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Acoustic communication can play an important part in mother-young recognition in many mammals. This, however, has still only been investigated in a small range mainly of herd- or colony-living species. Here we report on the behavioral response of kittens of the domestic cat, a typically solitary carnivore, to playbacks of "greeting chirps" and "meows" from their own versus alien mothers. We found significantly stronger responses to the chirps from kittens' own mother than to her meows or to the chirps or meows of alien mothers. Acoustic analysis revealed greater variation between vocalizations from different mothers than for vocalizations from the same mother. We conclude that chirps emitted by mother cats at the nest represent a specific form of vocal communication with their young, and that kittens learn and respond positively to these and distinguish them from chirps of other mothers and from other cat vocalizations while still in the nest. © 2016 Wiley Periodicals, Inc. Dev Psychobiol 9999: 1-10, 2016.
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Mother–Offspring Recognition
in the Domestic Cat: Kittens
Recognize Their Own Mother’s
Call
ABSTRACT: Acoustic communication can play an important part in mother-
young recognition in many mammals. This, however, has still only been
investigated in a small range mainly of herd- or colony-living species. Here we
report on the behavioral response of kittens of the domestic cat, a typically
solitary carnivore, to playbacks of “greeting chirps” and “meows” from their
own versus alien mothers. We found significantly stronger responses to the chirps
from kittens’ own mother than to her meows or to the chirps or meows of alien
mothers. Acoustic analysis revealed greater variation between vocalizations from
different mothers than for vocalizations from the same mother. We conclude that
chirps emitted by mother cats at the nest represent a specific form of vocal
communication with their young, and that kittens learn and respond positively
to these and distinguish them from chirps of other mothers and from other cat
vocalizations while still in the nest. ß 2016 Wiley Periodicals, Inc. Dev
Psychobiol 9999: 1–10, 2016.
Keywords: vocalization; vocal recognition; mother-offspring communication;
maternal care; domestic cat; Felis silvestris catus; playback;
acoustic analysis
INTRODUCTION
In many mammals it is important for the early survival
of the young that they learn to recognize their own
mother and to distinguish her from other conspecifics.
This is clearly the case and has been best studied in
various herd-living ungulates (Nowak, Porter, L
evy,
Orgeur, & Schaal, 2000) and in colony-living species
such as various pinnipeds and bats (Insley, Phillips, &
Charrier, 2003; Jin et al., 2015, respectively). For the
newborn young of such species the attempt to suckle
from an alien mother, for example, may result not only
in rejection but also in serious injury or even death
(Harcourt, 1992; Le Boeuf, Whiting, & Gantt, 1972;
Trillmich, 1981; Wolski, Houpt, & Aronson, 1980).
Also for the young of more solitary species which are
hidden in nests or dens, it can be vital for their early
survival that they remain quiet at the approach of
predators or potentially infanticidal conspecifics
(Sieber, 1986; Torriani, Vannoni, & McElligott, 2006;
Va
nkov
a, Barto
s, & M
alek, 1997), and only respond
positively with approach to their mother.
Acoustic communication has been found to play an
important part in the recognition by newborn mammals
of their mother in a variety of mammals (Balcombe &
McCracken, 1992; Barfield, Tang-Martı
´
nez, & Trainer,
1994; Briefer & McElligott, 2011; Charrier, Mathevon,
& Jouventin, 2001; Jin et al., 2015; S
ebe, Nowak,
Poindron, & Aubin, 2007; Shillito Walser, 1986;
Trillmich, 1981). However, much of this work has been
done in herd- or colony-living species, with less
Manuscript Received: 11 June 2015
Manuscript Accepted: 14 February 2016
Correspondence to:P
eter Szenczi
Contract grant sponsor: Universidad Nacional Aut
onoma de
M
exico
Contract grant number: DGAPA- IN205513
Contract grant sponsor: Hungarian Academy of Sciences
Contract grant number: MTA 01 031
Contract grant sponsor: Postdoctoral Fellowship Program of the
Universidad Nacional Aut
onoma de M
exico
Article first published online in Wiley Online Library
(wileyonlinelibrary.com).
DOI 10.1002/dev.21402 ß 2016 Wiley Periodicals, Inc.
Developmental Psychobiology
P
eter Szenczi
1
Ox
ana B
anszegi
2
Andrea Urrutia
2
Tam
as Farag
o
3
Robyn Hudson
2
1
Centro Tlaxcala de Biologı
´
adela
Conducta
Universidad Aut
onoma de Tlaxcala
Tlaxcala, Mexico
E-mail: peter.szenczi@gmail.com
2
Instituto de Investigaciones Biom
edicas
Universidad Nacional Aut
onoma de
M
exico
Distrito Federal, Mexico
3
MTA-ELTE Comparative Ethology
Research Group
Budapest, Hungary
information available on other taxonomic groups. This
may be because the need for individual recognition
between mothers and their offspring is less obvious for
solitary than for social species (but see below). It may
also be partly due to the difficulty of observing the
behavior of mothers and young of solitary, more
secretive species, and to the difficulty, exemplified by
carnivores, of experimentally manipulating young often
defended by well-armed mothers or other caretakers.
An exception to such difficulties is presented by the
domestic cat Felis silvestris catus. Cats can be easily
kept and experimented with under semi-natural free-
ranging conditions, and mothers readily permit the
handling and manipulation of newborn young by
familiar caretakers (Hudson, Raihani, Gonz
alez, Bau-
tista, & Distel, 2009 ; Raihani, Gonz
alez, Arteaga, &
Hudson, 2009). In addition, cats have a broad and
complex vocal repertoire, which they also employ in
communicating with their young (Brown, Buchwald,
Johnson, & Mikolich, 1978; Farley, Barlow, Netsell, &
Chmelka, 1992; Moelk, 1944; Scheumann et al., 2012;
Yeon et al., 2011). Although they do not construct nests
or dens, they are adept at hiding their kittens, already
well-furred at birth, in refuges (Feldman, 1993; Pontier
& Natoli, 1999). But as solitary-living obligate carni-
vores, cat mothers must spend considerable time away
from their young to hunt (Bradshaw, Goodwin,
Legrand-Defretin, & Nott, 1996; Martin, 1986), leaving
the young unprotected. During these periods, kittens
are most vulnerable to predators and potentially infanti-
cidal males (MacDonald, Apps, Carr, & Kerby, 1987;
Pontier & Natoli, 1999). Although their age is almost
impossible to determine, remains of cats, sometimes in
large quantities (Bateman & Fleming, 2012) have been
found in feces of several carnivores such as coyotes
(Morey, Gese, & Gehrt, 2007), foxes (Contesse, Heg-
glin, Gloor, Bontadina, & Deplazes, 2004; Kidawa &
Kowalczyk, 2011), and stone martens (T
oth, B
ar
any, &
Szenczi, 2011) in urban and natural environments alike.
The kittens typically remain still and silent when the
mother is absent and at the approach of animals other
than their mother (Haskins, 1977, own observations).
However, as we and others have observed, when
mothers approach the “nest” and while nursing, they
emit a particular soft call referred to in the literature as
a “chirp” and phonetically transcribed as
Iə
mhrn”
(Martin, 1986; Moelk, 1944). Chirps and purrs seem to
be the only vocalizations emitted by mothers at the nest
(own observations).
Although kittens are altricial and are born with
closed eyes and external auditory canals, they rapidly
develop good acoustic abilities. Already by around
postnatal day 5, electrophysiological recordings from
auditory cortex show responses to acoustic stimuli, and
most strongly to those of a naturalistic, biologically
relevant nature (Olmstead & Villablanca, 1980). By
around postnatal week 4 the auditory canals are
completely open and kittens have developed the fine
auditory acuity of the adult (Ehret & Romand, 1981;
Villablanca & Olmstead, 1979). There have, however,
been few studies of mother-young vocal communica-
tion in the cat (Haskins, 1977; Scheumann et al., 2012),
and to our knowledge only one of kittens’ behavioral
responses to mothers’ vocalizations at the nest (Lusche-
kin & Shuleikina, 1989). In that study the authors
investigated the homing efficiency of kittens able to use
visual, olfactory and auditory cues, although there was
not always a clear experimental differentiation between
the kittens’ use of particular types of acoustic or other
sensory stimuli to orient to the nest, nor whether the
acoustic stimuli were from their own or alien mothers.
In the present study it was therefore our aim to
investigate if kittens distinguish between their own
mother’s and alien mothers’ vocalizations at around
postnatal week 4, the age at which they start to leave
the nest. We predicted: 1) that kittens would respond
more strongly with positive behaviors such as approach
to their own mother’s chirps than to a presumably
unknown stimulus, her meows; and 2) that they would
respond more strongly and positively to the chirps of
their own mother compared to the chirps of an alien
mother.
METHODS
Animals
We collected data from 29 kittens of seven litters (average
litter size 4.14 1.8 SD) from three mixed-breed multiparous
females (2, 2, and 3 litters per mother) belonging to an
established breeding colony of cats (four adult females and
two adult males plus other visiting stray males), between May
and December 2014. With the intention of studying animals
in semi-natural conditions, the cats were kept in a private
house with a garden, which they were free to leave at will.
They were fed daily with commercial canned cat food and
fresh meat, and received regular treatment against parasites.
Water, milk, dried cat food and litter trays were always
available. There was sufficient space in the house for each
animal to have its own resting place, and for mothers to raise
their kittens in separate rooms, apart from other mothers and
their young. The doors of the rooms were remodeled to 1.2 m
in height, so that all the adult cats were free to jump in or
out, but the kittens were not able to leave. Mothers showed
little interest in the litters of other females and communal
nursing did not occur.
Mothers always gave birth in the house. A day or so after
delivery, the litters with their mothers were moved to one of
the rooms in a quiet, undisturbed part of the house. Within
2 Szenczi et al. Developmental Psychobiology
the rooms nest sites were provided: a commercial foam cat
bed (oval, 68 57 cm) was placed inside a large cardboard
box (60 80 70 cm). The top of the box was open and a
small floor-level opening (22 27 cm) was cut for the mother.
The box was removed when litters were 28 days old and
began leaving the bed.
Kittens were weighed at birth and daily thereafter to check
for normal growth and to habituate them to human presence and
handling. Each kitten was fitted at birth with a colored neck
ribbon for individual identification. From the 4th week onward,
kittens were fed daily with commercial canned cat food and ad
libitum dry cat food. Water and a litter tray were also provided.
All kittens survived to weaning at approximately 8 weeks
of age, when they were given away as pets with the help of
local veterinarians. As in our previous studies of kitten
behavior (Hudson et al., 2009; Hudson, Rangassamy, Salda
~
na,
B
anszegi, & R
odel, 2015; Raihani et al., 2009; Raihani,
Rodrı
´
guez, Salda
~
na, Guarneros, & Hudson, 2014), animals
were kept and treated according to the guidelines for the care
and use of animals in research of the Instituto de Investiga-
ciones Biom
edicas, Universidad Nacional Aut
onoma de
M
exico, and the National Guide for the Production, Care and
Use of Laboratory Animals, Mexico (Norma Oficial Mex-
icana NOM-062-200-1999).
Procedures
Recording of Vocalizations. For each litter, four kinds of
playback stimuli were used: “chirps” and “meows”, and either
from kittens’ own mother or from alien mothers at the same
lactational phase (Fig. 1 for sample chirp and meow spectro-
grams). Recordings were made in WAV format, using a
unidirectional microphone (Sennheiser ME66, Wedemark,
Germany; frequency range: 40–20,000 Hz) on a stand, con-
nected to a recorder (Tascam DR-40, Montebello CA; 96 kHz
/ 24 bit). Editing was carried out in Audacity 1.2.6, and
stimuli were saved and used in the playbacks in lossless AIFF
format. Recordings were obtained as follows:
“Chirps”. Continuous recordings were made at the nest
when litters reached 3 weeks of age. Recording was carried
out overnight (approx. 23:00–06:00 hr) to minimize back-
ground household and street noise. The microphone was
placed inside the box, 30 cm above the nest and pointing
towards it.
“Meows”. Recordings were made from each mother when a
highly preferred food (raw ground beef) was held above her.
The microphone was held on a boom pole 30 cm away from
the mother.
Playback Stimuli. Individual chirps and meows, when clear
and free of background noise, were cut from the recordings.
Stimuli were prepared by editing together a train of seven
chirps or seven meows, separated from each other by 2 s of
silence and in each test session were repeated twice (
X SE
¼ 36.5 1.7 s, n ¼ 2 7 different vocalizations for each
vocalization type). All of the chirps or meows in one 7-call
stimulus train belonged to the same mother, and to avoid
pseudoreplication each call and train of calls was used for
any of the litters only once. Sound pressure of all stimuli was
normalized to 60 dB measured with a sound pressure meter
(General DSM402SD, New York, NY) at 1 m distance from
the same speaker used in the tests. To ensure that all the
kittens were in the nest and were engaged in some neutral
behavior unrelated to the study (play, grooming), at the
beginning of the playback we included 1 min of pre-playback
video recording. Additionally, we continued video recording
for 1 min after the playback ended.
FIGURE 1 Spectrograms of sample chirps and meows from a single mother. Frequency range
0–10 000 Hz, window length .01 s, dynamic range 50 dB.
Developmental Psychobiology Kittens Recognize Their Own Mother’s Call 3
Experimental Procedure. Each litter was tested twice with
each of the four kinds of stimuli. The tests took place from
10:00–12:00 and 15:00–17:00 hr on four consecutive days,
starting when the kittens were 32–33 days old. The testing
schedule was balanced such that test days were alternated
between chirps (first and third days) and meows (second and
fourth days); the order of the own mothers’ and alien mothers’
vocalizations were played in reversed order the second time.
A40 50 cm screen made of white corrugated plastic was
placed in the litters’ room four days before the start of testing
so that the kittens could habituate to its presence. The screen
was placed between the nest and the door, about 1.5 m from
the nest. Two hours before each experiment the mother was
removed from the room. Playback of stimuli was conducted
in lossless AIFF format using a wireless speaker (SoundLink
1
Mini, Bose Inc., Framingham MA, frequency response 20–
20,000 Hz) connected to a 5th generation iPod
1
(Apple Inc.
Cupertino CA) placed behind the screen. Experimenters
checked that the kittens were awake and in the nest and then
left the room.
Video Recording and Analysis. Experiments were video
recorded (Sony HDR-CX130 camera placed so as to overlook
the test area) in the absence of the experimenter for later
analysis. Using Solomon Coder software (P
eter, 2011), the
following behaviors were scored separately for each kitten
from the video recordings:
Latency and duration of alertness (s). Alertness was
defined as a kitten stopping what it was doing, lifting its
head, pricking up its ears, and/or orienting towards the
stimulus.
Latency to approach the speak er (s). Time taken by a
kitten to approach within a 15-cm radius of the speaker or the
screen.
Time spent near the speaker (s). Time a kitten spent
within a 15-cm radius of the speaker or the screen.
In addition, we calculated the percentage of the kittens
from each litter that approached the speaker: defined as a
kitten within 15 cm of the speaker or screen.
Acoustic Analysis of Chirps and Meows. To t est whether the
chirps and meows in our tests were sufficiently distinctive to
be potentially used by kittens for individual r ecognition of
thei r mothers, the acoustic properties of the chirps and
meows of the thr ee mothers contributing to the stimulus
material were analyzed. Sixty-one good quality recordings of
chirps from 11 bouts (3, 3, and 5 from each mother, at least
5 calls per bout, taken during the periods they were nursing
each of their first tested litters), and 89 meows from 11 bouts
(7, 8, and 4 from each mother, at least 3 calls per bout, taken
during the periods they were nursing each of their li tters)
free of background noise were selected and were analyzed
usin g a custom made PRAAT script (Boersma & Weenink,
2015). The quantified parameters are listed in Supplementary
Material 1.
Data Treatment and Statistical Analysis
All behavioral data were analyzed using Generalized Linear
Mixed Models (GLMM) with nested random effects design.
Unless stated otherwise we used litter averages for the
response variables with a Poisson distribution. We used litters
as the unit of analysis because individual measures from
members of the same litter cannot be considered independent
(Zorrilla, 1997). Call type (chirp/meow) and call identity
(own mother/alien mother) were included as fixed factors, and
litter and mother identities (litter identity nested in mother
identity) were included in the models as random effects.
Where significant factor effects were found we performed
multiple comparisons using Mann–Whitney U-tests with
Bonferroni adjustments as post-hoc tests to identify signifi-
cant differences between groups. Statistical analysis of the
behavioral data was performed using Statsoft STATISTICA
10.0 (2011).
For acou stic an alysi s of the vocalizations we applied
Prin cipal Component Analysis (PCA) with covariance
matrix and Varimax rotation to simplify the set of acoustic
variables. In order to do this we standardized the variables
by transforming them to Z scores and ran the PCA on these
values. For chirps we formed 8 and for meows 9 factor
scales (for detailed str ucture and Chronbach alpha values
see Supplementary Material 2.). We then performed conven-
tional and permuted Discriminant Function Analysis (DFA
and pDFA) to test the acoustic discriminability of the three
mothers’ vocalizations. During the conventional DFA we
applied a forward stepwise method based on Wilk’s lambda
changes to find the subset of factors which best discrimi-
nated between the three individuals. For validation we us ed
leave-one-out cross validation. Finally, as the calls were
obtained from call bouts and so cannot be consid ered as
independent data points, we performed pDFA following the
suggestion of Mundry and Sommer ( 2007) to validate ou r
findings. We used an R script (written and provided by
Roger Mundry) with nested design, where our test factor
was the individua ls, while the ID of bouts from which the
calls originated was used as a fixed factor. We fed the
factor scores best discriminating the individuals based on
the DFA results into the analysis. This pDFA pick ed 100
rand om sel ections from the bouts to balance the sample and
to determine the baseline level of correct classification, and
then it generated 1000 randomly permuted samples and
reran the classification for each. The low numb er of random
samp les (ratio less than .05) with better discriminability
than t he balanced sample showed good validity o f the
discrimination. Again, a cross-validation was performed
with the unused items in the balanced DFA.
RESULTS
Behavioral Response of Kittens to Mothers’
Vocalizations
In all of our models we included the mothers’ and
litters’ (nested in mothers) identities as random factors,
4 Szenczi et al. Developmental Psychobiology
but we found no significant effect of either. Kittens’
latencies to show signs of alertness depended on the
type of stimulus only (GLMM: Call type
Call identity
x
2
¼ 3.17, p ¼ .075; Call type x
2
¼ 7.76, p ¼ .005; Call
Identity x
2
¼ 2.85, p ¼ .091), as they became alert
faster in response to chirps than to meows. Further
types of behavioral responses, however, differed more
clearly depending on the kind of stimulus. During and
after the playbacks of own mother’s chirps, kittens
remained alert significantly longer (GLMM: Call type
-
Call identity x
2
¼ 5.62, p ¼ .018; Call type x
2
¼ 61.3,
p < .00001; Call Identity x
2
¼ 45.6, p < .00001;
Fig. 2A) than with other types of playback. Kittens
were also quicker to approach the speaker (GLMM:
Call type
Call identity x
2
¼ 15.5, p ¼ .00008; Call type
x
2
¼ 13.0, p ¼ .0003; Call Identity x
2
¼ 15.0, p ¼ .0001;
Fig. 2B) and stayed near it for longer than for any other
stimulus type (GLMM: Call type
Call identity
x
2
¼ 2.11, p ¼ .14; Call type x
2
¼ 28.1, p < .00001; Call
Identity x
2
¼ 31.2, p < .00001; Fig. 2C). We also
calculated the percentage of kittens from each litter
that approached the speaker. Figure 2D shows that a
higher proportion of kittens did so during and following
the playback of their own mother’s chirps than when
other types of stimuli were used (GLMM: Call type
-
Call identity x
2
¼ .23, p ¼ .63; Call type x
2
¼ 17.5,
p ¼ .00003; Call Identity x
2
¼ 20.9, p < .00001).
Since there was possibly a social effect, where some
kittens merely imitated their siblings’ responses, we
also compared the data across stimuli of the first kitten
of each litter to show alertness and to go to the speaker.
Latencies of the first kittens to become alert during the
playbacks did not differ for the different vocalizations
(GLMM: Call type
Call identity x
2
¼ 3.41, p ¼ .067;
Call type x
2
¼ .34, p ¼ .55; Call Identity x
2
¼ 3.25,
p ¼ .071), which suggests that they were able to hear
all of them. However, they approached the speaker
significantly sooner during their own mother’s chirps
than during other types of playback (GLMM: Call
type
Call identity x
2
¼ 16.7, p ¼ .00004; Call type
x
2
¼ 16.8, p ¼ .00004; Call Identity x
2
¼ 13.6,
p < .0002).
Acoustic Analysis of Mothers’ Vocalizations
Chirps. The conventional DFA showed that the chirps
of the three mothers were acoustically distinct. For the
best discrimination three factors were included (F2-
Pitch [-ppm, f0mean, f0end, f0max, f0min, f0st], F3-
Pitch change [f0maxpoz, f0mxpozr, f0minpoz,
-f0mnpozr, f0chng], F7-Pitch variability [f0sd, f0range,
ppj]; n ¼ 3 mothers, n ¼ 61 calls, Wilk’s l ¼ .085,
p < .001), and 93.4% of the cases were correctly
classified (cross validated: 90.2%; Fig. 3, left panel).
The pDFA including only the first two factors (due to
the restriction that allows a lower number of variables
than the lowest number of calls within one bout, in this
case 3) showed poorer (51.79%) discriminability but
significantly different from the permuted sample (n ¼ 3
mothers; n ¼ 61 calls, p < .001), supporting the validity
of the conventional DFA.
Meows. In the case of meows the conventional DFA
showed lower but still good discriminability (77.8%;
71.7% cross-validated, Fig. 3, right panel) by three
factor scores (F1-Pitch [f0mean , -ppm, f0min, f0max,
f0st]; F3-Range of Intensity [-cmom, intmin, intmax,
intend]; F6-Call length [call_lenght, ppp, intmaxpoz,
f0minpoz]; n ¼ 3 mothers, n ¼ 89 calls, Wilk’s
l ¼ .367, p < .001). The pDFA was run with the first
two factors again, resulting in lower (23.36%) but still
significant discriminability (n ¼ 3 mothers; n ¼ 89 calls;
p < .05).
DISCUSSION
Returning to the main aim of the study, the results
clearly show that kittens of the domestic cat recognize
and respond to the distinctive chirp vocalizations
emitted by their mother as she approaches the nest and
while she nurses and cleans them inside it. Further-
more, kittens distinguish the chirps of their own from
those of other mothers at an equivalent lactational
(maternal) phase, as well as from the meows of their
own or from alien mothers. This suggests that the
mother’s chirp call may have evolved to have a specific
communicatory function, on the one hand signaling to
the young kittens that her arrival at the nest is not to be
feared, and as they grow older and start to be weaned,
using it to call them to leave the nest and follow her
(Moelk, 1944).
Acoustic analysis suggests that that the chirps of
the individual mothers can be sufficiently distinctive
and sufficiently stable on a range of physical charac-
teristics to represent individu al vocal “signatures (see
also Supplementary Material 2) enabling kittens to
distinguish ch irps of thei r own mother from those of
other females. Nevert heless, we have to admit that the
small sample size m ay exaggerate th is acoustical
distinction and if analyzing a larger number of
mothers’ calls we might observe stronger overlap
among individuals. To more rigorously test this, and
to avoid pseudoreplication (Kroodsma, 1989), each
train of chirps used in the present stu dy compris ed
seven different vocalizations cut from seven different
chirp bouts recorded for each female, and the kittens
were tested with two such trains of independently
Developmental Psychobiology Kittens Recognize Their Own Mother’s Call 5
obtained and constructed material on two separate
occasions. Thus, the kittens indeed seem to have
perceived and to have used inter-individual and not
simply inter-vocalization differences when responding
to their own versus another mother’s chirp s (cf.
Sauv
e, Beauplet, Hammill, & Charrier, 2015). In
addition , the design of the experim ents r equired that
the kittens leave the nest to approach the speaker,
rather than to return to their nest as in the study by
Luschekin and Shuleikina (1989) . T his excluded them
using olfactory, thermal or s patial cues as even much
younger kit tens have been shown to effectively use to
return to their nest (Freeman & Rosenblatt, 1978a,b).
A question arising from the present findings is what
prompts mothers to emit these distinctive calls on
approaching or entering the nest? While we were
recording at nests to obtain material to construct the
playbacks, we consistently found, in agreement with
previous reports (Luschekin & Shuleikina, 1989), that
mothers emit only chirps and purrs at the nest, and not,
for example, meows. Somewhat unexpectedly (but
noting that our sample size of mothers and litters was
FIGURE 2 Kittens were alert for significantly longer during and after the playback of their
own mother’s chirps than after the playback of other vocalizations (A); they approached the
speaker significantly sooner during and after playback of their own mother’s chirps than for other
types of playback (B); they spent significantly longer near the speaker during and after the
playback of their own mother’s chirps than for other types of playback (C); and significantly
more kittens in each litter approached the speaker during and after the playback of their own
mother’s chirps than with other types of playback (D). The data are presented as medians (bold
horizontal lines), upper and lower quartiles (boxes), and minimum and maximum values (dotted
lines). Each circle represents the average value for a litter and these may sometimes overlap.
Letters indicate significant differences as reported by multiple comparisons using Mann-Whitney
U-tests with Bonferroni adjustments following application of Generalized Linear Mixed Models.
Post hoc tests were run only when interaction effects were significant. Details of statistical tests
are given in the text.
6 Szenczi et al. Developmental Psychobiology
rather small), we also found that mothers did not start to
emit chirps until the kittens were around two to three
weeks of age (see also Martin, 1986). At present it is not
clear what stimulated the mothers to start doing this:
signals from the developing kittens such as an increase
in motor activity or an increase in the squeaking
vocalizations we often recorded from them in the nest in
response to their mother’s arrival, or a change in the
mothers’ hormonal and motivational state across lacta-
tion, or both? Here cross-fostering studies might help
provide an answer, for example, by investigating
whether chirping is delayed in mothers given younger
foster litters, or advanced in mothers given older litters.
The present findings also raise questions as to when
and how the kittens learn to recognize and respond to
their own mother’s distinctive chirps. Apparently they
do not do so prenatally (cf. Moon & Fifer, 2001) as they
should then also have responded to their mother’s
apparently similarly complex, distinctive and frequently
emitted meows. Furthermore, they would not be able to
learn their mother’s chirps until around the second or
third postnatal week, when as mentioned above, mothers
first start to emit these at the nest. This is consistent with
reports that the auditory canals are almost completely
open and that kittens have good auditory function by
this age, and virtually mature function by the age of one
month when we started to test them (Ehret & Romand,
1981; Olmstead & Villablanca, 1980).
It is certainly not difficult to imagine how kittens
could learn to respond positively to these calls via
pairing with food, warmth and licking provided by the
mother. Nevertheless, the ability of kittens to learn such
fine distinctions so early demonstrates their consider-
able cognitive abilities. It also raises the question
whether they might be pre-adapted to learning chirps,
and/or whether these vocalizations have specific quali-
ties particularly co-adapted to the kittens’ developing
auditory system? This could be addressed by presenting
kittens at the time of the mother’s presence at the nest
with chirps acoustically modified in specific ways, with
other cat vocalizations (for example meows), calls of
other species, or even non-biological acoustic stimuli.
FIGURE 3 Vocal individuality in calls based on the first two canonical discriminant functions
from the conventional DFAs. The data points represent individual calls of the three mothers. In
the case of Chirps (left panel), Function 1 contained the Pitch factor with the highest loading
(F2: 0.948), and was also moderately affected by the Pitch variability factor (F7: 0.547), while
Function 2 was mainly affected by the Pitch change factor (F3: 0.855). The centroids (mean
discriminant score of group) of Mothers 1 and 2 were close to each other, suggesting that their
voices were more similar, but they were still distinguishable by the cross validation (87% of the
two mothers’ calls correctly assigned). In the case of Meows (right panel), Function 1 contained
the Pitch and the Intensity range factors with the highest loading (F1: 0.842; F3: 0.739), while
Function 2 was mainly affected by Call length (F6: 0,737). The centroids (mean discriminant
score of group) of Mothers 1 and 2 were close to each other, suggesting that their voices were
more similar, but that they were still distinguishable by the cross validation (72% of Mother 2’s
calls and 67% of Mother 1’s calls were correctly classified). Details of statistical analysis are
given in the text.
Developmental Psychobiology Kittens Recognize Their Own Mother’s Call 7
Such experiments could also help decide how early
kittens can learn such stimuli by presenting them before
mothers start to emit chirps, thereby providing a means
of investigating kittens’ early sensory and cognitive
abilities. From previous studies it is already known that
kittens are able to learn to identify their own nipple(s)
in the litter’s “teat order”, presumably using olfactory
cues, within a few hours of birth (Hudson et al., 2009;
Raihani et al., 2009).
Returning to the observation in the Introduction that
most studies of mammalian mother-young acoustic
communication have been conducted in herd- or colony-
living species, the present study provides convincing
evidence that the young of species as solitary in the wild
state as the cat Felis silvestris catus may also learn to
recognize a distinctive call of their mother and to
distinguish it from equivalent vocalizations of other
mothers. Whether this has a functional significance for
cats later in life, for example when kittens leave the nest
to follow their mother on hunting forays, remains to be
investigated. Also remaining to be investigated is
whether, as in some other mammals, acoustic communi-
cation between mother and young in the cat is bi-
directional, that is, if mothers also learn to distinguish
the vocalizations of their own from those of alien kittens
(e.g., separation calls; Hudson et al., 2015). The
directionality of mother-young vocal recognition is
shaped by the ecological and social environment of the
species. In cases where selection pressure is high for
both parties to recognize each other, as in colonial or
herd-living species, usually mutual recognition is found
(Espmark, 1971; Insley, 2000; McCulloch & Boness,
2000; M
uller & Manser, 2008; S
ebe et al., 2007).
Theory suggests that in species where the mother hides
her offspring and the young should reveal their exact
location only to her, while she uses other, spatial and
olfactory cues to locate them, only the young are
responsible for mother-offspring acoustic recognition
(Briefer & McElligott, 2011; Sieber, 1986; Torriani
et al., 2006; Va
nkov
a & Malek, 1997), and as is reflected
in the distinctive vocal signature of individual mothers.
NOTES
We thank Karl-Heinz Esser for valuable advice on the
recording and analysis of vocalizations and Carolina Rojas
for excellent technical and bibliographical assistance.
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10 Szenczi et al. Developmental Psychobiology
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... Such behavior may be influenced by various factors, including too early separation from the dam and siblings. Young kittens should stay together with their dam in a family unit until about 12 weeks of age (Senczi et al. 2016). Living in a group, kittens are able to acquire skills useful in the future during hunting and social interactions (Crowell--Davis 2007). ...
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... Here we propose the domestic cat (Felis silvestris catus) as a model species to study mother-young olfactory communication in a carnivore evolved from a solitary-living ancestor (Felis silvestris lybica). Cats can be kept and experimented with under semi-natural free-ranging conditions, and mothers readily permit the handling and manipulation of newborn young by familiar caretakers (Hudson et al. 2009;Szenczi et al. 2016), thereby providing an exception to the difficulties in observing and conducting research with solitary carnivores. Although cats do not construct nests or dens, they are adept at hiding their kittens in refuges (referred to here as ''nests'') providing protection from weather, predators and potentially infanticidal males (MacDonald et al. 1987;Pontier and Natoli 1999). ...
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Two vocalizations, utilized by raccoon (Procyon lotor) mothers ("chitter") and their dependent cubs ("whistle") to establish and maintain contact among each other, are studied in captive groups containing a total of 6 mothers and their 23 cubs. The paper describes frequency of occurrence of the calls, contexts of the callers, individual variation in the call&apos;s structure and the responses of the callees both in uncontrolled situations and in playback experiments. Maternal chitters are most frequently used during the month following the first excursion of the cubs from the litter den by females approaching the cubs or leading them to the food. The frequency of whistling in cubs is high during the nestling period and decrease when they become mobile. The main context of whistling in the cub-mother relationship is answering maternal chitters. Mobile cubs follow their chittering mother silently. The chitters of 4 females differ individually, the main distinctive feature being frequency and pulse rate. The whistles of 12 cubs are individually distinctive, too; duration and frequency measures differ most between individuals. Hence, mothers and cubs have the potential for individual acoustic identification. Seven-week-old nestlings, tested in an experimental arena with successive playbacks, answered maternal chitters on average more often and faster than alien ones, warning grunts or a noise. Mobile cubs approached maternal chitters more often when tested in simultaneous playback experiments. Only 2 of 6 females, however, confronted with whistle-playbacks of their own vs alien cubs in their cages, responded more strongly to calls of their offspring. Results indicate that raccoons may be capable of recognizing family members by acoustic cues alone on a familiar vs strange basis. Advantages of using vocalizations in mother-young relationship and of the potential for acoustic identification and recognition in a solitary mammal are discussed.
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In Arctocephalus galapagoensis and Zalophus californianus wollebaeki, high calling activity and intensive interactions of mother and pup immediately after birth establish recognition within the first few hours (mother) or days (pup) of birth. Females of both species nurse exclusively their own young and reject strange ones, sometimes aggressively. The prompt reactions of pups to their mothers' Pup Attraction Calls (PACs) suggest that the mother too is individually recognized. Interindividual variability of calls provides a sufficient basis for individual recognition in both species. Pups (10 days to 2 yr old) can discriminate between their mothers' and strange females' PACs. Only by means of individual recognition can females in crowded otariid rookeries limit maternal investment to their own offspring. -from Author Arctocephalus galapagoensis Zalophus californianus wollebaeki