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CHEMICAL
RELEASERS
OF
NECROPHORIC
BEHAVIOR
IN
ANTS
By
E.
O.
WILSON,
N.
I.
DURLACH,
2AND
L.
M.
ROTH
3
INTRODUCTION
One
of
the
more
conspicuous
and
stereotyped
patterns
of
social
behavior
exhibited
by
ants
is
the
transport
of
dead
members
of
the
colony
from
the
nest
to
the
refuse
piles
(McCook,
1882;
Wheeler,
1926).
Because
of
the
obvious
simplicity
of
this
"necrophoric"
response
and
the
ease
with
which
it
can
be
experimentally
elicited,
it
has
proven
to
be
one
of
the
forms
of
ant
behavior
most
amenable
to
physiological
analysis.
In
the
present
paper
are
presented
the
results
of
a
preliminary
study
of
the
response
in
the
myrmicine
ants
Pogonomyrmex
badius
(Latreille)
and
Solenopsis
saevissima
(Fr.
Smith),
in
which
special
atten-
tion
has
been
paid
to
the
releasing
stimuli.
DESCRIPTION
OF
THE
BEHAVIOR
When
the
corpse
of
an
adult
Pogonomyrmex
badius
work-
er
that
has
been
allowed
to
decompose
in
the
open
air
for
a
day
or
more
is
placed
inside
the
nest
or
outside
near
the
nest
entrance,
the
first
sister
worker
to
encounter
it
ordin-
arily
investigates
it
briefly
by
repeated
antennal
contact,
then
picks
it
up
and
carries
it
directly
away
from
the
nest
toward
the
refuse
piles.
Under
the
conditions
existing
dur-
ing
the
present
study,
most
of
the
refuse
piles
of
the
captive
colonies
were
located
less
than
one
meter
from
the
nest
entrance
along
the
back
wall
of
a
closed
foraging
arena.
This
distance
was
evidently
inadequate
to
allow
the
rapid
consummation
of
the
corpse
removal
response,
for
workers
bearing
corpses
frequently
wandered
for
many
minutes
1
Biological
Laboratories,
Harvard
University,
Cambridge
Mass.
2
Lincoln
Laboratory,
Lexington,
Mass.
U.
S.
Army
Quartermaster
Research
and
Engineering
Center,
Natick,
Mass.
108
1958]
Wilson,
Durlach,
Roth
Chemical
Releasers
109
back
and
forth
along
the
back
wall
before
dropping
their
burdens
on
the
refuse
piles.
Others
were
seen
to
approach
the
back
wall
unburdened,
o
pick
up
corpses
already
on
the
piles,
and
to
transport
them
in
similarly
restless
fashion
before
re-depositing
them.
It
is
a
curious
fact
that
in
nature
such
"cemeteries"
are
rare
or
non-existent
in
the
vicinity
of
Pogonomyrmex
badius
nests.
During
field
studies
conducted
in
northern
Florida
and
southern
Alabama,
it
was
found
that
corpses
re-
moved
from
the
nests
are
carried
only
a
short
distance
beyond
the
rim
of
the
nest
crater
before
being
dropped.
Once
abandoned,
they
are
soon
collected
by
scavenging
workers
of
the
dolichoderine
species
Conomyrma
pyramica
(Roger),
one
of
the
dominant
ants
occurring
with
P.
badius
in
its
native
range.
The
swift
Conomyrma
workers
patrol
the
vicinity
,of
the
Pogonomyrmex
nests
in
large
numbers
during
the
day,
and
their
activities
apparently
prevent
the
accumulation
of
Pogonomyrmex
dead.
It
is
not
known
whether
other
ant
species
assume
this
role
outside
the
range
of
Conomyrma.
In
the
laboratory
most
injured
and
dying
Pogonomyrmex
badius
workers
leave
the
nest
interi.or
before
succumbing.
These
individuals
are
usually
found
wandering
through
the
foraging
arena,
unattended
by
sister
workers.
If
sim-
ilar
behavior
is
exhibited
in
nature,
it
can
safely
be
in-
ferred
that
the
removal
of
corpses
is
thus
accomplished
in
large
part
by
the
dying
ants
themselves,
as
their
last
act
as
living
workers.
Under
laboratory
conditions
queens
and
some
larger
major
workers
remain
within
the
nest
while
dying.
Several
times
it
was
observed
that
the
bodies
of
these
individuals
remained
in
the
nest
for
three
days,
during
which
they
were
frequently
licked
and
moved
about
by
the
workers.
After
that
time
they
were
removed
to
the
refuse
piles.
EXPERIMENTS
Assay
of
decomposition
products.
The
following
experi-
ment
was
designed
to
determine
whether
certain
substances
separated
from
the
body
of
the
corpse
could
by
themselves
elicit
necrophoric
behavior.
A
square
of
filter
paper
six
110
Psyche
[December
millimeters
on
the
side
was
daubed
with
an
acetone
ex-
tract
of
Pogonomyrmex
badius
worker
corpses
and
placed,
in
company
with
five
untreated
control
squares,
inside
he
foraging
arena
five
centimeters
2rom
the
nest
entrance.
In
three
separate
trials,
the
treated
squares
were
picked
up
within
five
minutes
by
the
first
workers
to
encounter
them
and
transported
directly
to
the
refuse
piles.
In
their
reaction
to
the
treated
squares
and
in
their
locomotory
patterns
during
transport,
the
workers
appeared
to
behave
in
the
same
fashion
as
toward
worker
corpses.
No
immedi-
ate
reaction
to
the
control
squares
was
noted,
and
they
were
not
moved
significantly
from
their
original
positions
during
the
first
several
hours.
In
only
one
case
was
a
con-
trol
square
transported
in
the
direction
of
the
refuse
piles
during
the
course
of
the
first
twenty-four
hours.
A
similar
response
was
also
evoked
by
objects
other
than
paper
squares.
Seeds,
2or
example,
which
ordinarily
would
be
ignored
or
carried
into
the
nest
for
storage,
when
daubed
with
the
extract
were
carried
to
the
refuse
pile.
The
most
dramatic
example
of
the
potency
.of
this
extract
as
a
releaser
occurred
on
three
occasions
when
the
objects
chosen
for
experiment
were
live
workers.
Despite
the
fact
that
these
ants
were
moving
around
under
their
own
power
and
providing
socially
significant
stimuli,
they
were
treated
by
their
sisters
as
corpses.
However,
unlike
authentic
corpses
they
would
allow
themselves
to
be
carried
to
the
refuse
pile
only
to
rise
again
and
return
to
the
nest!
The
cycle
was
observed
to
occur
repeatedly
during
periods
of
one
to
two
hours.
During
transport,
the
workers
folded
their
appendages
in
.he
"pupal"
posture
usually
taken
by
normal
w,
orkers
being
carried
to
nest
site.s.
An
attempt
was
next
made
to
determine
whether
the
chemical
releasers
could
be
removed
from
worker
bodies
by
leaching
so
as
to
modify
the
response
of
living
workers
to
the
bodies.
Three
worker
corpses
were
placed
in
bottles
containing
50
cc.
of
acetone
2or
periods
of
one
to
three
weeks,
then
thoroughly
dried
and
presented
in
succession
to
living
workers
in
the
manner
described
above.
The
behavior
toward
these
treated
bodies
was
markedly
dif-
ferent
2rom
that
shown
toward
untreated
corpses.
Instead
95s]
Wilson,
Durlach,
Roth-
Chemical
Releasers
111
of
transporting
them
away
from
the
nests,
the
workers
began
to
lick
and
chew
them
vigorously.
One
was
carried
quickly
into
the
nest;
the
other
two
were
dragged
back
an.d
forth
for
short
distances
near
the
nest
entrance.
Several
untreated
corpses
pla.ced
around
the
leached
bodies
were
at
the
same
time
carried
directly
off
to
the
refuse
piles.
One
of
the
leached
bodies
was
recovered
several
minutes
after
its
introduction,
daubed
with
corpse
extract,
and
re-
intr.oduced.
The
same
workers
that
had
been
licking
it
pre-
viously
now
carried
it
directly
to
the
refuse
piles.
The
other
two
leached
bodies
were
left
in
position
to
observe
their
subsequent
treatment.
One
was
dismembered
by
the
living
workers;
both
were
carried
away
from
the
nests
only
after
forty
minutes
or
longer.
The
paper-square
test
described
previously
was
next
employed
to
test
a
few
common
fat
and
protein
decomposi-
tion
products
and
related
compounds
obtained
as
chemical
reagents.
The
following
substances
produced
no
detectable
response,
either
in
saturated
or
dilute
solutions"
ammonium
sulfide,
di-alpha-amine.
Weak
to
moderate
alarm
behavior,
followed
occasionally
by
digging
behavior
,
was
evoked
by
the
following
substances:
phenylethylamine,
triethano-
lamine,
phenol,
n-valeric
acid,
n-caproic
acid,
n-caprylic
acid,
n-butyric
acid,
formic
acid.
The
only
substance
tested
that
released
the
necrophoric
response,
or
anything
re-
sembling
it,
was
oleic
acid.
In
repeated
trials,
oleic
acid
daubed
onto
paper
squares
and
other
small
neutral
objects
invariably
elicitecl
a
behavioral
response
from
P.
badius
indistinguishable
from
that
evoked
by
worker
corpses.
On
the
assumption
that
oleic
acid,
or
a
related
compound,
is
a
principal
natural
releaser
of
the
necrophoric
response,
an
attempt
was
made
to
separate
and
analyze
the
long-
chain
atty
acids
found
in
Pogonomyrmex
worker
corpses.
Infrared
spectra
were
prepared
from
a
crude
extract
of
about
200
dead
bodies
of
P.
barbatus
(Fr.
Smith).
These
spectra
were
made
from
a
sample
in
CC14
and
from
a
liquid
film
after
the
carbon
tetrachloride
was
evaporated.
A
fuller
account
of
alarm
and
digging
behavior,
and
of
the
various
stimuli
that
release
these
linked
responses,
has
been
presented
elsewhere
(Wilson,
1959).
112
Psyche
:December
The
spectra
indicated
the
presence
in
the
crude
extract
of
an
ester
(the
principal
compound)
and
a
fatty
acid.
An
attempt
was
made
to
separate
the
fatty
acid
from
the
mix-
ture.
The
solvent
of
the
original
solution
was
evapor-
ated
and
the
residue
dissolved
in
ether
which
was
then
washed
with
dilute
NaCO.
The
alkaline
wash
containing
the
sodium
salt
of
the
fatty
acid
was
separated
from
the
ether
solution
containing
the
ester.
The
infrared
spectrum
of
the
ether
solution
compared
well
with
the
original
crude
material,
indicating
that
the
ester
had
been
removed.
The
alkaline
wash
containing
the
Na
salt
of
the
fatty
acid
was
acidified
with
dilute
HC1
and
extracted
wih
ether.
The
infrared
spectrum
of
this
ether
extract
indicated
a
fatty
acid
though
the
spectrum
was
not
sufficiently
distinctive
to
identify
the
compound
specifically.
In
a
series
of
tests
using
treated
and
untreated
(control)
paper
squares,
it
was
found
that
both
the
fatty
acid
and
the
ester
evoked
the
necrophoric
response.
However,
the
fatty
acid
appeared
to
be
the
more
effective
of
the
two,
in
that
it
tended
to
release
the
response
more
quickly
and
to
induce
transport
of
the
treated
squares
over
greater
distances.
It
was
further
observed
that
the
acid-daubed
squares
were
as
a
rule
trans-
ported
further
away
from
the
nest
entrance
during
initial
transport.
Also,
the
ester-daubed
squares
frequently
caused
an
initial
mild
alarm
reaction
that
delayed
the
necrophoric
response
even
more,
whereas
the
acid-daubed
squares
were
never
observed
to
do
so.
It
is
possible
that
complete
sep-
aration
of
the
acid
and
ester
was
not
obtained
and
that
contamination
of
the
ester
fraction
with
the
acid
could
account
for
the
equivocal
results.
Use
of
another
test
species.
An
attempt
was
next
made
to
determine
whether
the
fatty
acid
obtained
from
Pogon-
omyrmex
barbatus
would
release
necrophoric
behavior
in
a
phylogenetically
remote
ant
species,
Solenopsis
saevissima
(Fr.
Smith).
Four
paper
squares
daubed
with
the
acid
were
inserted,
along
with
four
control
squares,
into
the
brood
chamber
of
an
artificial
nest
containing
a
colony
of
S.
saevissima.
Within
25
minutes
all
four
of
the
treated
squares
had
been
carried
out
and
placed
at
the
edge
of
the
nest.
Soon
afterward
the
control
squares
were
brought
1958]
Wilson,
Durlach,
Roth---
Chemical
Releasers
113
out
and
dropped
at
the
same
pla.ce.
Five
hours
later
all
of
the
treated
squares
had
been
moved
to
a
position
about
twenty
centimeters
beyond
the
nest
edge.
A
saevissima
worker
was
later
seen
carrying
a
treated
square
back
and
forth
in
the
restless
fashion
commonly
seen
in
workers
of
this
species
carrying
corpses.
Assay
of
extract
from
another
insect
species.
To
deter-
mine
whether
fatty
extracts
of
corpses
of
another
insect
species
causes
the
necrophoric
response
in
Pogonomyrmex
badius,
extracts
from
meal
worms
(Tenebrio
molitor)
al-
lowed
to
decompose
in
open
air
for
two
weeks
were
tested
in
the
usual
fashion.
Treated
paper
squares
were
carried
promptly
to
the
refuse
piles
by
the
Pogonomyrmex
workers,
whereas
control
squares
were
left
untouched
for
the
first
several
hours.
The
behavior
of
the
ants
toward
the
treated
squares
seemed
identical
to
that
shown
toward
squares
treated
with
the
extract
of
Pogonomyrmex
corpses.
CONCLUSIONS
Pogonomyrmex
badius
workers
utilize
a
relatively
lim-
ited
range
of
stimuli
in
"recognizing"
insect
corpses.
More-
ever,
the
stimuli
appear
to
be
exclusively
chemical
in
nature.
One
of
the
principal
chemical
releasers
is
evidently
the
fatty
acid
that
accumulates
in
the
bodies
of
sister
work-
ers
allowed
to
decompose
in
open
air.
An
ester
may
also
play
a
secondary
role.
Of
several
chemical
compounds
test-
ed
commonly
iound
in
insect
corpses,
oleic
acid
was
the
only
substance
which
caused
the
ants
to
behave
as
they
do
toward
dead
insect
bodies.
Whether
other
substances
present
in
ant
corpses
(and
those
of
other
animals)
re-
lease
the
necrophoric
response
is
not
known.
It
may
be
suggestive
that
the
common
smaller
molecular
products
.of
decomposition
thus
far
tested
have
all
produced
neutral
or
alarm
behavior
without
any
element
of
necrophoresis.
It
is
also
noteworthy
that
long-chain
fatty
acids
are
chem-
ically
among
the
most
stable
and
least
volatile
of
fat
and
protein
decomposition
products
and
hence
tend
to
accumu-
late
disproportionately
in
insect
corpses.
As
a
result
hese
substances
have
he
potential
to
serve
as
efficient
signals
of
the
presence
of
aging
corpses,
as
opposed
to
freshly
114
Psyche
[December
killed
and
edible
insect
prey.
Finally,
the
fact
that
the
fatty
acid
from
Pogonomyrmex
barbatus
corpses
induced
t,
ypical
necrophoric
behavior
in
both
P.
badius
and
Solen-
opsis
saevissima
workers
suggests
that
this
behavior
and
its
natural
releasers
may
be
widespread
in
the
ants.
LITERATURE
CITED
McCooK,
H.
C.
1882.
The
honey
ants
of
the
Garden
of
the
Gods
and
the
occident
ants
of
the
American
Plains.
J.
B.
Lippincott.
WHEELER,
W.
M.
1926.
Ants,
their
structure,
development
and
behavior.
Columbia
Uni-
versity.
WILSO1N-,
].
O.
1959.
A
chemical
releaser
of
alarm
and
digging
behavior
in
the
ant
Pogonomyrmex
badius
(Latrellle).
Psyche,
65:41-51
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Hindawi Publishing Corporation
http://www.hindawi.com Volume 2013
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2013
The Scientic
World Journal
ISRN
Molecular Biology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2013
International Journal of
Evolutionary Biology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2013