after, n = 7; partner before, n = 6; partner after, n = 2). Bowers (n = 20) were more likely to perform
bite behaviors, in general, than partners (n = 8) (p < 0.01).
Table 4. Distribution of play bows within and across dog puppy dyads.
Dyad Dyad Sex Play Bow Count1 Bow Mean2 Play Bow Ratio3
Banzai/Enzi M/M 6 4.41 1:5
Banzai/Imara M/F 4 2.94 2:2
Banzai/Pepeo M/M 2 2.21 1:0
Banzai/Sahibu M/M 1 0.74 1:0
Enzi/Gombo M/M 5 3.68 5:0
Enzi/Hiari M/M 12 8.82 3:8
Enzi/Imara M/F 13 9.56 4:9
Enzi/Panya M/F 7 5.15 3:4
Enzi/Pepeo M/M 16 11.76 8:8
Enzi/Sahibu M/M 2 1.47 1:1
Hiari/Banzai M/M 1 0.74 0:1
Hiari/Imara M/F 1 0.74 1:0
Hiari/Panya M/F 6 4.41 4:2
Hiari/Pepeo M/M 8 5.88 6:2
Imara/Gombo F/M 1 0.74 1:0
Imara/Pepeo F/M 12 8.82 9:3
Nia/Kali F/F 1 0.74 1:0
Panya/Banzai F/M 3 2.21 3:2
Panya/Gombo F/M 3 2.21 3:0
Panya/Imara F/F 1 0.74 1:0
Panya/Pepeo F/M 3 2.21 3:0
Panya/Sahibu F/M 10 7.35 7:3
Pepeo/Gombo M/M 1 0.74 0:1
Pepeo/Sahibu M/M 13 9.56 7:6
Sahibu/Gombo M/M 3 2.21 2:1
Sahibu/Imara M/F 1 0.74 1:0
Note:
1
—The number of play bows performed by members of the dyad.
2
—The mean of play bows performed by members of the dyad across all play bows for the sample.
3
—The relative number of play bows within the dyad by individual. The first value corresponds to the number
of play bows performed by the first dog in the corresponding “dyad” column. The second value corresponds
to the number of play bows performed by the second dog in the corresponding “dyad” column.
doi:10.1371/journal.pone.0168570.t004
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Hypothesis 3: Attacking & escaping the play partner. Hypothesis 3a predicted that play
bows might function to better position the bower to ‘attack’ the play partner. If so, bowers
should perform more offensive behaviors after the play bow than before. As noted above
(Hypothesis 2), bowers, in both dog and wolf puppy samples were not more likely to perform
offensive behaviors after the bow than before (Table 6, row 3 column A; Table 7, row 3 column
A). In fact, after the play bow, dog puppy partners rather than bowers were more likely to perform
offensive behaviors (Table 6, row 3 column D). For wolf puppies, this difference was not
observed, as no differences were observed in offensive behaviors between wolf puppy play
bowers and partners (Table 7, row 3 columns D).
Hypothesis 3b alternatively suggested that play bows might function to better position the
bower to escape from the play partner. If so, bowers would be expected to perform more vulnerable/escape
behaviors after the play bow than before. The prediction for hypothesis 3b was
confirmed for both dog and wolf puppies: bowers performed more vulnerable/escape behaviors
after the play bow than before (Table 6, row 2 column A; Table 7, row 2 column A).
Table 5. Distribution of play bows within and across wolf puppy dyads.
Dyad Dyad Sex Play Bow Count1 Bow Mean2 Play Bow Ratio3
Aragorn/Tatonga M/F 1 1.45 0:1
Aragorn/Cherokee M/M 1 1.45 0:1
Geronimo/Cherokee M/M 1 1.45 0:1
Geronimo/Tatonga M/F 3 4.35 1:2
Chitto/Kay M/F 1 1.45 1:0
Tala/Wamblee F/M 1 1.45 1:0
Tala/Amarok F/M 2 2.90 2:0
Apache/Cherokee M/M 13 18.84 4:9
Shima/Yukon F/F 1 1.45 0:1
Kaspar/Tala F/M 1 1.45 0:1
Yukon/Tatonga F/F 2 2.90 1:1
Chitto/Amarok M/M 2 2.90 1:1
Geronimo/Amarok M/M 5 7.25 0:5
Amarok/Kay M/F 1 1.45 0:1
Nanuk/Apache M/M 2 2.90 2:0
Aragorn/Nanuk M/M 1 1.45 0:1
Nanuk/Yukon M/F 2 2.90 2:0
Tala/Una F/F 2 2.90 1:1
Yukon/Cherokee F/M 2 2.90 2:0
Geronimo/Apache M/M 5 7.25 4:1
Apache/Tatonga M/F 2 2.90 0:2
Tala/Chitto F/M 3 4.35 1:2
Nanuk/Geronimo M/M 4 5.80 0:4
Una/Wamblee F/M 5 7.25 5:0
Yukon/Una F/F 6 8.70 0:6
Note:
1
—The number of play bows performed by members of the dyad.
2
—The mean of play bows performed by members of the dyad across all play bows for the sample.
3
—The relative number of play bows within the dyad by individual. The first value corresponds to the number of play bows performed by the first wolf in the
corresponding “dyad” column. The second value corresponds to the number of play bows performed by the second wolf in the corresponding “dyad”
column.
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Fig 1. Percentages of Behavior by Timing and Role in Dog Pups. The percentage of behaviors in each behavior categories observed for
both the bower and partner before and after the play bow in dog puppies (n = 544).
doi:10.1371/journal.pone.0168570.g001
Fig 2. Percentages of Behaviors by Timing and Role in Wolf Pups. The percentage of behaviors in each behavior categories observed
for both the bower and partner before and after the play bow in wolf puppies (n = 276).
doi:10.1371/journal.pone.0168570.g002
Investigating the Function of Play Bows in Dog and Wolf Puppies
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Additionally, both dog and wolf puppy play bowers were also more likely to perform vulnerable/escape
behaviors after the play bow than were their play partners (Table 6, row 2 column
D; Table 7, row 2 column D), an effect of role consistent with hypothesis 3 but not predicted
by it.
Hypothesis 4: Re-initiation of play. Hypothesis 4 predicted that both the bower and the
partner would show more pause behaviors before the play bow than after. To test this hypothesis,
the effects of timing (before versus after the play bow) were compared for proportions of
pause behavior by both the bower and the partner. Results confirmed the predicted effect for
dog puppies (Table 6, row 1, columns A and B). Both the bower and the partner displayed
more pause behaviors before the play bow than after. Results did not confirm the prediction
for wolf puppies (Table 7, row 1, columns A and B). However, wolf partners were significantly
more likely to show a pause behavior before the play bow than was the bower (Table 7, row 1,
column C); a difference that was not significant for the dog puppies.
Hypothesis 5: Play bow synchronization. Hypothesis 5 predicted that if play bows help a
pair to synchronize behaviors, then synchronous behaviors should be more common after a
play bow than before. Since, by definition, the proportion of synchronous behaviors must
always be the same for the bower and the partner, one statistical test applies to both roles. The
prediction was not confirmed for either dog or wolf puppies: bowers and partners were no
more likely to perform synchronous behaviors after the play bow than before (Table 6, row 5,
column A; Table 7, row 5, column A).
Discussion
In order to address the function of the play bow within wolf and dog puppy dyadic play we
analyzed the behaviors occurring immediately before and after a bow for both the play bower
Table 6. General Linear Mixed Model Results for Dog Puppies.
Timing Role
Behavior Categories A. Before vs. After for Bower B. Before vs. After for Partner C. Bower vs. Partner Before D. Bower vs. Partner After
1. Pause p = .0003 p = .0022 p = 0.8934 p = 0.5774
2. Vulnerable/ Escape p < .0001 p = .7258 p = 0.1723 p < .0001
3. Offensive p = 1.0000 p = .0002 p = 0.9592 p = .0002
4. Miscellaneous p = 0.0409 p = 0.1343 p = 0.1542 p = 0.3769
5. Synchronous p = .3243 p = 1.000
Note. “Bold face”–Significant results
doi:10.1371/journal.pone.0168570.t006
Table 7. General Linear Mixed Model Results for Wolf Puppies.
Timing Role
Behavior Categories A. Before vs. After for Bower B. Before vs. After for Partner C. Bower vs. Partner Before D. Bower vs. Partner After
1. Pause p = 1.000 p = .4816 p = 0.0091 p = 0.0471
2. Vulnerable/Escape p = 0.0026 p = .3869 p = 0.7539 p = 0.0091
3. Offensive p = .5729 p = .0793 p = 0.0793 p = .5729
4. Miscellaneous p = 0.0265 p = 0.1028 p = 0.3575 p = 0.7042
5. Synchronous p = 1.000 p = 1.000
Note. “Bold face”–Significant results
doi:10.1371/journal.pone.0168570.t007
Investigating the Function of Play Bows in Dog and Wolf Puppies
PLOS ONE | DOI:10.1371/journal.pone.0168570 December 29, 2016 11 / 16
and play partner. In particular, our aim was to evaluate a variety of proposed hypotheses
derived from the literature.
Our results suggest that dog and wolf puppy play bowers, like adult dogs, use play bows as a
visual signals [11,24]. Almost all bows were performed when the dyad was visually attentive to
one another, suggesting that dog and wolf puppy play bowers, like adult dogs, may understand
the context in which it is appropriate to use the visual signal. Moreover, the single play bow in
dog puppies that occurred without visual contact also included an attention-getting behavior
in the form of a bark, providing proof of concept that dog puppies may understand when to
use attention-getting behaviors in association with a bow. Future research should be conducted
to determine the age at which awareness of the partner’s attentional state occurs and
how it develops over time.
No evidence was found in the GLMM to suggest that play bows in dog and wolf puppies
function as a means to clarify easily misinterpretable behaviors. Play bows did not emphasize
playful intent during instances in which the bower’s behaviors were most susceptible to misinterpretation
(Table 8). When behavior categories were analyzed for dog puppies, behaviors
shown after play bows differed by role but in the opposite direction to that expected by Bekoff
[26] results: partners showed offensive behaviors more often after the bow than bowers did,
whereas neither bowers nor partners showed any difference in the proportions of this behavior
category before the bow. For the wolf puppies, when behavior categories were analyzed, no difference
was found as a function of either role or timing. Furthermore, no bite-shakes were
ever observed in either species, and bite behaviors, such as nips and bites, occurred at low
rates. For dog puppies, bowers and partner were equally likely to perform bite behaviors, and
partners rather than bowers were more likely to perform bite behaviors after the bow than
before. However, wolf puppy play bowers performed more bite behaviors than their partners.
Furthermore, bowers and partners were more likely to perform bite behaviors before the bow
than after. Therefore, in a handful of instances, wolf puppy bowers may perform play bows
after bite behaviors, potentially to clarify the misinterpretability of the signal. However, these
results may simply be an effect of the tendency for the wolf puppy play bowers to show more
play activity than their partners did.
These findings contrast with those of Bekoff [26], but it is worth emphasizing that the age of
the subjects observed may be one reason for the differences. The dog and wolf puppies in Bekoff’s
study were all younger than any of those observed in this study (3–7 weeks old compared
to approximately 2–8 months). Bekoff’s dog sample intermixed 3–7 week old puppies with
adult dogs without information on how many observations each accounted for. Without this
information we cannot say how likely it is that differences between Bekoff’s results and ours
Table 8. Summary of evidence for hypotheses 1–5 in wolf puppies, dog puppies, and adult dogs.
Hypothesis Wolf Puppies Dog Puppies Adult Dogs
1: Play bows as visual signals Yes Yes* Yes*
2: Clarification of easily misinterpretable behaviors Maybe No* No*
3a: Attacking the play partner No No* No*
3b Escaping from the play partner Maybe Maybe* Maybe*
4: Re-initiation of play No Yes* Yes*
5: Play bow synchronization No No Yes
Note.–Adult dog results are from Byosiere et al. [24]
“Bold face”–Results consistent across samples
*—Results consistent across young and adult dogs
doi:10.1371/journal.pone.0168570.t008
Investigating the Function of Play Bows in Dog and Wolf Puppies
PLOS ONE | DOI:10.1371/journal.pone.0168570 December 29, 2016 12 / 16
are due to differences in the ages of the wolf and dog puppies in each study, so we simply note
it as a possibility. However, the results reported here are consistent with Byosiere et al. [24],
who found that play bows did not function to clarify easily misinterpretable behaviors in adult
dogs (Table 8).
No support was found to indicate that play bows function st
including continuation of play by enticing the partner into a runaway/chase interaction. However,
while many of our findings are similar across dog and wolf puppies, and consistent with
those observed in adult dogs, species differences may exist. Whether these reflect confounds,
behavioral patterns specific to our sample, or species differences due to domestication requires
further investigation.
Supporting Information
S1 File. Ethogram, behavioral codes, and definitions.
(PDF)
S2 File. GLMM analysis output for both dog and wolf puppies.
(PDF)
S1 Table. Determinants of Visual Signals. The bower and the partner were considered to be
within each other’s field when the majority of the front torso was facing towards the play partner.
Players were considered to be not facing one another when more than half of each individual’s
front torso was facing away from the other.
(PDF)
Acknowledgments
The Wolf Science Center was founded and is run by Kurt Kotrschal, Zso´fia Vira´nyi and Friederike
Range. We are grateful to them for allowing us access to their video database. Specifically
we would like to thank Jenny Essler and Simona Cafazzo for their help in locating and
accessing the relevant video footage analyzed for this project. Marianne Heberlein for her statistical
support. Martina Russignan, Stefanie Heufelder, Anais Racca and Ba´lint Pataky for collecting
and recording the video footage and Karin Bayer, Jennifer Bentlage and Peter Fu¨reder
for logistic support.
Author Contributions
Conceptualization: S-EB JE BS.
Data curation: S-EB JE BS.
Formal analysis: S-EB JE.
Funding acquisition: FR.
Investigation: S-EB JE.
Methodology: S-EB BS.
Project administration: S-EB.
Resources: FR.
Supervision: S-EB BS FR.
Visualization: S-EB JE SM-P BS FR.
Writing – original draft: S-EB JE SM-P BS FR.
Writing – review & editing: S-EB JE SM-P BS FR.
Investigating the Function of Play Bows in Dog and Wolf Puppies
PLOS ONE | DOI:10.1371/journal.pone.0168570 December 29, 2016 14 / 16
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