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Energy Saving through Trail following in a Marine Snail
Author(s): Mark S. Davies and Janine Blackwell
Source: Proceedings: Biological Sciences, Vol. 274, No. 1614 (May 7, 2007), pp. 1233-1236
Published by: The Royal Society
Stable URL: http://www.jstor.org/stable/25223917 .
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PROCEEDINGS
Proc- R' Soc- B (2007) 274' 1233-1236
-OF-T??
THEROYAL
doi:10.1098/rspb.2007.0046
^
27 February2007
online
SOCIETY JXJJ Published
Energy
in a marine
Mark
S. Davies
School ofHealth, Natural
Most
snails
and
we
produce,
and
trail following
snail
Janine Blackwell
and Social Sciences, University ofSunderland, Sunderland SRI
over
locomote
slugs
show
through
saving
3SD, UK
a layer of mucus
to
the resultant mucus
and although
trail is expensive
can be reduced
over
trail
When
fresh
by
following.
tracking
conspecific
that this expense
intertidal snail Littorina littorea(L.) produced only approximately 27% of themucus
trails, themarine
laid
over weathered
a
to recreate
snails. When
their mucus
trails, snails adjusted
by marker
tracking
production
convex
to the trail as originally
of similar
and thickness
trail profile
laid. Maximum
energy
shape
saving
occurs when
are little weathered.
laid trails which
and diverse
roles for
following
recently
Many
ecological
across
trail following
is
have been proposed.
the
that
role
the
and so
saving
Energy
only
applies
Gastropoda
may
to explain
help
Littorina
energy;
Keywords:
a well-established
is such
trail following
why
littorea', mucus;
1. INTRODUCTION
snails
Most
and
leave
slugs
trail as theymove. Although
almost
and
Hawkins
of locomotion is
extend
their
obvious
resolved.
Yet,
that
in
in marine,
loss
energy
to
with
gastropods
of mucus
(e.g. Calow
species
acts as
overhangs,
production
a significant
terrestrial
and
and
&
snails
allowed
terrestrial
the
represents
freshwater
those
for
plants.
locomotion
verticals
Davies
themucus
that
evolved
to
habitat
advantages
on
feed
in locomotion
its evolution
both
(1998) suggested that because
a role
glue,
thismode
in the Gastropoda,
are yet to be
functions
ubiquitous
ancillary
a silvery mucus
them
behind
1974;
Denny
1980a; Edwards & Welsh 1982; Horn 1986; Peck et al
et al 1990, 1992?>; Navarro & Torrijos
1987; Davies
to
thishigh cost, it seems unlikely that post
1995). Owing
of mucus-based
benefit
of mucus
functions
depositional
locomotion,
from
these
to
relationship
functions
be
vision
moving
tracking
Animals
difficult.
home (e.g. Delia
to aggregate
Cook
Stafford
et al
grazers.
trail
that are opportunistic,
the potential
existing mucus
We
over
the
which
with
limited
find
follow
& Davies
visual
might
their own
trails
or mate
2005)
it might
following
might
we examined
to reduce
to
(e.g.
costs
energy
the
trap
thus
deliver
food
of
benefits
a more
direct
by
locomoting
benefit:
over
that
substratum
because
mucus
trails may
both
a smoother
surface
produce
amount
of mucus
is
produced
and
to move,
the
reduced while animals are trailfollowing.Culley & Sherman
(1985) demonstrated that surface topography can influence
the amount
*Author
Accepted
of mucus
costs by 35 X (Davies ?ra/. 1992b).
We used the intertidal, rocky shore Littorina littorea(L.)
as
a model
required
6 February
2007
examine
of its widespread
Atlantic
and
because
energy
in trail
following
in the East
and West
of information
available
saving
distribution
of the wealth
on itsbiology. Its pedal mucus will begin to decay shortly
after deposition (Herndl & Peduzzi 1989), perhaps as
quick as 5-8 h after immersion (Davies & Beckwith 1999).
Edwards & Davies
(2002) suggested that the mucus of
ismost
littorea
1 -day
or
old
embedded
escence
to conspecifics
useful
in terms
less,
we
Here
microalgae.
when
of nutritional
used
profile
mucus
trails produced
tracker
by marker
between
relationship
the shore,
trail
and
the response,
animals
to weathered
fluor
trails,
a
giving
the thickness
tracker
and
in terms
are
through
conventional
and
thickness
the trails
benefit
mucus
to visualize
microscopy
of mucus
thickness. We
examined
time
of trail
of
animals,
the
exposed
on
of
thickness,
trails.
for locomotion
2. MATERIAL
AND METHODS
A Leitz
22EB
using
Dialux
an eyepiece
in the ormer
(mark. davies(a)sunderland.
ac.uk).
fluorescence
and
graticule
was
microscope
slide
calibrated
calibrated
to measure
the
diameters
of six lengths of stretched wire, each taped separately
to a microscope
slide. Each wire was then rotated through 90?,
with
to the slide
the
slide,
we
calibration:
transverse
was
its diameter
rotation
did
not
For
onto
the wire
re-measured
of the wire was
assume
section.
brushed
that its full length was
ensuring
and
units. The
focusing
that
to ensure
the wire
the re-measurement,
to provide
in contact
in microscope
a proper
a circular
had
talcum
a reference
point
powder
on which
to focus;
was focused on the powder particles on
the microscope
the slide on which
on the
the wire was
laid and then re-focused
powder
for correspondence
to
because
re-taped
trails.
hypothesized
stabilize
snails
surfaces
where
1992a),
While
the substratum
has been implicated in feeding (e.g.
1992). Mucus
Davies
of
range
is an energy-saving
then any saving
in
device
following
mucus
is more
since
the mucus
production
significant,
costs
of locomotion
the metabolic
production
outweigh
1994) and those of conspecifics
Santina
(e.g.
where
might
no
shows
suggested that trails
(1989)
in navigation
over
complex
used
on
trails deposited
will
species
a
Nevertheless,
has been proposed. Denny
might
all
trail following
snail;
Haliotis tuberculata.Tankersley (1989) demonstrated that
the locomotory force applied is reduced in trailfollowing, as
opposed to trail laying, in Littorina irrorata.But if trail
L.
the evolution
driven
not
occurrence
whose
phylogeny.
for the mucus
functions
have
since
behaviour.
of
units
11 January
Received1233
2007
particles
moved
This
on the surface
on
the
of the wire,
fine
graduated
journal
is ?
noting
the number
focusing
2007 The
Royal
knob.
Society
1234 M.
Diameters
recorded
between wire
=
r2
0.999,d.f.
Littorina
focusing
littorea
mm
shell
UK
length)
slides
(75X25
squares.
Double
with
etched
laid by
of a single mucus
snail to the beginning
a trail directly
on top of the single
as the marker
snail.
direction
it laid
of mucus
measurement
For
where
rehydrated,
trails
approximately
trails were
trail
that
in the same
trail,
mucus
thickness,
trails
seawater
in filtered
necessary,
a
introducing
trail such
for
10min. The slide was flooded with a 0.2% (w/v) solution of
the fluorescent
s. Small
30
volumes
The
hydration.
on
acridine
orange
the edge
of an etch
the mucus,
on
re-focused
of the mucus,
the upper
of
of the slide beneath
surface
noted.
of focusing units between
the two
were recorded
in this way
thicknesses
Mucus
at 10% divisions of the trailwidths.
assess
To
mucus
the effect of
decay,
single
at a semi-exposed
mid-shore
and
trails were
the rate of
trails were
mucus
site at Sunderland,
exposed
UK
(national
to a frame fixed on near-horizontal
fixed
rock
of wave
by cages to prevent grazer ingress. Degree
is not a significant factor in the rate at which
covered
exposure
mucus
littorea decays
of L.
and mucus
recovered
two tidal cycles,
one week
and
straddle
two and a half weeks.
two
and
out in a random
order over two months.
=
in filtered
(n
10) were kept submerged
measurement
for microscopic
=
(n
10) were
10) were
and
of dehydration
carried
controls
'Laboratory'
seawater
until required
'Field'
(a few minutes).
to and
from
the site
transported
a period
experienced
half-life
et al
(Davies
a half weeks
and
n=
tidal cycle,
The
12 days
(for which
Treatments
this period.
1992a).
is approximately
the pedal
were
Slides
after one
measured
of one week
the periods
1992a):
et al
(Davies
thickness
littorea pedal mucus
of L.
at
412 565). Etched glass slides with single
grid referenceNZ
mucus
on
of exposure'
'period
double
and
controls
so
they
to
prior
hydration
To assess
the effect
(typically 2 h post-laying).
of mucus
trails on the quantity
of single mucus
onshore
by tracker snails, single trails were exposed
produced
a
above. On return to the laboratory,
described
for the periods
being measured
of the decay
trail was
second
thickness^
was
of exposed
(n=l0
of tracker
thickness
the
thickness
the first to create
then measured
the thickness
determine
between
laid over
of
single
these
a double
per
double
To
the difference
snail mucus,
trails was
trail whose
treatment).
trails
the mean
and
fresh
trails
in the middle
were
a convex
showed
than
thicker
significantly
thickness
thicker
of 35.4
fresh
1.5
s.e.,
n=
single
were
10, though
=
slightly thicker at the 60% point (mean 37.7 jam?2.3
s.e.,
single
n=
trails were
10). Double
trails
Mann-Whitney
Proc. R. Soc. B
at
the
50%
test
(2007)
point
17=3.5,
thicker
significantly
um+1.1
s.e.,
(46.8
p<0.001).
At
the
p
=
double
20;
0.003).
By
more
27%
approximately
i.e. a tracker snail produces
of the mucus
of a marker
snail.
than
single
mucus
only
27%
approximately
When exposed onshore, the profiles of both double and
single trails became thinner and progressively flattened,
a trail was
though
detectable
cases
in both
after one week
(figure lb,c). No trail could be detected after two and a
half weeks' exposure. ANO VA showed that both at the
=
edge (repeated measures, n 20) and at the midpoint
reductions in
(n= 10), trails showed significant (p<0.05)
at each
thickness
increasing
and
treatment,
temporal
that
afterone week both single and double trailshad decayed to
the
same
11.0
their
profile:
different.
=
double
(Means
6.7
=
laying
=10.2
double
s.e.,
a
over
trail
not
significantly
6.1
um?0.57
edges:
single
s.e. Means
for midpoint:
urn?0.55
urn?1.4
were
thicknesses
for
urn?0.45
a mucus
s.e.,
=
single
s.e.)
that
trail
been
had
onshore for two and a half weeks (figure Id), animals
produced a convex deposit which was similar in profile to
that of single trails laid on glass (figure la). Statistical
that
showed
comparison
two
these
were
trail groups
not
=
significantlydifferent in thickness at themidpoint (L7 46,
=
on
laid
but
that
trails
p 0.759, n=l0),
single
glass
were
19.0
1.7
um?
over
s.e.;
decayed
w= 20 in both cases (U=
121, p
=
means,
trail = 14.0
week
=
glass
urn?0.7
s.e.,
0.032).
laying a trail over trails that had been
a much
or less, animals
produced
On
over
at the edges:
thicker
significantly
for one
onshore
flatter
deposit,
markedly differentfrom thatproduced on trails exposed for
two and a halfweeks (figure Id). An ANOVA on the data in
=
figure 1d revealed that at themidpoint (n 10), therewas a
in mean
difference
significant
thickness
(F5}54
=
225.96,
p < 0.001 ) and a post hoc SNK test showed trails grouped in
thickness (from thickest to thinnest) as two and a half
weeks > one week=two tidal cycles > one tidal cycle> field
=
control
measures,
laboratory
n = 20),
control.
At
there were
also
edge
(repeated
differences
significant
as two and a half
trails grouping
=
= one
tidal
tidal
cycle
cycles
In
the
control.
then,
general
?
< 0.001),
21.35,p
0^5,114
> one week > two
weeks
control
laboratory
> field
longer
mucus
the marker
snail's
the tracker
snail
mucus
and
example,
figure
energy
by
the
trail had
laid over
trail
been
following
the area
by determining
Id, an animal moving
over
onshore,
the more
animals
can
save
over
fresh
trails.
For
under
the
it. Thus
a two
tidal
curves
cycles-old
in
trail
produces only approximately 49% of themucus deposited
over
a two and
a half-week-old
trail.
The effect of tracker snails laying a relatively flat trail
over aged trails (figure Id) is to produce a total (marker+
tracker) trailprofile that is again convex (figure 2), largely
restoring the original trail profile and volume.
trails
(50%) point single trails had a
um?
(7=91.0,
trails
than at the edges, and fresh double
(figure la). At the mid
mean
were
cross-section,
20;
have
inmoving
calculated.
3. RESULTS
All
s.e.,
n=
s.e.,
trails,
On
the number
and
positions
the surface
on
a particle
on
focused
for
at
pipetted
to maintain
being measured
was
microscope
were
seawater
of filtered
seawater
in filtered
orange
the mucus
onto
intervals
regular
acridine
dye
1.7
um?
n=
determining the area under the curves infigure 1a, double
laid
only once. Trails were
an array of touching
onto
mm),
19.0
single
25.1um?0.6
and used
tracker
were
collected
grid reference NZ
of 4 days at approximately
seawater
urn)
were
(national
for a maximum
(0.2
microscope
1X1 mm
(12-18
seawater
in aerated
in filtered
(means:
atWhitburn,
stored
616),
12?C
(calculated for the 10 and 90% points combined), double
trails were again significantly thicker than single trails
28 to 107 urn; the relationship
linear (Pearson's
units was
ranged from
diameter
and
=
4,?<0.001).
from mid-shore
414
Snail trailfollowing saves energy
S. Davies & J.Blackwell
than
n=l0;
edges
4. DISCUSSION
In making
following,
used
claims
we
produced
make
mucus
about
the
energy
assumption
a constant
with
is proportional
costs. We
to energy
thus
trail thickness
and
in turn
saving
that
through
the
snails
trail
we
and
composition
content
to trail organic
regard
this assumption
as
Snail trailfollowing saves energy M.
S. Davies & J.Blackwell
(b)
(a)
fresh single
1235
control
laboratory
field control
1 tidalcycle
2 tidalcycles
trail
freshdouble trail
lweek
20 r
(d)
control
laboratory
-laboratory control
-field control
field control
1 tidalcycle
2 tidalcycles
-1 tidal cycle
-2 tidal cycles
lweek
-lweek
-2Vi weeks
20 h
10
10
20
10 %
30
40
50
across
divisions
60
70
80
90
of the mucus
the width
10
trail
20
10 %
30
50
40
across
divisions
60
70
80
1. Thickness
trails, (a) Fresh
trails laid in the laboratory,
Figure
profiles of mucus
single and double
(b) The
decay
after periods
of exposure
onshore,
of double
trails after periods
of exposure
onshore,
(c) The
decay
(d) Trails
over decayed
tracker animals
at the midpoint
Mucus
thickness measures
by subtraction).
single trails (obtained
did not
differ
reasonable
between
significantly
because
while
of laboratory
any pair
in
variations
and field
controls
as
stationary
substratum.
as mucus
trails.
In
adhesive
we
Thus
energy
an
attest
between
that
locomoting
over
a
locomoting
are
snails
over
by
shell
the
and
to
able
save
laid mucus
previously
fresh
the saving
of
trail,
costs as mucus
of energy
70%
is consider
approximately
able in the context
of an animal
that expends
much
energy
on mucus
are not
L.
While
values
for
littorea
production.
available,
literature
consumed
energy
of
estimates
on
expended
the
in
laboratory
and
1998),
for polyplacophorans
Horn
higher (68% inChiton pelliserpentis,
We
weeks'
over
were
onshore
exposure
such
a
amucus
to detect
unable
and
trail which,
terms
in
animals
of
its
to lay a mucus
appear
of
the
was
thickness,
the broad
substratum
via mucus
Nevertheless,
fresh,
2005).
'full thickness'
Proc. R. Soc. B
(2007)
to be
mechanism:
a minimum
trails
in propulsion
effective
since
snails
it appears
10
B
0
deposit
10
20
30
50
40
across
divisions
60
70
80
90
of the mucus
the width
trail
that they are unable
after
off mucus
to
trails
of
production
to adjust
warrants
their production
further
Maximum
over
double
periods
laid
exposure
entirely.
in the laboratory
onshore.
?=10
The
mechanism
over
in
by
which the snails perceive the quality of a trail and thus are
able
(Chan
mucus
2. Resultant
trails
single
each case.
switch
layerofmucus might be required for the coupling of foot to
et al
15 20
Figure
laid mucus
trail that recreates
locomotory
G 30
a half
profile of the trail as originally laid and this may be a
requirement
? 40
10 %
indistinguishable from a fresh 'single' trail. Indeed, tracker
animals
control
1week
21/2weeks
+i
1986).
trail after two and
tracker
even
be
may
trails
field control
1 tidalcycle
2 tidalcycles
50
gastropods
inermis (Paine
range from 7% in the nudibranch Navanax
1965) to 31% in the limpet Patella vulgata (Davies &
Hawkins
n=
0.001).
of single
of
proportion
mucus
ps<
trail
produced
by
and the edges
10 in every case.
mucus
pedal
composition in littorinid snails have been described
(Smith & Morin 2002), differences have been between
the mucus produced while moving and that produced
while
(ANOVAs,
90
of the mucus
the width
terms
explain
will
benefit
occur
why
of mucus
is unknown
and
investigation.
when
recent
from
trails
trails
trail
are
are
following
recently
followed
in
energy
laid. This
may
more
often
1236 M.
Snail trailfollowing saves energy
S. Davies & J.Blackwell
(Chapman 1998; Edwards & Davies 2002), rather than as
Edwards & Davies
(2002) suggested, that snails are
to
responding
the
increased
Nevertheless,
nutrition
enhancing
content
food
of
these
trails.
trail followingmay have the added benefit of
for microphagous
snails:
food
particles
may be embedded in themucus (Davies & Beckwith 1999).
Denny (19806) measured the thickness of themucus trail
of the
terrestrial
typically 10-20 urn using themethod of Lissman
on
crawled
Slugs
aluminium
foil
a thinner mucus
leave
trail than
those
slugmay
here,
though the fixingtechnique may have distorted the structure
of the trail. The
or profile
convex
shape
it is possible
that
of the trail was
the
shape
not given
here
reported
and
could
enhance the capacity of the trailforcollecting organic (food)
seawater.
from
particles
This
surface
a
is because
as opposed
to a flat profile,
area for organic
enrichment.
profile,
will
domed
trail
a greater
present
significant savings in energy through trail following
may help to explain why trail following is such a well
established behaviour. Littorinid snails usually move in
The
to
order
to
forage,
with
compatible
or
shelter
the purpose
a mate.
to find
Where
snails may
of the movement,
preferentially trail follow for the purpose of energy saving,
rather
than
any
reason
functional
other
in littorinids
following
manner
2002;
in an
opportunistic
(see Davies & Beckwith 1999; Edwards & Davies
see Davies & Hawkins 1998, for review) probably
because
are unable
snails
encounter
to detect
mucus
trails until
they
them.
Culley & Sherman
that mucus
demonstrated
(1985)
of the sub
the microtopography
on rough surfaces
to
laying more mucus
gastropods
on
smooth
surfaces.
than
and
Hence,
crevices,
varies
production
stratum,
fill pits
with
on rough
crawling
ofmucus
and
thank
energy
requires more
on a carpet of mucus
surfaces
trail following
could
circumstances
We
to occur
tends
in the
claimed
1998, for review). Trail
literature (see Davies & Hawkins
be particularly
two referees
in the form
under
such
beneficial.
Calow,
and
P.
on
observations
fluviatilis
Ancylus
contortus
and Planorbis
M?ll,
Linn. Oecologia 16, 149-161. (doi:10.1007/BF00345579)
N.
A.
Chan,
B., Balmforth,
J. & Hosoi,
and adhesive
better
lubrication
snail:
E.
a
2005 Building
locomotion.
Phys.
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