Reviewer 2
The paper deals with the role of predator-induced fear in regulating
play behavior of juvenile rats. Not only do the juveniles of many
species of mammals engage in play, but juveniles are also more likely
to engage in risk taking behavior more generally (see L. A. Fairbanks
(1993) Risk-taking by juvenile vervet monkeys. Behaviour, 124, 57-72 in
addition to papers already cited). It is likely that such conspicuous
behavior as play would draw the attention of predators. Interestingly,
however, there are few documented cases of juveniles engaging in
antipredator behavior during play to mitigate such risk. One such case
is the loud vocalizations of playing squirrel monkeys, as compared to
the usual low volume tones of playful vocalizations in other species
(S. Kipper & D. Todt (2002). The use of vocal signals in the social
play of Barbary macaques. Primates, 43: 3-17) which induce a state of
alertness in the troops adults (M. Biben & D. Symmes (1986). Play
vocalizations of squirrel monkeys (Saimiri sciurus). Folia
Primatologica, 46: 173-182; M. Biben, D. Symmes & D. Bernhards (1989).
Vigilance during play in squirrel monkeys. American Journal of
Primatology, 17: 41-49).
If play places juveniles at greater danger of predation, you would
predict that they should be sensitive to cues that indicate the
presence of predators. In the present paper, the authors build on a
body of work on adult rats showing various kinds of antipredator
responses to predator odors. Furthermore, it is shown that play is a
sensitive marker for evaluating predator-induced responses in juvenile
rats. To me, two major insights arise from this study. Firstly, it
corroborates earlier work showing that odor cues signifying the
imminent presence of a predator (i.e., fur-derived smells) have a more
profound effect than odor cues indicating a predator had been present
at some time, but not necessarily imminent (i.e., fecal smells).
Secondly, juveniles are not insensitive to the presence of danger when
they play, but rather, will modify their play to reduce predatory risk.
It is known that juveniles are more impulsive than adults, and
the paradigm presented in this paper will serve as a useful model to
compare and
contrast the mechanisms of antipredator behavior in juveniles versus
adults. In
this regard, there are several points in the paper where additional
analyses
could greatly increase this paper's contribution to the characterizing
of the
relevant mechanisms.
A major theoretical issue that arises from the findings is why the cat
odor-induced suppression of play should not be complete. That is, why
play at
all in the context of the imminent threat of a predator? The results
from
several of the experiments show a gradual increase of play over time
following
the initial suppression. One can imagine a different strategy, the
complete
absence of play for some period of time and then a return to normal
levels of
play. Play, even at a lower frequency, could still attract the
attention of a
predator. As all experiments have been videotaped, it would be of value
to
examine whether the overall pattern of behavior is different following
suppression and at various stages of its recovery. For example, when
they play
little, what do they do between play bouts (freeze, explore, risk
assessment,
etc.)? Indeed, are play bouts clustered together in quick succession or
widely
dispersed over the test session? When they do play, is the manner of
play
different when playing at a low frequency versus a higher frequency?
For
instance, in Figure 1, guestimating from the data points, it looks like
at E2
for the suppressed group that nape contacts lead to pins in about 25%
of cases,
whereas by E7, the percentage is around 60% (compared with about 75%
for all
time periods for the control group). Such data would also be very
valuable when
comparing the cat fur odor effects with the fecal odor effects - is the
pattern
of suppression the same between the two cases with the difference being
in
magnitude and duration, or do the rats? patterns of play and activity
differ,
indicating a different mechanism of suppression in these two cases?
Although not
essential for the core aim of this paper, if possible, such data should
be
provided to allow more detailed analyses of the mechanisms involved (at
the
least, a follow-up paper examining these details should be considered
by the
authors).
For experiment 2, it would be useful to know the duration of the test
period
spent in the small escape chamber versus the main test enclosure and
whether the
percentage of play differed between these two locations for the odor
group
versus the control group. Since play is suppressed even when they have
an escape
chamber to which to retreat, again, it raises the question of why play
should
not be completely suppressed for some time following exposure to the
cat odor,
rather than continuing to occur at lower frequencies (see above).
On page 25, second last paragraph, it is concluded that the
impulsiveness and
distractibility of juveniles may lead them to be more attentive to
important
environmental cues. I would have argued the exact opposite. Indeed, the
pattern
of antipredator response in juveniles may need to differ from that of
adults
precisely to counteract their greater impulsiveness and distractibility
(see
final paragraph on page 25).
Reviewer 1
This MS describes a neat series of experiments that document a
surprisingly
long-lasting suppression of play behavior in juvenile rats following
exposure to
cat odor. The data are convincing and impressively robust.
My only notable concern about this project is that the juveniles
being tested
for their reaction to cat odor were already under considerable (and
abnormal)
stress conditions. They were isolate housed which is a considerable
stressor,
especially for highly social juvenile animals, and some of the
juveniles were
further challenged by shipping stress only a couple of days prior to
the onset
of manipulations. Thus I would think that the relatively high basal
stress
level of these animals might have primed them for perhaps a more
intense (and
long-lasting?) stress reaction relative to animals that were not under
a state
of chronic stress prior to the exposure to cat odor. Minimally, there
should
perhaps be some discussion of this issue in the Discussion section to
alert
readers to the possibility that the specific conditions used in this
experiment
may have primed animals to be unusually responsive to cat odor.
I had a few other minor comments/questions about the MS as detailed
below:
Methods: More details about the methods would be useful:
- No information is provided regarding the number of litters
represented in each
experiment or whether the dyads of animals consisted of littermate
pairs. The
wording of "two sets of births" on p.9 is confusing, and could be
interpreted to
suggest that offspring from only 2 litters were used. Hopefully this
was not
the case, given ample evidence that litter should be used as the unit
of
analysis in developmental studies (see Holson & Pearce, 1998).
- Further details of the cat odor stimulus would be useful for someone
attempting to replicate/extend these findings. Were they indoor or
outdoor
cats? Spayed or not? Of what sex?
Were the collar pieces reused
across
sessions? When the authors say that the collar pieces were warmed,
what
temperature was used?
- Length of the odor exposure period should be mentioned prominently in
Exp.1
(first mention of the timing that I noticed was in the intro to Exp.3
on P.12,
although it might have appeared earlier someplace).
Results: The authors sometimes used multiple t-tests for post-hoc
comparisons did they include a bonferroni correction or some other correction for
the use of
such multiple tests?