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The period before pups are weaned represents a key developmental stage for canids that is directly related to the survivability of the pack. Yet our understanding of the role of the parents during this period when pups are confined to a den is rather limited. We sought further insight into this period by observing diurnal patterns of pre-weaning den visits and nursing behaviour in a captive population of dingoes (Canis dingo). We continuously video-monitored behaviour at dens of four captive, genetically pure, dingo pairs (one litter each) during the first three postpartum weeks just before the start of weaning. Mothers occupied the den almost continuously during the night, but significantly less so during the day, and consistently spent most den time nursing. Fathers were largely absent from inside the den despite lack of apparent aggression from females, low outside temperatures, and space for them inside. They spent a large percentage of time on top of the den, suggestive of sentinel duty, although further experiments are necessary to substantiate this. Although limited to captive animals, our observations are consistent with scant reports of bi-parental care in wild dingoes and with suggestions in the literature that reduced parental care in household and free-ranging domestic dogs might be, at least partly, due to the weakening of bi-parental care during their long history of close association with and dependence on humans.
Content may be subject to copyright.
Please
cite
this
article
in
press
as:
Hudson,
R.,
et
al.,
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo).
Mammal.
Biol.
(2018),
https://doi.org/10.1016/j.mambio.2018.07.002
ARTICLE IN PRESS
G Model
MAMBIO-41031;
No.
of
Pages
6
Mammalian
Biology
xxx
(2018)
xxx–xxx
Contents
lists
available
at
ScienceDirect
Mammalian
Biology
jou
rn
al
hom
epage:
www.elsevier.com/locate/mambio
Short
communication
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo)
Robyn
Hudsona,,
Heiko
G.
Rödelb,
Marise
T.
Elizaldea,
Gerard
A.
Kennedyc,
Bradley
P.
Smithd,
aInstituto
de
Investigaciones
Biomédicas,
Universidad
Nacional
Autónoma
de
México,
Ciudad
Universitaria,
CP
04510,
CDMX,
Mexico
bLaboratoire
d’Ethologie
Expérimentale
et
Comparée
EA4443,
Université
Paris
13,
Sorbonne
Paris
Cité,
Villetaneuse,
France
cSchool
of
Health
and
Biomedical
Sciences,
College
of
Science,
Engineering
and
Health,
RMIT
University,
P.O.
Box
71,
Bundoora,
Victoria,
Australia
dAppleton
Institute,
Central
Queensland
University,
44
Greenhill
Road,
Wayville,
South
Australia
5034,
Australia
a
r
t
i
c
l
e
i
n
f
o
Article
history:
Received
30
January
2018
Accepted
3
July
2018
Available
online
xxx
Handled
by
Sabine
Begall
Keywords:
Canis
lupus
Den
attendance
Parental
care
Suckling
Wild
dog
a
b
s
t
r
a
c
t
The
period
before
pups
are
weaned
represents
a
key
developmental
stage
for
canids
that
is
directly
related
to
the
survivability
of
the
pack.
Yet
our
understanding
of
the
role
of
the
parents
during
this
period
when
pups
are
confined
to
a
den
is
rather
limited.
We
sought
further
insight
into
this
period
by
observing
diurnal
patterns
of
pre-weaning
den
visits
and
nursing
behaviour
in
a
captive
population
of
dingoes
(Canis
dingo).
We
continuously
video-monitored
behaviour
at
dens
of
four
captive,
genetically
pure,
dingo
pairs
(one
litter
each)
during
the
first
three
postpartum
weeks
just
before
the
start
of
weaning.
Mothers
occupied
the
den
almost
continuously
during
the
night,
but
significantly
less
so
during
the
day,
and
consistently
spent
most
den
time
nursing.
Fathers
were
largely
absent
from
inside
the
den
despite
lack
of
apparent
aggression
from
females,
low
outside
temperatures,
and
space
for
them
inside.
They
spent
a
large
percentage
of
time
on
top
of
the
den,
suggestive
of
sentinel
duty,
although
further
experiments
are
necessary
to
substantiate
this.
Although
limited
to
captive
animals,
our
observations
are
consistent
with
scant
reports
of
bi-parental
care
in
wild
dingoes
and
with
suggestions
in
the
literature
that
reduced
parental
care
in
household
and
free-ranging
domestic
dogs
might
be,
at
least
partly,
due
to
the
weakening
of
bi-parental
care
during
their
long
history
of
close
association
with
and
dependence
on
humans.
©
2018
Deutsche
Gesellschaft
f¨
ur
S¨
augetierkunde.
Published
by
Elsevier
GmbH.
All
rights
reserved.
There
is
still
little
detailed
information
on
early
parental
care
in
canids,
particularly
during
the
pre-weaning
period
when
the
young
are
completely
dependent
on
the
mother’s
milk
(Arteaga
et
al.,
2013;
Hudson
et
al.,
2016).
This
is
even
the
case
for
the
grey
wolf
(Canis
lupus),
arguably
the
best
studied
of
the
wild
canids
in
this
regard
(see
Packard,
2003,
and
references
therein).
Most
of
what
is
known
comes
largely
from
anecdotal
observations
in
the
field,
or
from
studies
in
captivity
of
both
wild
and
domestic
canids
(Lord
et
al.,
2013).
The
most
notable
gaps
relating
to
parental
care
exist
in
relation
to
the
presence
of
the
male
and
female
at
den
sites,
nurs-
ing
schedules,
and
the
temporal
organisation
of
parental
behaviour
across
the
24-h
day.
This
is
understandable
given
that
before
the
start
of
weaning
at
around
four
weeks
of
age
the
young
are
typi-
cally
confined
to
an
underground
den,
difficult
for
human
observers
to
access
and
where
disturbance
might
result
in
changes
in
the
Corresponding
authors.
E-mail
addresses:
rhudson@biomedicas.unam.mx
(R.
Hudson),
b.p.smith@cqu.edu.au
(B.P.
Smith).
behaviour
of
the
parents
and
even
in
them
relocating
or
abandoning
the
young
(e.g.,
Thomson,
1992a;
Smith
and
Vague,
2017).
Free-ranging
domestic
dogs
appear
to
differ
notably
from
wild
canids
in
relation
to
characteristics
and
frequency
of
reproductive
activity
(e.g.,
less
marked
seasonality,
earlier
age
of
first
repro-
duction,
greater
frequency
of
oestrus,
less
marked
pair
bonding)
and
parental
feeding
(e.g.,
poor
nursing,
failure
of
male
or
other
pack
members
to
provision
the
mother
and
young)
(Boitani
et
al.,
1995;
review
by
Lord
et
al.,
2013).
These
differences
are
thought
to
reflect
the
domestic
dog’s
adaptation
to
the
human
niche,
and
ready
access
to
associated
resources
relaxing
the
selection
pressure
for
extended
and
biparental
care.
Investigating
the
patterns
and
function
of
parental
care
across
canid
species
(or
subspecies)
may
help
identify
commonalities
across
the
genus
and
provide
insight
into
the
impact
of
domestication
and
feralisation
on
parental
care.
Comparative
information
on
early
parent-young
relations
is
funda-
mental
to
developing
a
fuller
understanding
of
canid
biology
(Lord
et
al.,
2013),
as
well
as
of
the
reproductive
success
of
pairs
and
packs
(Benson
et
al.,
2013;
Fuller
et
al.,
2003).
In
turn,
knowledge
of
parental
care
can
assist
in
the
conservation
and
captive
manage-
https://doi.org/10.1016/j.mambio.2018.07.002
1616-5047/©
2018
Deutsche
Gesellschaft
f¨
ur
S¨
augetierkunde.
Published
by
Elsevier
GmbH.
All
rights
reserved.
Please
cite
this
article
in
press
as:
Hudson,
R.,
et
al.,
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo).
Mammal.
Biol.
(2018),
https://doi.org/10.1016/j.mambio.2018.07.002
ARTICLE IN PRESS
G Model
MAMBIO-41031;
No.
of
Pages
6
2
R.
Hudson
et
al.
/
Mammalian
Biology
xxx
(2018)
xxx–xxx
ment
of
wild
canids
(Smith
and
Watson,
2015),
and
provide
insight
into
the
influence
of
domestication
on
canid
parental
behaviour.
With
the
aim
of
extending
our
knowledge
of
parental
care
dur-
ing
the
pre-weaning
period
in
the
genus
Canis,
we
focus
here
on
the
dingo
(Canis
dingo
-
but
also
referred
to
as
Canis
lupus
dingo,
Canis
familiaris
dingo
or
simply
as
Canis
familiaris;
Crowther
et
al.,
2014;
Jackson
et
al.,
2017),
a
free-ranging
canid
endemic
to
Australia
(Smith,
2015a).
The
dingo
provides
a
unique
comparative
oppor-
tunity
to
investigate
the
impact
of
domestication
on
dog
evolution
under
natural
selection.
Although
sharing
a
genetic
lineage
with
dogs
(Ardalan
et
al.,
2012;
Oskarsson
et
al.,
2011;
Sacks
et
al.,
2013;
Savolainen
et
al.,
2004),
the
dingo
has
been
a
wild-living
canid
on
a
continent
geographically
isolated
from
other
canids
(including
dog
or
wolf
lineages),
and
independent
from
humans
for
at
least
5000
years
until
the
arrival
of
the
British
and
their
dogs
in
1788
(Cairns
and
Wilton,
2016;
Cairns
et
al.,
2017;
Smith
and
Litchfield,
2009;
Smith,
2015a).
Reports
directly
relating
to
dingo
reproductive,
parental
and
denning
behaviour
are
scant,
with
most
restricted
to
anecdotal
observations
(e.g.,
Corbett
and
Newsome,
1975;
Harden,
1981;
Jones
and
Stevens,
1988;
Thomson,
1992a;
Smith
and
Vague,
2017),
or
conducted
with
captive
populations
(e.g.,
Breckwoldt,
1988;
Corbett,
1988;
Hudson
et
al.,
2016).
Like
most
wild
canids
(Lord
et
al.,
2013),
male
and
female
din-
goes
exhibit
long-term
pair
bonding,
maintain
and
defend
a
shared
territory,
cooperatively
care
for
the
young,
and
reproduce
season-
ally
(Corbett
and
Newsome,
1975;
Thomson,
1992a,b,c;
Corbett,
2001;
Lord
et
al.,
2013;
Smith,
2015a).
Dingo
pups
are
generally
born
in
dens
in
the
winter
months
(June
to
August),
which
coin-
cides
with
the
period
best
suited
for
rearing
young
(Smith,
2015b).
Litter
size
varies
according
to
seasonal
conditions
and
with
the
con-
dition
and
past
experience
of
the
mother.
The
average
litter
size
is
four
to
five
pups,
with
a
possible
range
of
one
to
10
(Catling
et
al.,
1992;
Corbett
and
Newsome,
1975;
Corbett,
2001;
Jones
and
Stevens,
1988).
Choice
of
den
sites
is
generally
similar
to
that
of
other
wild
canids
including
preference
for
elevated
sites
provid-
ing
extensive
views
of
lower
approaches,
close
to
water,
and
with
the
den
opening
positioned
so
as
to
offer
maximum
protection
from
the
weather.
Site
selection
varies
according
to
food
resources
and
habitat,
and
can
include
hollow
logs,
enlarged
rabbit
warrens,
rock
piles,
or
under
trees
or
tussocks
(Smith
and
Vague,
2017;
Thomson,
1992a).
Alloparental
behaviour
has
been
identified
in
both
wild
(Corbett
and
Newsome,
1975;
Corbett,
2001;
Thomson,
1992a)
and
captive
dingoes
(Corbett,
1988),
beginning
at
15
days
postpartum
(Breckwoldt,
1988).
Communal
denning
has
also
been
observed
in
locations
where
resources
are
abundant
(Smith
and
Vague,
2017).
However,
it
is
clear
that
specific
parental
behaviours
(e.g.,
the
role
of
the
father,
diurnal
patterns
of
care)
are
not
well
understood
for
most
wild
canids
including
the
dingo
(see
Lord
et
al.,
2013),
and
particularly
during
the
first
three
postnatal
weeks,
which
occur
underground
and
so
out
of
human
sight.
In
this
paper
we
describe
the
pattern
of
parental
care
in
reproductive
pairs
of
captive
dingoes
based
on
continuous
24-h
monitoring
of
the
behaviour
of
parents
and
pups
within
the
den
during
the
first
three
postnatal
weeks,
that
is,
just
before
the
start
of
weaning.
Although
our
study
has
the
limitation
of
being
con-
ducted
with
captive
animals
kept
in
single
pairs,
the
results
might
provide
a
useful
starting
point
for
further
work
under
the
hugely
more
difficult
conditions
in
nature.
We
expected
dingoes’
pat-
tern
of
early
parental
care
to
reflect
that
observed
in
wild
canids
(e.g.
wolves)
given
their
long
separation
from
cohabitation
with
humans
and
similarity
to
wild
canids
in
other
aspects
of
reproduc-
tion
rather
than
to
dogs
(reviewed
by
Lord
et
al.,
2013).
Specifically,
we
expected
greater
participation
of
fathers
as
reflected
by
greater
den
attendance
than
appears
to
be
the
case
in
free-ranging
domes-
tic
dogs.
Methods
have
been
published
in
detail
in
a
previous
study
(Hudson
et
al.,
2016)
from
which
the
present,
completely
new
data
are
drawn.
Four
pairs
of
dingoes
and
their
litters,
born
in
May/June
2013,
contributed
to
the
study
(Table
1).
Parents
were
captive
born
from
wild-caught
animals
and
raised
at
the
Dingo
Discovery
Centre
(-37.565184
S,
144.566024
E),
a
private
facility
located
in
Victoria,
Australia,
where
the
present
study
was
conducted.
All
wild-caught
animals
had
passed
an
analysis
of
genetic
purity
conducted
by
the
University
of
New
South
Wales,
Australia
(Wilton,
2001).
The
breeding
pairs
were
housed
in
pens
(9
×
1.5
m
=
13.5
m2)
compris-
ing
10.5
m2of
gravel
flooring
and
3
m2of
concrete
flooring
where
a
wooden
den
box
(94
×
63.5
×
86
(high)
cm,
with
a
36
×
46
cm
open-
ing
at
the
top
of
the
long
side)
was
located
(Fig.
1;
see
video
clip
in
Supplementary
material).
Shredded
paper
was
placed
inside
the
den
and
was
replaced
daily
or
as
required.
Once
the
pups
were
able
to
walk
and
to
independently
leave
the
den
(at
approximately
20
days
of
age)
the
box
was
inverted
so
they
could
readily
leave
it.
A
corrugated
iron
roof
covered
2
m
of
the
pen
above
the
concrete
section,
and
the
remaining
roof
was
covered
with
wire
mesh
to
prevent
escape.
The
walls
of
the
pens
were
2
m
high,
of
wire
mesh,
with
the
addition
of
1.2
m
high
floor-level
sheets
of
corrugated
iron
to
act
as
windbreaks
and
to
prevent
fighting
between
neighbours.
Observations
were
made
from
May
to
June
2013
during
the
South-
ern
Hemisphere
winter,
which
is
the
normal,
once-yearly
breeding
period
for
dingoes
(Lord
et
al.,
2013;
Smith,
2015b).
The
parents
were
accustomed
to
human
presence
and
handling
and
appeared
well
adjusted
to
the
study
conditions.
In
general,
adult
dingoes
were
fed
a
combination
of
dry
dog
food
and
fresh
chicken
(carcass
or
ground
carcass
mince)
each
morning
(between
0900
and
1200
h).
However,
starting
14
days
before
whelping,
the
mothers
were
also
fed
in
the
evening
(between
1600
and
1800
h).
This
continued
until
the
pups
started
to
leave
the
den
at
approx-
imately
21
days
of
age
and
to
eat
semi-solid
food,
by
which
time
their
teeth
had
fully
erupted.
The
pens
and
dens
were
also
cleaned
daily
during
the
morning
feed.
The
evening
feed
marked
the
time
when
human
activity
in
the
vicinity
of
the
dingo
facility
ceased
for
the
day.
During
the
study
period
direct
contact
with
the
ani-
mals
was
restricted
to
two
regular
members
of
staff.
This
included
handling
the
pups
for
health
checks
and
weighing
(Crofton
kitchen
scales,
limit
4
kg,
resolution
1
g)
at
birth
and
then
on
average
every
third
day
(see
Table
1
for
birth
weights).
Visits
to
the
sanctuary
were
restricted
until
the
pups
had
been
weaned
and
transferred
to
communal
enclosures
for
juveniles.
For
further
details
on
the
management
of
dingoes
at
the
sanctuary
see
Smith
and
Watson
(2015).
Behaviour
within
the
dens
was
recorded
continuously
using
a
small
day/night
surveillance
camera
(1/3”
SwannTruColor
image
sensor,
728
×
488
pixels;
Swann
Pro
530,
Swann
Communications)
that
provided
a
good
overview
of
the
interior
(Fig.
1a,
b),
and
a
digital
video
recorder
(Swann
4
channel
DVR,
model
DVR4-4000,
Swann
Communications).
Recordings
were
made
at
a
frame
rate
of
20
fps,
and
a
maximum
bit
rate
of
1024
kbps,
in
colour
during
the
day
and
switched
to
black
and
white
at
night
using
infra-red
LED
(minimum
illumination
0
lx
with
infra
red
activated).
The
cameras
were
installed
in
a
top
corner
of
each
of
the
four
dens
at
least
24
h
prior
to
birth.
Recording
began
at
this
time
and
ceased
when
the
pups
started
to
leave
the
den,
or
at
21
days,
whatever
occurred
first.
For
behavioural
analysis
we
used
the
two
most
complete
24-h
records
per
week
(i.e.,
six
24-h
records
for
each
parental
pair).
This
selection
was
necessary
due
to
lost
footage
from
power
outages
and
destruction
of
cameras
by
the
dingoes,
and
resulted
in
a
total
sam-
ple
of
576
h
of
observation.
The
main
behaviours
scored
were
the
frequency
and
time
spent
by
each
parent
in
the
den
and
the
time
mothers
spent
nursing.
This
was
defined
as
the
time
during
which
at
least
one
pup
was
attached
to
a
nipple
but
without
implying
milk
ingestion.
Behaviours
were
scored
per
second
but
for
the
analyses
Please
cite
this
article
in
press
as:
Hudson,
R.,
et
al.,
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo).
Mammal.
Biol.
(2018),
https://doi.org/10.1016/j.mambio.2018.07.002
ARTICLE IN PRESS
G Model
MAMBIO-41031;
No.
of
Pages
6
R.
Hudson
et
al.
/
Mammalian
Biology
xxx
(2018)
xxx–xxx
3
Table
1
Details
of
the
parents
and
litters
of
this
study.
Birth
weights
were
taken
within
48
h
of
birth.
Parents
were
born
at
the
Dingo
Discovery
Centre
from
genetically
pure
wild-caught
animals.
Mother
Age
(years)
Parity Father
Date
of
birth
Litter
size Sex Weight
at
birth
(g)
Natal
deaths
Post
natal
deaths
Final
litter
size
M
F
Amelia
2
0
Wallace
9-5-13
5
2
3
M:
344,
331
F:
324,
311,
288
0
0
5
Petal
5
0
Bingo
17-5-13
6
4
2
M:
358,
350,
322,
310,
F:
334,
292
0
0
6
Freckle
8
2
Sterling
24-5-13
6
2
4
M:
368,
311
F:
366,
360,
337,
250a
0
1a5
Opal
7
3
Teddy
1-6-13
7
3
2
M:
391,
391,
375,
356b
F:
304,
284
0
2b5
aOn
day
3
one
pup
went
missing.
Cause
unknown.
bTwo
dingo
pups
euthanized
by
DDC
staff
at
birth.
The
details
of
the
second
euthanized
pup
are
unknown.
Fig.
1.
View
inside
a
den
box
with
a
nursing
mother
during
the
first
(a)
and
third
(b)
postnatal
week,
and
of
the
dingo
enclosure
with
the
father
on
top
of
the
den
(c).
Images
are
screen
shots
taken
from
actual
footage.
(see
below)
data
were
collapsed
into
1-hour
bins
(see
Supplemen-
tary
material
for
a
video
clip
of
the
behaviour
of
a
mother
and
her
week-old
pups
in
the
den).
External
ambient
air
temperature
and
temperature
in
the
den
were
continuously
monitored
and
recorded
in
5
min
intervals
using
temperature
data
loggers
(HOBO
Pendant®Temperature/Alarm
Data
Logger
64
K,
model
UA-001-64;
measurement
range
20
to
70 C;
resolution
0.14 C
at
25 C).
Loggers
were
attached
to
the
ceiling
of
the
far
left
corner
of
the
den
away
from
the
entrance,
and
to
the
outside
of
the
den
at
the
same
height
on
the
side
clos-
est
to
the
enclosure
wall.
During
the
study
period
the
temperature
outside
the
dens
during
the
day
(0700–1800
h)
was
mean
13.03 C,
0.06
SE,
range
6.06–24.64,
and
during
the
night
(1800–0700
h)
was
mean
11.26 C,
0.05
SE,
range
5.96–22.33.
The
temperature
inside
the
dens
during
the
light
phase
was
mean
14.50 C,
0.06
SE,
range
6.98–26.19,
and
during
the
dark
phase
was
mean
12.64 C,
0.05
SE,
range
6.98–23.87.
Wilcoxon
signed-rank
tests
reported
that
during
both
the
day
and
night,
temperatures
inside
the
dens
were
signif-
icantly
higher
than
external
temperatures
(Z
=
47.78,
P
<
0.001)
and
Z
=
49.65,
P
<
0.001,
respectively).
Mothers
gave
birth
with
no
natal
deaths,
raised
their
young
to
weaning
without
apparent
difficulty,
and
allowed
observation
and
manipulation
of
their
pups
by
sanctuary
staff
without
protest.
After
weaning
at
around
10–12
weeks
of
age
pups
were
sold
as
pets
or
to
zoos
or
fauna
parks.
Methods
were
approved
by
the
Central
Queensland
University
Animal
Ethics
Committee,
project
number
A12/11-293.
Statistical
analyses
were
done
with
R,
version
3.3.2
(R
Core
Team,
2016).
We
applied
generalized
linear
mixed-effects
models
(GLMM)
for
proportional
data,
using
a
model
structure
for
bino-
mial
distribution
with
a
logit
link.
Thus,
for
analysis,
the
different
response
variables
(mother’s
presence
in
den
in
min/h
and
mother’s
nursing
activity
in
%
time)
were
transformed
into
proportions.
Cal-
culations
were
based
on
Laplacian
maximum
likelihood
estimates
using
the
package
lme4
(Bates
et
al.,
2015).
P-values
were
calcu-
lated
by
Wald
Chi-square
tests.
Analyses
were
based
on
repeated
measurements
of
the
four
parental
pairs
across
the
first
three
post-
partum
weeks,
with
two
full
days
of
sampling
per
week
and
pair
(see
above
for
details).
Data
were
analyzed
on
an
hourly
basis,
either
as
min/h
(for
the
response
variables
‘time
spent
by
mothers
in
the
den’
and
‘time
spent
by
fathers
in
the
den’)
or
as
%
observation
time
(for
the
response
variable
‘%
time
in
the
den
mothers
spent
nursing’).
For
each
of
the
three
response
variables
given
above
we
ran
a
statistical
model
considering
week
as
a
factor
with
three
levels
and
photoperiod
as
a
factor
with
two
levels
(day
and
night).
The
daily
photoperiod
was
determined
based
on
the
start
and
end
of
civil
twilight
at
the
study
site
(Melbourne,
Australia)
during
early
May
to
early
June
2013
using
information
available
at
www.timeanddate.
com/sun.
Based
on
averages
across
the
observation
days,
the
start
of
daylight
was
defined
as
0655
h
and
the
start
of
night
as
1738
h.
To
account
for
repeated
measurements
we
included
the
identity
of
the
parental
pair
and
the
postpartum
day
of
sampling
as
random
factors.
We
also
included
an
observation-level
random
factor
to
account
for
over-dispersion
of
our
models
(Browne
et
al.,
2005).
Mothers
spent
on
average
1131.2
min
per
24
h
period
(±19.5
SE)
in
the
den
during
the
first
three
postpartum
weeks;
significantly
more
and
around
10-fold
the
mean
time
fathers
spent
in
the
den
(values
for
fathers
see
below;
x2
1=
291.53,
P
<
0.001).
Mothers’
time
in
the
den
showed
a
clear
diurnal
pattern;
whereas
they
remained
almost
continuously
in
the
den
during
the
night
they
spent
sig-
nificantly
less
time
there
during
the
day
(x2
1=
439.31,
P
<
0.001;
Fig.
2a–c).
The
time
they
spent
in
the
den
during
the
night
did
not
differ
significantly
between
weeks
1,
2
and
3
(P
>
0.30
for
all
pair-
wise
comparisons),
but
during
the
day
mothers
spent
significantly
more
time
in
the
den
during
the
first
postpartum
week
(mean
40.2
min/h
±
1.9
SE)
compared
to
the
second
week
(mean
32.1
min/h
±
2.2
SE;
x2
1=
8.73,
P
=
0.003),
and
to
the
third
week
(mean
26.5
min/h
Please
cite
this
article
in
press
as:
Hudson,
R.,
et
al.,
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo).
Mammal.
Biol.
(2018),
https://doi.org/10.1016/j.mambio.2018.07.002
ARTICLE IN PRESS
G Model
MAMBIO-41031;
No.
of
Pages
6
4
R.
Hudson
et
al.
/
Mammalian
Biology
xxx
(2018)
xxx–xxx
Fig.
2.
Pattern
across
the
day
of
mothers’
presence
in
the
den
(a–c)
and
percentage
time
mothers
spent
nursing
while
in
the
den
(d–f)
during
postpartum
weeks
1–3.
Mean
values
(with
95%
confidence
intervals)
represent
data
from
two
24-h
periods
per
week
from
four
mothers.
Night-time
indicated
by
grey
shading.
Time
of
day
is
given
in
hours
with
0
representing
the
time
from
0001–0100
h,
and
23
the
time
from
2301
to
2400
h.
See
text
for
statistics.
±
2.4
SE;
x2
1=
19.85,
P
<
0.001),
but
with
no
statistically
significant
difference
between
weeks
2
and
3
(x2
1=
3.12,
P
=
0.07).
The
most
notable
finding
was
the
large
amount
of
time
moth-
ers
spent
in
the
den,
although
markedly
less
so
during
the
day.
The
most
obvious
explanation
for
this
difference
was
the
possible
effect
of
human
activity
in
or
around
the
pens
during
the
day,
par-
ticularly
during
the
morning
hours
when
the
initial
sharp
drop
in
the
time
mothers
spent
in
the
den
coincided
with
feeding
and
pen
and
den
cleaning.
Although
this
schedule
of
maintenance
is
surely
different
to
the
pattern
of
feeding
and
other
daily
activities
of
din-
goes
in
the
wild,
reports
suggest
them
to
be
very
flexible
in
their
feeding
habits
and
diet,
and
when
unmolested,
tolerant
of
close
human
presence
(Thomson,
1992b;
Smith
and
Vague,
2017).
From
the
early
afternoon,
mothers
then
spent
increasing
time
back
in
the
den
(Fig.
2a–c).
A
contributing
factor
to
greater
night-time
den
occupancy
might
also
have
been
mothers
seeking
shelter
from
the
cold.
When
in
the
den,
mothers
spent
a
large
percentage
of
time
‘nursing’
irrespective
of
time
of
day
(Fig.
2d–f).
As
we
reported
pre-
viously
(Hudson
et
al.,
2016)
this
did
not
necessarily
involve
the
whole
litter
simultaneously,
and
it
was
common
for
one
or
two
pups
to
be
attached
to
a
nipple
while
others
played
or
‘slept’.
No
diurnal
pattern
in
mothers’
nursing
behaviour
was
apparent,
and
the
percentage
time
while
in
the
den
they
spent
nursing
at
least
one
pup
did
not
differ
significantly
between
day
and
night
(x2
1=
0.35,
P
=
0.55;
Fig.
2d–f).
There
were,
however,
significant
differences
between
postpartum
weeks
1,
2
and
3
(x2
1=
23.27,
P
<
0.001).
Post
hoc
comparisons
showed
that
the
percentage
time
mothers
spent
nursing
was
significantly
greater
during
the
first
postpartum
week
(mean
80.8%
±
1.3
SE)
than
during
the
second
week
(mean
55.7%
±
1.6
SE;
x2
1=
13.98,
P
<
0.001)
and
third
week
(mean
55.6%
±
2.0
SE;
x2
1=
12.04,
P
<
0.001),
whilst
the
percentage
time
spent
nursing
dur-
ing
postpartum
weeks
2
and
3
did
not
differ
significantly
(x2
1=
0.03,
P
=
0.86).
Fathers
spent
relatively
little
time
in
the
den,
on
average
only
106.1
min
per
24-hour
period
(±17.2
SE)
during
the
first
three
postpartum
weeks,
although
there
appeared
to
be
sufficient
room.
Based
on
the
admittedly
small
available
sample
size,
the
average
time
did
not
differ
significantly
across
the
first
three
postnatal
weeks,
although
there
was
an
increase
in
the
mean
values
(week
1:
mean
1.7
min.
h
±
0.7
SE;
week
2:
mean
3.0
min.
h
±
1.0
SE;
week
3:
mean
9.0
min.
h
±
1.8
SE;
x2
2=
2.69,
P
=
0.26).
There
were
also
no
statistically
significant
differences
in
the
time
fathers
spent
in
the
den
at
night
(mean
7.2
min/h
±
1.3
SE)
and
during
the
day
(mean
1.1
min/h
±
0.3
SE;
x2
1=
2.51,
P
=
0.11).
The
reasons
for
paternal
absence
are
not
clear.
No
overt
aggres-
sion
by
females
towards
their
mate
in
or
at
the
den
was
seen,
and
the
den
was
sufficiently
large
to
accommodate
both
parents.
How-
ever,
such
behaviour
may
not
be
uncommon
among
males
during
the
pre-weaning
period.
Packard
(2003),
and
references
therein)
suggests
that
in
grey
wolves
the
contribution
of
the
father
consists
mainly
in
defence
of
the
home
site
(particularly
from
predators,
in
the
case
of
dingoes
potentially
wedge-tailed
eagles
(Aquila
audax),
cattle
or
buffalo,
snakes,
and
goannas;
Fleming
et
al.,
2001),
and
hunting
and
provisioning
the
lactating
female.
During
the
sec-
ond
month,
and
thus
beyond
the
scope
of
the
present
study,
this
changes,
with
male
wolves
spending
almost
as
much
time
in
the
den
as
the
mother
(Packard,
2003).
In
the
present
study
the
males
spent
considerable
time
on
top
of
the
den
(Fig.
1c).
A
simple
explanation
might
be
that
this
position
Please
cite
this
article
in
press
as:
Hudson,
R.,
et
al.,
Diurnal
pattern
of
pre-weaning
den
visits
and
nursing
in
breeding
pairs
of
captive
dingoes
(Canis
dingo).
Mammal.
Biol.
(2018),
https://doi.org/10.1016/j.mambio.2018.07.002
ARTICLE IN PRESS
G Model
MAMBIO-41031;
No.
of
Pages
6
R.
Hudson
et
al.
/
Mammalian
Biology
xxx
(2018)
xxx–xxx
5
was
the
most
comfortable
in
the
enclosure.
However,
we
suggest
that
the
males
were
possibly
acting
as
‘sentinels’
and
adopting
a
protective
role
enabling
their
mate
to
remain
calmly
within
the
den
with
the
pups.
This
is
consistent
with
anecdotal
reports
of
male
and
female
grey
wolves
residing
by
den
entrances,
seemingly
acting
as
sentinels
(e.g.
Murie,
1944;
Packard,
2003).
Also,
in
descriptions
of
the
dens
of
wild
dingoes,
Thomson
(1992a)
and
Smith
and
Vague
(2017)
report
a
preference
for
elevated
sites,
which
include
exten-
sive
views
of
lower
approaches,
and
with
well-worn
rest
pads
near
the
entrance.
To
check
this
sentinel
hypothesis
it
would
be
useful
to
have
information
on
dingoes’
resting
behaviour
in
relation
to
the
den
during
winter
but
no
longer
with
pups
present.
Despite
the
limitations
of
studying
captive
animals
our
results
seem
robust.
Behavioural
patterns
were
consistent
across
the
four
breeding
pairs
all
first
generation
descendants
of
wild-caught,
genetically
pure
dingoes
and
despite
differences
in
parents’
age
and
parity.
The
results
are
also
consistent
with
observations
of
den
attendance
and
parental
behaviour
in
the
taxonomically
closely
related
grey
wolf
(Mech
and
Boitani,
2003;
Mech
et
al.,
1999).
Clearly,
the
validity
of
these
results
needs
to
be
checked
against
fur-
ther
information
on
the
parental
behaviour
of
dingoes
in
the
wild.
The
results
nevertheless
provide
a
starting
point
for
a
comparison
with
parental
behaviour
in
other
canid
species,
and
particularly
with
free-ranging
dogs
(cf.
Arteaga
et
al.,
2013;
Hudson
et
al.,
2016).
It
is
possible
that
in
dogs
the
lack
of
a
close
pair
bond
and
clear
divi-
sion
of
labour
at
the
den
is
one
reason
for
their
generally
reduced
breeding
performance
and
the
inability
of
free-ranging
packs
to
form
self-sustaining
populations
independent
of
human
habitation
(Boitani
et
al.,
1995).
Conflict
of
interest
None.
Acknowledgements
We
thank
Lyn
Watson
and
Lyn
Whitworth
from
the
Dingo
Dis-
covery
Centre
and
Carolina
Rojas
for
technical
and
bibliographical
assistance.
Financial
support
was
provided
by
Central
Queens-
land
University,
the
Australian
Dingo
Foundation,
and
by
the
French-Mexican
scientific
exchange
program
ECOS
Nord
-
CONA-
CYT
(M14A02).
This
study
was
part
of
the
master’s
thesis
of
M.T.E
who
received
a
post-graduate
fellowship
(294591)
from
the
Mexi-
can
national
funding
agency
CONACYT.
Appendix
A.
Supplementary
data
Supplementary
material
related
to
this
article
can
be
found,
in
the
online
version,
at
doi:https://doi.org/10.1016/j.mambio.2018.
07.002.
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