The epipharyngeal sensilla of the damselfly Ischnura elegans (Odonata, Coenagrionidae)


Rebora, M.; Gaino, E.; Piersanti, S.

Micron 66: 31-36

2015


The knowledge on Odonata adult mouthparts sensilla is scanty and, notwithstanding the epipharynx in the labrum is considered an organ of taste, no ultrastructural investigation has been performed so far on this structure in Odonata. The labrum of the adult of the damselfly Ischnura elegans (Odonata, Coenagrionidae) shows on its ventral side the epipharynx with sensilla represented by articulated hairs and by small pegs located at the apex of slightly raised domes. Under scanning and transmission electron microscope, the articulated hairs, with a well developed socket and tubular body, have the typical structure of bristles, the most common type of insect mechanoreceptors, usually responding to direct touch; the pegs, showing an apical pore together with a variable number of sensory neurons (from two to five), the outer dendritic segments of which show a dendrite sheath stopping along their length, have features typical of contact chemoreceptors.

Micron
66
(2014)
31-36
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micron
Micron
ELSEVIF
journal
homepage:
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The
epipharyngeal
sensilla
of
the
damselfly
Ischnura
elegans
(Odonata,
Coenagrionidae)
Manuela
Rebora
,
Elda
Gaino,
Silvana
Piersanti
Dipartimento
di
Chimica,
Biologia
e
Biotecnologie,
Universita
di
Perugia,
Via
Elce
di
Sotto,
06121
Perugia,
Italy
U)
CrossMark
ARTICLE
INFO
Article
history:
Received
20
February
2014
Received
in
revised
form
7
May
2014
Accepted
19
May
2014
Available
online
27
May
2014
Keywords:
Aquatic
insects
Mouthparts
Chemoreceptors
Mechanoreceptors
Gustatory
sensilla
ABSTRACT
The
knowledge
on
Odonata
adult
mouthparts
sensilla
is
scanty
and,
notwithstanding
the
epipharynx
in
the
labrum
is
considered
an
organ
of
taste,
no
ultrastructural
investigation
has
been
performed
so
far
on
this
structure
in
Odonata.
The
labrum
of
the
adult
of
the
damselfly
Ischnura
elegans
(Odonata,
Coena-
grionidae)
shows
on
its
ventral
side
the
epipharynx
with
sensilla
represented
by
articulated
hairs
and
by
small
pegs
located
at
the
apex
of
slightly
raised
domes.
Under
scanning
and
transmission
electron
microscope,
the
articulated
hairs,
with
a
well
developed
socket
and
tubular
body,
have
the
typical
struc-
ture
of
bristles,
the
most
common
type
of
insect
mechanoreceptors,
usually
responding
to
direct
touch;
the
pegs,
showing
an
apical
pore
together
with
a
variable
number
of
sensory
neurons
(from
two
to
five),
the
outer
dendritic
segments
of
which
show
a
dendrite
sheath
stopping
along
their
length,
have
features
typical
of
contact
chemoreceptors.
2014
Elsevier
Ltd.
All
rights
reserved.
1.
Introduction
Most
terrestrial
animals,
including
insects,
possess
two
classes
of
chemical
sensory
organs.
Molecules
in
the
atmosphere
are
detected
by
smell
(olfactory)
sensory
organs,
whereas
molecules
dissolved
in
a
solution
interact
with
taste
(gustatory)
sensory
organs.
The
essential
elements
of
the
gustatory
sensory
organs
in
insects
are
neuronal
sensory
cells,
expressing
gustatory
receptors
(Clyne
et
al.,
2000;
Scott
et
al.,
2001),
responding
to
the
four
primary
taste
stimuli
of
sweet,
sour,
salty,
and
bitter,
and
conduct
informa-
tion
in
the
form
of
electrical
signals
to
the
central
nervous
system
(see
reviews
in
Mitchell
et
al.,
1999;
Singh,
1997).
Insect
gustatory
sensilla
are
typically
located
on
mouthparts,
due
to
the
pivotal
role
that
these
sensilla
play
in
feeding
behav-
ior;
however,
investigators
have
also
recognized
that
gustatory
receptors
on
the
ovipositor
are
involved
in
host
recognition
for
oviposition,
while
other
receptors
on
the
tarsi
are
potentially
used
in
both
feeding
and
oviposition
(Mitchell
et
al.,
1999).
Gustatory
sensilla
have
been
described
in
many
insects
such
as
Diptera
(Colbo
et
al.,
1979;
Lee
and
Davies,
1978;
Minnich,
1926a,b,
1929;
Rice,
1973),
Hymenoptera
(de
Brito
Sanchez
et
al.,
2014;
Isidoro
et
al.,
2001),
Coleoptera
(Giglio
et
al.,
2013),
Homoptera
(Backus,
1985;
Backus
and
McLean,
1983;
Foster
et
al.,
1983;
*
Corresponding
author.
Tel.:
+39
0755855722.
E-mail
address:
manuela.rebora@unipg.it
(M.
Rebora).
http://dx.doLorg/10.1016/j.micron.2014.05.003
0968-4328/C
2014
Elsevier
Ltd.
All
rights
reserved.
Heming,
1978;
Ullman
and
McLean,
1986;
Wensler
and
Filshie,
1969),
Hemiptera
(Baker
et
al.,
2008;
Miles,
1958),
Lepidoptera
(DeBoer
et
al.,
1977;
Minnich,
1921),
Ephemeroptera
(Gaino
and
Rebora,
1998).
As
far
as
Odonata
are
concerned,
typical
gustatory
sensilla
have
been
described,
together
with
mechanoreceptors,
on
the
endo-
phytic
cutting
ovipositor
of
the
dragonfly
Aeshna
cyanea
and
of
the
damselfly
Ischnura
elegans
(Rebora
et
al.,
2013a,b),
while
the
occur-
rence
of
single-pore
sensilla
have
been
demonstrated
on
the
larval
maxillary
palps
of
damselflies
Coenagrion
puella
and
Ischnura
ele-
gans
(Bassemir
and
Hansen,
1980).
Knowledge
on
adult
mouthparts
sensilla
is
scanty
and,
even
though
the
labrum
and
the
epiphar-
ynx
are
considered
organs
of
taste
in
Odonata
adults
and
larvae
(Pritchard,
1965;
Tillyard,
1917),
so
far
no
ultrastructural
investi-
gation
has
been
performed
to
describe
in
detail
the
sensilla
located
on
these
parts.
Therefore,
this
study
investigates
under
scanning
and
trans-
mission
electron
microscope
the
sensory
structures
located
on
the
inner
side
of
the
labrum
of
the
damselfly
Ischnura
elegans
(Coena-
grionidae),
with
the
aim
of
describing
the
mechanosensory
and
gustatory
sensilla
of
Odonata
epipharynx.
2.
Material
and
methods
Adults
of
L
elegans
(Coenagrionidae)
were
collected
along
an
artificial
pond
close
to
Sant'Arcangelo
(Perugia,
Central
Italy)
in
June
2013.
In
the
laboratory,
the
mouthparts
of
10
specimens
32
M.
Rebore
et
al
/
Micron
66
(2014)
31-36
a
-
7
-
*
d
H
fj
-
e
D
f
4
1
Fig.1.
Labrum
of
the
adult
of
the
damselfly
Ischnura
elegans
under
SEM.
(a)
Dorsal
view
of
the
head
showing
the
labrum
(arrow)
with
long
setae
on
its
surface,
bar
=
1
mm;
(b)
Ventral
side
of
the
labrum.
The
epipharynx
is
well
evident
with
its
oval
shape
(dotted
line).
The
surrounding
cuticle
(asterisks)
is
decorated
with
microsculptures,
bar
=
200
pm;
(c)
Zoomed
view
of
the
microsculptures
in
the
form
of
spines
oriented
toward
the
epipharynx,
bar
=
10
pm;
(d)
Epipharynx
showing
two
brush-like
structures
on
its
proximal
portion
(arrow)
and
sensilla
on
its
distal
portion,
represented
by
articulated
hairs
(H),
and
pegs
at
the
apex
of
slightly
raised
domes
(D),
bar=
200
pm;
(e)
Detail
of
the
hairs
(H)
and
of
the
slightly
raised
domes
(D)
bearing
cone-shaped
small
pegs
that
can
be
in
groups
(double
arrow)
or
isolated
(arrow)
at
the
apex
of
the
dome,
bar=
20
pm;
(1)
Detail
of
one
dome
showing
three
cone-shaped
small
pegs
(arrow),
bar=
10
pm.
were
dissected
from
anaesthetized
damselflies
and
fixed
for
12
h
in
2.5%
glutaraldehyde
(Electron
Microscopy
Society,
Hatfield,
PA)
in
cacodylate
buffer
(Electron
Microscopy
Society,
Hatfield,
PA),
pH
7.2.
For
scanning
electron
microscopy
(SEM)
analysis,
the
fixed
material
was
repeatedly
rinsed
in
the
same
buffer,
and
then
dehydrated
by
using
ethanol
gradients,
followed
by
critical-point
drying
in
a
critical-point
dryer
CPD
030
Bal-Tec
(Bal-Tec
Union
Ltd.,
Balzers,
Liechtenstein).
Specimens
were
mounted
on
stubs
with
silver
conducting
paint,
sputter-coated with
gold-palladium
in
an
Emitech
K550X
sputterer
(Emitech,
Ashford,
England),
and
observed
with
a
Philips
XL30
(Philips,
Eindhoven,
the
Netherlands),
at
an
accelerating
voltage
of
18
kV.
For
transmission
electron
microscopy
(TEM),
the
fixed
mouthparts
were
repeatedly
rinsed
in
cacodylate
buffer
and
post-fixed
for
1
h
at
4
°C
in
1%
osmium
tetroxide
(Electron
Microscopy
Society,
Hatfield,
PA)
in
cacody-
late
buffer.
The
samples
were
then
repeatedly
washed
in
the
same
buffer,
dehydrated
by
using
ethanol
gradients
and
finally
embed-
ded
in
an
Epon-Araldite
mixture
resin
(Fluka,
Sigma—Aldrich).
Afterward,
ultrathin
sections
were
cut
on
a
Leica
EM
UC6
ultracut
(Leica
Microsystem
GmbH,
Wetzlar,
Germany),
collected
on
col-
lodium
coated
copper
grids,
stained
with
uranyl
acetate
and
lead
citrate
(Fluka,
Sigma—Aldrich),
and
examined
with
a
Philips
EM
208
(Philips,
Eindhoven,
the
Netherlands).
3.
Results
The
adult
of
the
damselfly
Ischnura
elegans
shows
the
typical
Odonata
chewing
mouthparts.
When
at
rest,
the
mouth
is
com-
pletely
closed
by
the
labrum
above,
and
by
its
appendages
below
and
at
the
sides.
These
appendages
are
the
mandibles,
the
maxillae
and
the
labium;
the
first
two
placed
laterally,
the
last
ventrally.
The
labrum
and
labium
act
as
upper
and
lower
lips
respectively,
while
the
mandibles
and
the
maxillae
constitute
two
pairs
of
laterally
working
jaws.
The
labrum
(Fig.
1
a)
is
characterized
by
a
lot
of
long
setae
on
its
dorsal
surface;
on
its
ventral
side
the
epipharynx
is
well
evident
with
its
oval
shape
(Fig.
1
b),
surrounded
by
cuticle
decorated
with
microsculptures
in
the
form
of
spines
which
are
oriented
toward
SS
C
TB
SS
DS
TB
M.
Rebora
et
al
/
Micron
66
(2014)31-36
33
\
TB
DS
C
AC
Fig.
2.
Articulated
hairs
in
longitudinal
section
under
TEM.
(a)
Thick
cuticle
(C)
of
the
epipharynx
showing
the
hairs
(arrows)
innervated
by
the
neurons,
bar
=10
pm;
(b)
Detail
of
an
articulated
hair
(H)
showing
its
connection
to
the
socket
(S)
via
an
elastic
joint
membrane
UM)
and
the
innervation
by
a
single
neuron.
AC,
accessory
cell,
C,
cuticle,
DS,
dendrite
sheath,
SS,
socket
septum,
TB,
tubular
body,
bar=
2µm;
(c)
Detail
of
the
tubular
body
(TB)
with
densely
packed
microtubules
enveloped
by
the
dendrite
sheath
(DS).
The
white
arrow
points
out
the
projection
of
the
dendrite
sheath
touching
the
sensory
cuticle.
Double
arrows
point
out
the
infolds
of
dendrite
sheath.
C,
cuticle,
MC,
molting
channel,
SS,
socket
septum,
bar=
2µm;
(d)
Longitudinal
section
of
the
tubular
body
(TB)
at
a
more
proximal
level
showing
the
infoldings
of
the
dendrite
sheath
(DS).
C.
cuticle,
SS;
socket
septum,
bar=
2µm.
the
epipharynx
(Fig.
1c).
The
epipharynx
shows
two
brush-like
structures
on
the
proximal
portion
and
sensilla
on
the
distal
one
(Fig.
1d).
The
sensilla
are
represented
by
articulated
hairs
of
vari-
able
length
(from
5-50µm),
located
in
well
developed
sockets
and
oriented
toward
the
center
of
the
epipharynx,
and
by
pegs
at
the
apex
of
slightly
raised
domes
of
variable
diameter
(Fig.
l
e).
These
pegs
are
very
small
cone-shaped
structures
measuring
about
1µm
in
length,
isolated
or
in
groups
at
the
apex
of
a
single
dome
(Fig.
10.
The
articulated
hairs
are
about
30
and
the
pegs
about
50
in
number.
In
transversal
section
the
labrum
shows
the
thick
cuticle
of
its
ventral
side
crossed
by
the
neurons
innervating
the
epipharyngeal
sensilla
(Figs.
2a
and
3a).
In
longitudinal
section
the
articulated
hairs
show
the
complex
structure
of
their
socket.
Each
hair
is
con-
nected
to
the
socket
via
an
elastic
joint
membrane
(Fig.
2b),
and
is
innervated
by
one
bipolar
neuron
whose
outer
dendritic
seg-
ment
shows
a
very
developed
tubular
body
with
microtubules
tightly
packed
into
an
electron-dense
substance
(Fig.
2b
and
c).
The
tubular
body
is
attached
to
the
base
of
the
hair
through
a
thick
dendrite
sheath
connected
to
the
cuticle
by
the
intermediate
of
a
well
developed
socket
septum
(Fig.
2b
and
c).
The
neuron
is
sur-
rounded
by
the
accessory
cells
(Fig.
2b).
The
dendrite
sheath,
at
the
tip
of
the
outer
dendritic
segment,
shows
a
projection
touching
the
sensory
cuticle
of
the
hair
base
(Fig.
2c).
A
molting
channel,
typ-
ical
of
hemimetabolans,
is
visible
at
the
base
of
the
shaft
cuticle,
in
correspondence
of
the
end
of
the
dendrite
sheath
(Fig.
2c).
The
dendrite
sheath
shows
infolds
within
the
outer
dendritic
segments
(Fig.
2d).
The
small
pegs,
located
at
the
apex
of
slightly
raised
domes,
are
innervated
by
groups
of
bipolar
neurons
of
variable
number
(from
two
to
five)
(Fig.
3a
and
b).
Each
group
of
outer
dendritic
segments
is
unbranched
and
wrapped
by
the
dendrite
sheath.
The
accessory
cells
around
the
dendritic
segments
are
very
developed
and
pro-
duce
an
abundant
electron-dense
secretion
which
is
interspersed
among
the
microvilli
of
the
labyrinth
entering
the
sensillar
sinus
(Fig.
3c).
In
longitudinal
section,
the
long
outer
dendritic
segments
crossing
the
thick
cuticle
of
the
epipharynx
and
the
ciliary
constric-
tions
are
evident
(Fig.
3d).
The
dendrite
sheath
enveloping
the
outer
dendritic
segments
seems
interrupted
and
not
reaching
their
distal
portion
(Fig.
3e).
In
longitudinal
section
the
small
peg
is
unarticu-
lated
(Fig.
3f)
and
perforated
by
a
single
apical
pore
very
reduced
in
size
(measuring
about
20
nm
in
width)
(Fig.
3g).
The
outer
den-
dritic
segment
stops
just
under
the
small
porous
peg
(Fig.
3c).
A
schematic
reconstruction
of
a
small
peg
is
reported
in
Fig.
4.
4.
Discussion
The
present
ultrastructural
investigation
shows
that
the
epipharynx
of
the
damselfly
Ischnura
elegans
is
a
sensory
structure
bearing
mechanoreceptors
and
gustatory
receptors.
The
articulated
hairs
located
externally
to
the
pegs
and
oriented
toward
the
center
of
the
epipharynx
have
the
typical
structure
of
bristles,
the
most
common
type
of
mechanoreceptors,
usually
responding
to
direct
touch
(see
review
in
Keil,
1997),
thanks
to
the
complex
structure
of
the
socket
and
of
the
sensory
neuron
with
'fs
C
"
C
AC
16
AC
.r-
,
90
D
S
ODS
4
1
DS
,
a
11V
V
C
AC
f
C
AC
34
M.
Rebora
et
al
/
Micron
66
(2014)31-36
S
fr
e
AC
ODS
DS
C
Fig.
3.
Sections
of
the
small
pegs
located
at
the
apex
of
slightly
raised
domes,
under
TEM.
(a)
Group
of
three
pegs
in
longitudinal
section.
Each
peg
is
innervated
by
a
variable
number
of
neurons
(arrows).
AC,
accessory
cells,
C,
cuticle,
bar
=
10
pm;
(b)
Cross
section
of
the
outer
dendritic
segments
(arrows)
of
three
pegs,
each
differently
innervated
by
three
(3N),
four
(4N)
and
five
neurons
(5N).
AC,
accessory
cells,
DS,
dendrite
sheath,
bar
=
2µm;
(c)
Three
pegs
with
their
outer
dendritic
segments
(arrows)
in
longitudinal
section.
AC,
accessory
cells
with
electron-dense
secretion
(asterisks),
C,
cuticle,
MV,
microvilli.
Note
that
one
of
the
outer
dendritic
segments
stops
just
under
the
small
peg
(black
arrow),
bar=
5µm;
(d)
Longitudinal
section
of
an
outer
dendritic
segments
(ODS).
AC,
accessory
cells,
C,
cuticle,
CC,
ciliary
constrictions,
N,
nucleus
of
the
accessory
cell.
The
arrow
points
out
the
interruption
of
the
dendrite
sheath
(DS)
zoomed
in
(e),
bar=
5µm;
(e)
Detail
of
an
outer
dendritic
segment
(ODS)
in
longitudinal
section
showing
the
interruption
(arrow)
of
the
dendrite
sheath
(DS).
AC,
accessory
cell,
bar
=1
pm;
(1)
Small
peg
in
longitudinal
section
(arrow)
detailed
in
figure
(g).
AC,
accessory
cell,
C,
cuticle,
bar=
2.5µm;
(g)
Detail
of
the
apical
region
of
the
small
peg
showing
the
single
apical
pore
(arrow).
C,
cuticle,
bar=
0.5
pm.
its
tubular
body.
These
bristles
have
probably
the
task
to
sense
the
presence
of
prey
inside
the
mouth,
whereas
the
microsculptures
located
on
the
ventral
side
of
the
labrum
around
the
epipharynx
and
oriented
toward
the
sensilla
act
to
prevent
the
escape
of
the
prey.
Many
mechanoreceptors
show
a
directional
sensitivity,
which
means
that
they
respond
maximally
to
deflection
or
deformation
in
one
plane,
or
only
in
one
direction.
A
deflection
of
the
hair
shaft
is
transformed
into
a
small
oppositely-directed
movement
of
the
stimulating
edge
(Keil,
1997).
In
the
bristles
of
the
epipharynx
of
L
elegans
the
projection
of
the
dendrite
sheath
at
the
tip
of
the
outer
M.
Rebora
et
al
/
Micron
66
(2014)
31-36
35
interception
(Olberg,
2012);
recent
investigations
(Piersanti
et
al.,
2014)
demonstrated
by
means
of
behavioral
and
electrophysiolog-
ical
assays
that
adults
of
Ischnura
elegans
are
attracted
by
olfactory
cues
emitted
by
prey,
that
they
can
perceive
through
the
olfac-
tory
antennal
sensilla
described
in
many
Anisoptera
and
Zygoptera
species
(Piersanti
et
al.,
2010,
2014;
Rebora
et
al.,
2008,
2009,
2012).
Once
prey
has
been
caught,
it
is
fundamental
for
the
damselfly
to
be
able
to
assess
the
quality
of
the
food
before
its
ingestion.
This
ability
has
been
confirmed
by
some
observations
in
the
field.
In
fact,
damselflies
have
been
described
catching
a
ladybird
and
rejecting
it
before
ingestion
(Lambret,
2009),
a
process
probably
allowed
by
the
epipharynx
with
its
mechano
and
chemoreceptors.
Further
electrophysiological
investigations
may
clarify
which
chemicals
Odonata
are
able
to
detect
through
the
gustatory
sensilla
located
on
their
epipharynx.
AC
DS
D
AC
AC
n
Fig.
4.
Schematic
reconstruction
of
one
peg
on
the
basis
of
serial
longitudinal
and
cross
sections.
AC,
accessory
cells,
C,
cuticle,
DS,
dendrite
sheath;
ODS,
outer
den-
dritic
segments.
Arrow
points
out
the
interruption
of
the
dendrite
sheath;
arrow
head
points
out
the
apical
pore.
dendritic
segment
containing
the
tubular
body
could
have
a
role
as
stimulating
edge,
in
touching
the
sensory
cuticle
of
the
hair
base.
As
it
happens
in
many
mechanoreceptors,
if
the
hair
is
deflected
in
the
direction
of
the
stimulating
edge,
the
dendritic
membrane
is
depolarized
and
spikes
are
elicited,
while
deflection
of
the
hair
in
the
opposite
direction
hyperpolarizes
the
dendritic
membrane,
and
spike
activity
is
suppressed
(Keil,
1997).
The
small
pegs
located
at
the
apex
of
domes
are
innervated
by
a
variable
number
of
sensory
neurons
(from
two
to
five),
the
outer
dendritic
segments
of
which
show
a
dendrite
sheath
not
reaching
their
distal
portion
but
stopping
along
their
length.
This
feature,
together
with
the
apical
pore,
is
coherent
with
a
function
of
these
sensilla
as
contact
chemoreceptors.
A
typical
insect
taste
sensillum
is
a
uniporous
sensillum
that
has
both
chemosensory
and
mechanosensory
cells
allowing
the
function
"touch
and
taste"
(Altner
and
Prillinger,
1980;
Zacharuk,
1980),
but
gustatory
sen-
silla
without
the
mechanosensory
element
are
common
in
insects
as
well
(Zacharuk,
1985).
The
small
pegs
located
on
the
epipharynx
of
I.
elegans
are
unarticulated
and
do
not
show
any
mechanosen-
sory
neuron.
In
their
internal
structure
they
are
similar
to
those
described
on
the
maxillary
palps
of
the
larva
of
L
elegans
(Bassemir
and
Hansen,
1980)
where
four
single-pore
sensilla
possess
two-
six
bipolar
sensory
cells
and
their
dendritic
tips
have
access
to
the
outside
through
the
opening
of
the
pore
tubule,
without
any
outer
cuticular
structure.
Contact
chemoreceptors
evident
on
the
cuticular
surface
as
simple
pores,
without
either
any
outer
cuticu-
lar
structure
or
the
mechanosensory
neuron,
have
been
described
on
the
labral
sense
organ
of
other
insects
such
as
Drosophila
(Nayak
and
Singh,
1983).
The
pegs
on
the
epipharynx
of
I.
elegans
are
con-
tact
chemoreceptors
characterized
by
a
cuticular
structure
of
small
size
and
by
the
presence
of
a
pore,
at
their
apex,
of
a
very
reduced
width
(17
nm
against
the
0.12-0.22
pm
of
the
gustatory
sensilla
described
on
the
maxillary
palps
of
the
larva).
Odonata
adults
are
generalist
predators
with
a
diversified
diet
in
which
Diptera
numerically
prevail
(Corbet,
1999).
For
prey
recog-
nition,
Odonata
probably
use
different
kinds
of
stimuli.
We
know
that
vision
is
fundamental
in
dragonflies
and
damselflies
for
prey
Acknowledgments
We
are
very
grateful
to
Antonello
Sotgiu
for
his
technical
assistance.
Thanks
to
the
anonymous
referees
for
their
helpful
suggestions.
This
work
was
supported
by
the
Italian
Ministry
for
Universities
and
Research
(MIUR-Fondo
Integrativo
per
la
Ricerca
di
Base
-
F.I.R.B.,
2010,
RBFR10Z196).
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