(19831, 19: 35-50. With 5 figures
Biologiral Journal ofthe Linrrran So+y
An experimental investigation of the behaviour
and mortality of artificial and natural morphs
of Cepaea nernoralis (L.)
S. M. TILLING”
Department of Food and Biological Sciences,
T h e Polytechnic o f h o r t h London,
Holloway Road, London .N7 8DB
Accepted for publication May 1982
Two population cage experiments which examined the mortality and behaviour of artificial and
natural morphs of the landsnail C. nemoralis ( L . ) are described. In the first experiment artificial
‘morphs’ were manufactured from one genetically homogeneous founder group of snails by painting
the shells black or white. Differences in behaviour and mortality between these two ‘morphs’ were
observed during the course of the experiment. Daylight and weather conditions were important in
determining the activity patterns of the two types of snail.
In the second experiment naturally occurring brown and yellow colour morphs were used. These
exhibited very similar behaviour patterns to those of their artificial ‘mimics’ and it is concluded that
phenotype must play an important role in determining the behavioural responses of the snails to their
environment. Thermal relationships are suggested as causal factors for the differences between the
experimental morphs.
KEY WORDS:-Landsnail
artificial morph
behaviour - thermal relations.
~
-
natural morph
experimental population cage
~
CONTENTS
Introduction . . . . . . .
Materials and methods.
. . . .
The experimental site and cages .
Behavioural observations .
. .
Climatic observations . . . .
Mortality . . . . . . .
Experiment A (artificial morphs) .
Experiment B (natural morphs)
.
Internal temperatures in empty shells
Analysis . . . . . . . .
Results
. . . . . . . .
Experiment A .
. . . . .
Experiment B .
. . . . .
Additional temperature data .
.
Discussion and conclusions . . . .
Acknowledgements. .
. . . .
References.
. . . . . . .
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36
37
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38
38
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39
39
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40
40
40
46
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49
49
Present address: Leonard Wills Field Centre, Nettlecombe, Nr Williton, Taunton, Somerset
35
0024-4066/83/010035
+ 16$03.00/0
~TJ
1983 The Linnean Society of London
36
S. M. TILLING
INTRODUCTION
Ninety percent of all direct solar energy reaching the ground lies in the visible
light and near infra-red range: wavelength interval 400-1500 nm (Watt, 1968).
Darkly coloured materials have low reflective coefficients (albedo) and absorb a
large proportion of the energy transmitted at these wavelengths, whilst paler
materials possess a high reflective coefficient and absorb only a fraction of the
energy available. As a result, dark inert materials attain higher temperatures than
their paler copies (Parry, 1951 ; Digby, 1955; Porter & Gates, 1969; Monteith,
1973).
These thermal relationships apply to life systems. Poikilothermic animals are
particularly sensitive to fluctuations in environmental temperature. For example,
variation in behaviour and wing coloration allows butterflies to exist in subarctic
conditions, increasingly melanic forms of many Lepidoptera being found in cooler
and more northerly habitats (Watt, 1968; Kevan & Shorthouse, 1970; Clark et al.,
1973). Other arthropods exhibit similar modifications, e.g. desert locusts (Stower
& Griffiths, 1966), tenebrionid beetles (Edney, 1971), sycamore aphids (Dixon,
1972) and molluscs. Desert snails tend to be white or very pale, their shells
reflecting 80-900,.:, of all direct solar radiation and thus reducing the heating effect
of the extreme insolation (Yom Tov, 1971 ; Schmidt-Nielson et al., 1971).
Cepaea nemoralis (L.) is a visually highly polymorphic landsnail widely
distributed in Western Europe. The considerable inter-colony variation in morph
frequency is distributed in such a way as to suggest that selective mechanisms are
involved (seeJones et al., 1977, for a review). That climate affects gene frequencies
in C. nemoralis and related species, is suggested by strong statistical associations
between gene frequencies and physical factors (e.g. Cain, 1968; Arnold, 1969;
Jones, 1973; Bantock, 1980). Additionally, subfossil data indicate that climatic
perturbations in the past 3000 years have been accompanied by shifts in morph
frequencies (Cain, 197 1) .
It is likely that climate may act directly as a consequence of shell colour and
banding. Shell phenotype has a direct influence on internal temperature in
C. nemoralis, both in living snails and empty shells (Heath, 1975; Garcia, 1977). I n
natural populations these differences in internal temperature may lead to
directional selection when lethal temperature limits are approached and exceeded
(Richardson, 1974). The relative reproductive success of various morphs may also
be affected by temperature (Wolda, 1967).
Thermal differences resulting from shell colour variation are obvious
mechanisms through which climatic selection could act. However, in some
localities, the effects of any climatic selection may be overridden by other factors
including selective predation (Cain & Sheppard, 1950; O’Donald, 1968),
interaction with related species (Arthur, 1978), local ‘coadaptation’ (Goodhart,
1963; Clarke, 1968) or micro-environmental and random processes (Goodhart,
1973). Furthermore, even if an association between shell colour and a particular
climatic factor can be demonstrated it is difficult to distinguish the effect of a
particular phenotypic trait as such, from any ascribable to the genotype as a whole
(Cain, 1977).
There is obvious need for work to be carried out under conditions in which such
factors can be controlled. In cages such as those described by Bantock (1974),
environmental heterogeneity, morph frequency, species composition, density and
location of the experimental populations can all be controlled. Previous population
BEHAVIOUR AND MORTALITY OF C. .SFMORALIS
37
cage experiments have demonstrated that significant differences in mortality
between morphs sometimes occur and that these are strongly indicative of selection
by climate (Bantock, 1974; Knights, 1979; Bantock & Ratsey, 1980). However,
due to possible undetected genetic variation between the morphs, these differences
in mortality could not be attributed directly to shell colour. This paper describes
two population cage experiments in which the effect of shell colour on behaviour
and mortality was examined. In the first of these, two artificially coloured ‘morphs’
were manufactured from one genetically homogeneous founder group of snails.
Cryptic genetic variation between snails was minimized by using only snails
collected from an area of less than one panmictic unit. The second experiment, in
which mortality and behaviour of two visually contrasting natural morphs were
examined, was initiated during the course of the first experiment. It provided an
indication of whether similarities might exist between natural morphs and their
artificial copies.
MATERIALS BND METHODS
T h e experimental site and cages
Cages described for previous experiments (see Bantock, 1974, 1980) proved
unsuitable for behavioural observations, and cylindrical cages (height 50 cm :
diameter 65 cm) contructed wholly of weldmesh (0.5 cm) were used instead. These
were enclosed below by 15 mm chicken wire and planted 10 cm in the ground.
Above, the cages were sealed by a removable weldmesh lid. After ‘planting’ of the
cages the earth was replaced so that the ground inside the cages was level with that
outside. The weldmesh and chicken wire excluded all vertebrate predators and
prevented escape of the snails. Two cages were used for each experiment ; the four
cages were planted (in a row 1 m apart) in a level site of mown grass on the valley
floor at the Leonard Wills Field Centre, Nettlecombe, Somerset (Grid Ref. ST03
05623765). The cages were planted with grasses, nettles (Urtica spp), dock (Rumex
spp) and ground ivy (Glechoma hederacea) in March 1978. During the course of the
experiments the vegetation was periodically thinned to facilitate observation.
Behavioural Observations
Previous trial observations showed that C. n a o r a l i s is crepuscular, peaking in
activity at dusk and dawn and becoming inactive during the day. Most
observations were therefore made at these ‘peak’ times. They were grouped into six
periods; Pre-dawn, Dawn, Post-dawn 1, Noon, Pre-dusk/dusk, Post-dusk. Where
activity was prolonged after dawn, additional observations were made and these
are referred to as Post-dawn 2. Observations in the dark were made by torchlight.
Behaviour was categorized as follows.
(i) Inactive. Body withdrawn completely into the shell with an epiphragm
sometimes present.
(ii) Becoming active/inactive. Foot slightly everted with the head and tentacles
not protruding. Ross (1979) found that protrusion of the posterior part of the
foot through the mantle cover in Otala lactea (Mull.) preceded either
38
S. M.TILLING
complete activity, or withdrawal and subsequent inactivity. This behaviour
probably allows secondary testing of the environment and can therefore be
accepted as a form of activity.
(iii) Completely active. Head and tentacles completely protruding and snail often
moving.
In the analysis the data have been considered as two groups-Inactive (group (i)
above) and Active (groups (ii) and (iii)).
Only the snails that were actually observed in any one scoring period have
contributed to the analysis, that is, snails which were not seen but were known to
be present were not included. I n order to avoid multiple inclusion of individual
snails in one observation period, the cages were subdivided by means of vertical
marker sticks passing downwards from the lid of the cages to the ground. During
the course of the experiment, numbers of snails aestivating on these sticks were
recorded.
Climatic observations
Weather during the behavioural observations was recorded and grouped as :
(i) Predominantly clear periods. Little or no cloud cover plus periods which were
intermittently clear. Irradiation under these clear/cloudy conditions in the
daytime can be 5-10% higher than that under completely clear skies
(Monteith, 1973).
(ii) Predominantly overcast periods. Cloud cover was extensive and persistent.
Temperatures inside the cages were simultaneously recorded by four
temperature probes placed around the inside perimeter of each of the cages, 3 cm
above the ground. Condensation, rainfall, wind strength and direction were also
noted. I n addition, temperature readings were taken on a vertical gradient within
both cages used in the first experiment (see below). O n 15June 1978 probes were
placed 0, 5 and 15 cm above the ground and simultaneous readings were obtained
at half-hourly intervals over a 24-h period.
Mortality
Cages were periodically scored for mortality. Dead snails were removed and not
replaced. As a result, density within the cages declined throughout the course of
the experiments.
Experiment A (artijicial morphs)
Three hundred yellow midbanded C. nemoralis were collected from one
population in West Somerset (Grid Ref. ST25 294523) on 20 May 1978. The
sample involved an area of less than 300 m--2.The snails were washed and placed
in individual containers (inverted plastic beakers) until they had aestivated. They
were then removed individually and their shells were painted with non-toxic
enamel paint (Humbrol quick-drying model paint) before being replaced in their
containers.
Half of the original 300 snails were painted black, and the other half white.
Later a coat of varnish (Blackfriar polyurethane matt clear) was applied to the
BEHAVIOUR AND MORTALITY OF C. NEMORALIS
39
shell and when this had dried the snails were removed and separated into two
groups of 75 black and 75 white painted snails.
The replicate groups were put out on 26 May 1978. Behavioural observations
were initiated on 5 June 1978 and continued until 24 August 1978. The snails were
scored for mortality on 18 and 25 July, 7 and 16 August, 6 and 26 September, 11
October, 1 and 16 November. The experiment was terminated on 30 November
1978.
Numbers of snails aestivating on the marker sticks inside the cages were noted at
noon on 19 days. Each of these observations were separated by at least two whole
nights and since most snails moved between these periods the observations are
considered to be independent of each other.
Experiment B (natural morphs)
One hundred and fifty brown unbanded (BO) and 150 yellow midbanded (Y3)
were collected on 13 August 1978 from the same population as that used for
experiment A. The snails were washed and varnished as before. Two replicate
groups of 75 BO and 75 Y3 were sorted and put out on 17 August 1978. Behavioural
observations were initiated on 4 September and continued until 13 November
1978. Mortality was scored on 26 September, 19 October, 3 and 24 November, 18
December 1978, 13 March 1979. Numbers aestivating on the marker sticks were
noted on 16 days.
Internal temperatures in emp8 shells
Four empty shells of each of the artificial ‘morphs’ used in experiment A were
cleaned and filled with gelatine solution. Their apertures were then sealed with
candle wax. Temperature probes were inserted into the apertures and the shells
placed in an exposed ground level outdoor site. Simultaneous half-hourly readings
were obtained from all eight shells over a 24-h period (on 25 June 1979). In the
same way, internal temperatures in four shells of each of the two morphs used in
experiment B, were recorded on 20 June 1979.
ANALYSIS
The raw data are available from the author.
(i) The log likelihood ratio G test (Sokal & Rohlf, 1969) was used to compare the
results obtained from the replicate cages for each experiment. This test permits
assessment of factor independence and interaction.
(ii) Comparison of activity and mortality between morphs has been made using
(Manly, 1973, 1974). This expresses the relative
the selective co-efficient,
levels of activity and mortality of morphs and is independent of absolute levels
of activity and mortality.
pi
The two morphs in each experiment form the two classes ( k = 2 ) . The value of fli
ranges from 0 to 1, with a value of 0.5 indicating that there is no relative difference
between the morphs. Magnitude of deviation from 0.5 (towards 0 or 1 ) indicates
the degree of difference between the classes. In the results presented below,
values exceeding 0.5 indicate that the dark morph used in each of the experiments
pi
S. M. TILLING
40
(black-painted or BO) has exhibited either higher levels of mortality or lower levels
of activity than its paler counterpart (white-painted or Y3) depending on which
data are being presented. fli may be calculated as follows:
fi
log (ri/Ai) /zf=llog ( r ~ ~ s )
where r and A are the numbers offered and remaining in each class k respectively.
RESULTS
Experiment .4
(1) Activity
An average of 85"{, of snails known to be inside the cages were seen during the
observation periods. There was no bias in detection between the two morphs.
The three-way G tests carried out on replicate data reveal that significant
interactions occurred in nine out of a total of 71 observations. The replicate cage
data were combined for analysis.
Seventy-one observations were made during the experiment. The data are
presented in nominal form (Table 1A) and also grouped into observations made
under contrasting light regimes (Table 1B). The Dawn observation period is
included in the 'dark' grouping because there was likely to be a lag in response
Table 1. Artificial morphs. A-Diurnal variation in the activity of black and white
painted snails. B-Comparison of activity under contrasting visible-light regimes
(see text for details)
Artificial morphs
A Period
(a) Pre-dawn
(b) Dawn
(c) Post-dawn 1
(d) Post-dawn 2/Noon*
(e) Pre-dusk/dusk
(f) Post-dusk
Total
Activity: No. of
observations
Total no. of
observations
BI> Wh
13
15
14
6
10
13t
8
11
8
1
6
5
5
4
6
5
4
7
71
39
31
Wh>Bl
Activity: No. of
observations
B Light regime
Bl>Wh
Wh>Bl
~
Predominantly dark (periods a, b, f,
Predominantly light (periods c, d, e )
24
15
16
15
* Due to the small number of observation periods during which snails were active, the two periods are
considered together.
t In one observation there was no difference in activity between the morphs, therefore this period has been
dropped from the analysis.
Bl=Black painted; Wh=white painted.
BEHAVIOUR AND MORTALITY OF C..MEMORALIS
41
time (i.e. the time the snails took to react to environmental stimuli) and visible
light was minimal at the outset of this period. Further subdivisions of data into
groups of observations made under differing weather conditions are given in
Table 2. Overall, blacks were more active than whites in 39 of the 70 observations
in which a difference in activity was detected between the morphs, but the
difference is not significant. The data suggest that there is an effect due to time of
day. Table 1B shows that blacks were more active than whites during periods of
darkness whilst there was no difference between the morphs during daylight
observations. However, these differences in morph activity levels between
‘daylight’ and ‘dark’ observation periods are not formally significant. Overall
mean values for the black morph have been plotted for each of the observation
periods (Fig. 1A).This clearly illustrates the drop in relative activity of this morph
between the dark Pre-dawn period and the daylight Post-dawn 2/Noon periods.
Although the trends outlined above suggest an overall effect due to time of day,
the lack of any formal significance means that the evidence provided by these data
should be treated as circumstantial. However, the differences between observations
made in daylight and dark periods become more apparent when weather
conditions are also considered. Table 2 shows that blacks were more active than
whites on only two out of a total of eight observations made in overcast daylight
conditions; in contrast, the darker morph was more active than its counterpart in
16 of the total of 23 observations made under clear dark conditions. This difference
is significant, G, =4.89, P ~ 0 . 0 5 .
Overall then, there is a clear indication that black painted snails were more
active than white painted ones in ‘dark’ rather than daylight conditions. This
difference is most pronounced and is formally significant when ‘dark’ clear periods
are compared with overcast daylight periods. Blacks appeared to be at their most
active, relative to whites, during the Pre-dawn and Dawn periods, particularly in
clear conditions in the latter period (Fig. 1B).
pi
(2) Activiiy and ambient tmperature
There is a significant correlation between relative activity
and ambient
temperature (“C) during the Dawn observation period (Fig. 2). Black painted
snails were less active than whites at higher temperatures but were more active
than their paler counterparts at lower temperatures, r,,, =0.633, P C 0.05. There
is also a temperature effect due to weather. Mean temperatures recorded during
(pi)
Table 2. Artificial morphs. Influence of weather and daylight on diurnal activity
patterns
Light regime
Predominantly dark
Predominantly light
BI=Black painted; Wh=white painted.
Cloudy
Clear
Actitity: No. of
observations
Activity: No. of
observations
BI> Wh
Wh>BI
BI > W h
Wh > BI
8
9
6
16
13
7
9
2
S. M. TILLING
42
-
Overall
I
I
"
\'
0.461'
0-
\
*L-<
&-
\
0.48 -
\
\
\
\
'
0
-0----0
..'
Activity:
BI>Wh
,O
\
\
0.50
Cloudy
c-- - 4 Clear
+\\
\
-4
0
-
0-
,
-1
\
& Wh>BI
-0
0.52 -
the Dawn observation period show that it was cooler in clear, than in overcast
conditions during this period, (Mann-Whitney) U= 2, P=0.004. Figure 1B shows
the effect of weather on the relative activity of the two morphs. This, as suggested
by the above correlation, is most pronounced at Dawn during which period the
relative activity of the black painted group of snails falls sharply in overcast
conditions but remains high in the clear (and significantly cooler) conditions.
o.60
t
A
0.551
A
T I
8
I
I
10
I
I
I
12
I
14
1
I
I
16
Temp ('C)
Figure 2. Relative activity and ambient temperature in artificial morphs during the Dawn obserx ation
period.
BEHAVIOUR AND MORTALITY OF C. NEMORALIS
43
There is therefore a clear link between weather, ambient temperature and relative
activity during the dawn period.
( 3 ) Aestivation site
The proportions of snails aestivating above the ground were low, but on 16 of
the 19 observation days a larger proportion of white painted snails aestivated on
marker sticks. This is significant, (Binomial test) P<O.Ol.
(4)Mortality
In each scoring period the data for the replicate cages were combined as there
are no significant interactions between the three variables (cage, morph,
mortality) during the course of the experiment. The overall cumulative mortality
for the two
for both morphs combined is given in Fig. 3A. Selective coefficients
morphs have been calculated for the mortality in each scoring period and are
plotted on Fig. 3B. There is a significant trend in selective mortality during the
course of the experiment: r,=0.796, P < 0.02. White painted snails survived less
well during the initial stages but as the experiment progressed the black morph was
the least successful ; by scoring period 9 levels of mortality were significantly higher
in the black painted snails; G, =6.21, PcO.05.
In summary, there were clear differences in activity between the two artifical
morphs when comparing observations made in clear periods of darkness with those
made in overcast daylight conditions. A smaller proportion of blacks chose
aestivation sites on marker sticks inside the cages and during the experiment
significantly more of this group died.
(pi)
0.7
CB
0.3 -
Selection
/
/
---
/
I
I
I
I
I
I
I
Scoring period
Figure 3 . A, Mortality in artifical morphs. OLerall cumulative mortality for both rnorphs combined. H,
Mortality in artificial rnorphs. Selection against the morphs during the coiirse of the experiment
(BI= black, W h = white).
S. M. TILLING
44
Experiment B
(1) Activi[y
Seventy-eight observations were made. An average of 83",, of the snails known
to be inside the cages were seen during the observation periods. There was no bias
in observation of either morph.
Significant interactions between the replicate cages occurred in 12 out of 78
observations. The data for both cages have been combined and are presented in
Tables 3 and 4. The analysis reveals pronounced differences in activities between
the morphs.
Table 3. Natural morphs. A-Diurnal variation in the activity of brown unbanded
(BO) and yellow mid-banded (Y3). B-Comparison of activity under contrasting
light regimes
Natural morphs
Activity: No. of nbservations
Total no. of
observations
A Period
a
(a) Pre-dawn
(b) Dawn
(cj Post-dawn 1
(dj Post-dawn 2
(e) Noon
(f) Pre-dusk/dusk
(9) Post-dusk
13
17*
7
7*
12
14
78
Total
BO>Y3
Y3 > BO
5
7
3
I
1
3
6
13
3
8
6
5
9
6
28
48
Activity: No. of observations
B Light regime
BO>Y3
Y3>BO
Predominantly dark
Predominantly light
20
15
33
8
* In two observations there was no difference in activity between the two morphs. These have been dropped
from analysis.
Table 4. Natural morphs. Influence of weather and daylight on diurnal activity
patterns
Cloudy
Activity: No. of observations
Clear
Activity: No. of observations
~
Light regime
Predominantly dark
Predominantly light
BO>Y3
Y3>BO
BO>Y3
YI>BO
5
8
15
7
4
19
4
I4
BEHAVIOUR AND MORTALITY OF C. .VEEMORALIS
45
BO were more acti\‘e than Y3 in only 28 of the 76 observations in which a
difference in activity was detected (Table 3A). The paler morph was therefore
more active overall, (Binomial test) P=0.029. However, Table 3B shows that BO
were more active than Y3 in 20 out of a total of 35 observations made in the ‘dark’.
In contrast, BO were significantly less acti\.e than Y3 in daylight, (Binomial test)
P= 0.002. This difference in relative activities of the two morphs between daylight
and ‘dark’ observations is very highly significant, G, = 11.76, P< 0.001.
It is clear then that the relative activity of the two morphs changes during a 24-h
period. Figure 4A shows clearly the overall drop in the relati\-e activity of BO
between the dark Pre-dawn period and the daylight Post-dawn 2/Noon periods.
By the Post-dawn 1 period BO were significantly less active than Y3, (Binomial
test) P=0.022 (Table 3 A ) .
There is also an effect due to weather. Table 4 shows that the difference in
relative activity of the two morphs between ‘dark’ and daylight periods is
particularly pronounced when comparing ‘dark’ clear periods with overcast
daylight periods. The dark morph (BO) was significantly less active in the latter
group of the observations, (Binomial test) P ~ 0 . 0 1 In
. contrast, BO were more
active than Y3 in ‘dark’ clear periods. The difference between the two groups of
observations (‘dark’ clear and overcast daylight) is highly significant, G, = 24.93,
P < 0.001.
0.46-
B
e
.9
\
\
0.48 -
\/
d/ \
\
\
-
- - - 4 Clear
P
\
\
B>Y
\
\
\
0.52
0-
\
/
0.50-
e - - 4 Cloudy
\\
//’
\
/+L- \
\
e
\
\
/
/’
\
\
/
\
b----\_
/
0.54
I
dawn
I
/
’
’
,.
/
I
I
dawn I
noon
YZB
dusk
I
dusk
Period
Figure 4, .A, Relative actkity of natural morphs. Overall. B, Relative activity of natural morphs under
contrasting weather conditions. Only groups consisting of three or more observations are plotted on the
graphs (R=brown iinbanded. Y =yellow mid-banded’.
46
S. M. TILLING
The effect of weather is shown in Fig. 4B. As with the previous experiment this
effect was most marked during the Dawn observation period. During this period
high relative activity is maintained by the dark morph (BO) in clear conditions but
this was reversed under cloudy conditions with the paler morph (Y3) exhibiting
higher levels of activity.
T o summarize-B0 were relatively more active than Y3 during the observations
made in the ‘dark’ compared with those made in daylight. This contrast was
particularly marked between ‘dark’ clear periods and daylight overcast periods-a
pattern similar to that observed in the artificial ‘morphs’ (these similarities appear
in a comparison of Fig. 4A and B with Fig. 1A and B).
In contrast to these pronounced intermorph differences in behaviour, no
significant association was detected between relative activity and ambient
temperature, nor were there differences between aestivation site, or between
mortality in the two morphs.
Additional temperature data
Readings taken on a vertical temperature gradient in the experimental site
showed that daytime temperature levels at ground level were often above 10°C
higher than those recorded 5 and 15 cm above the ground. The differences
decreased at night, ground temperatures being marginally lower than air
temperatures in the early evening.
Internal temperature readings in ‘empty’ shells of artificial morphs are plotted
in Fig. 5A. t-Tests indicate that black shells reached significantly higher
temperatures throughout most of the day. Most of the differences were highly
significant, and persisted until late in the evening (21.15 hours). Differences during
the night were negligible but during the dawn period (05.15 hours onwards)
temperature differences again appeared. By 07.15 hours internal temperatures in
black painted shells were again significantly higher than those in white painted
shells.
Diurnal readings in ‘empty’ shells of natural morphs are plotted in Fig. 5B. The
temperatures in BO were significantly higher than those of Y3 in most of the
afternoon readings. These differences disappeared by late evening. No detectable
difference was found during the night but a small difference appeared during the
dawn period until BO internal temperatures were again significantly higher than
those in Y3 shells by 10.30 hours.
DISCUSSION AND CONCLUSIONS
The experimental results provide strong evidence of a mechanistic link between
the behaviour of different morphs of C. nemoralis and climate.
The first experiment demonstrated behavioural differences between the artificial
‘morphs’, the direction of which suggest that thermal relations may be responsible.
The black ‘morph’ was at its most active, relative to the white ‘morph’, during
observations made in complete or semi-darkness and under little or no cloud cover,
particularly during the dawn period. It is likely that at dawn, short wave radiation
absorption in the visible and near infra-red ranges leads to differing internal
temperature levels in the two contrasting morphs and that these give rise to the
observed differences in activity.
BEHAVIOUR AND MORTALITY OF C. .WEMORALIS
47
3c
2c
IC
-
V
0
a
5
+
o
20
10
0
I
Noon
I
16.00
I
I
20.00
I
II
- --Y3
I
24.00
I
04.00
I
I
08.00
I
1
12.00
Time (hours)
Figure 5. Internal temperatures in gelatine filled shells. A, Artificial morphs. B, Natural morphs.
Cameron (1970) showed that activity in C. nemoralis rose sharply between 0 and
8°C and thereafter remained fairly constant until 22°C when it began to fall.
Richardson ( 1972) demonstrated a similar direct relationship between oxygen
consumption and ambient temperature. The results of these two laboratory
investigations suggest that C. n a o r a l i s has an optimal temperature range. There is
circumstantial evidence supporting the existence of such a range in a wide range of
poikilotherms, including the landsnail Helix aspersa (Mull.) (Newell, 1966, 1967 ;
Newell & Northcroft, 1967). Black painted snails are more likely to reach the
temperatures optimal for activity during the early stages of dawn and this would
lead to higher levels of relative activity in this morph during this period. This
‘thermal advantage’ would be particularly pronounced in lower ambient
temperatures (such as those experienced on clear mornings). However this ‘morph’
would also attain the higher incapacitating temperatures sooner than its paler
counterpart and accordingly become inactive more quickly. Previous observations
on natural morphs of C. za’ndobonensis support this interpretation of the results
(Jones, 1973). The significant relationship between increasing ambient
temperatures and falling relative activity of the darker (black) morph during the
dawn observation period provide further evidence ofjust such a link between the
phenotype and the environment. Internal temperatures in empty shells indicate
48
S. M. TILLING
that small differences in temperature between the two types appear during early
dawn. After dawn, white painted shells take up to 1 h longer to reach absolute
temperature levels equivalent to those measured in the black shells. Similar
temperature differences were probably experienced by the living snails during the
course of the experiment; Richardson (1972) shows that the presence of living
tissue does little or nothing to reduce the daytime temperatures reached.
Prolonged activity after dawn in the white painted ‘morph’ was accompanied by
an increased preference for elevated aestivation sites. These two behavioural
patterns may not be coincidental. Extension of activity into the early morning may
have enabled the white painted snails to detect temperature gradients which begin
to form at this time of day and consequently select aestivation sites which are less
likely to be subjected to unfavourable daytime temperature levels. Elevated
aestivation sites, even if only small distances above the ground, can be considerably
cooler than those on or just below the surface of the ground (Geiger, 1953;
Richardson, 1972). Mortality due to heat shock is a likely form of selection in
terrestrial molluscs including C. nemoralis (Richardson, 1974).
I n Helicella virgata (da Costa) climbing is probably an adaptive response to a
temperature gradient. Pomeroy (1969) showed that these snails moved into cooler
aestivation sites above the ground during the early morning thereby avoiding the
higher temperatures in which greater mortality occurs. Any phenotypic effect on
the choice of aestivation site by C. nemoralis, such as that seen in the artificial
morph experiment, could be of considerable importance if repeated by natural
morphs in free living populations. Observations made by Cain & Currey (1968)
suggest that this may occur in downland grass populations in the Marlborough
Downs; brown unbanded C. nemoralis were harder to find and this led the authors
to suggest that this morph was possibly ‘skulking’ in the vegetation to a greater
extent than the more exposed pink and yellow morphs. Richardson (1972) suggests
from casual observation that similar differences may have occurred in the sand
dune populations sampled by him.
Towards the latter stages of the first experiment there were significantly higher
levels of mortality in the black painted group of snails. This implicates phenotype
as being of importance in determining adult survival and the behavioural
responses to temperature must incriminate heat exhaustion as a possible causal
factor.
The results from the second experiment facilitate comparison between the
behaviour of the artificial ‘morphs’ and their natural models. Similarities are
striking and it seems reasonable to invoke a mechanistic response such as that
previously described for the artificial morphs.
In both experiments differences in activity were observed between the morphs
during periods in which visible light was apparently absent (Pre-dawn and Postdusk). Under these conditions all morphs, irrespective of visual properties would
act as black body radiators thus eliminating any thermal differences experienced
during the daylight periods (Monteith, 1973; Jones, 1978). There was no
difference in size between the morphs used in either of the experiments and
consequently small differences in thermal capacity cannot be the cause. A
physiological mechanism may be involved ; possibly an endogenous rhythm cued
by exogenous zeitgebers such as has been demonstrated in Helix aspersa (Bailey,
1975) and ilrion ater (L.) (Lewis, 1969).
The results of the two experiments are evidence of a link between phenotype and
BEHAVIOUR AND MORTALITY OF C. NEMORALIS
49
the environment in both natural and artificial morphs. The effect of activity
patterns on the overall fitness of the morphs is still unknown but in view of the
importance of behavioural adaptation to the environment in other terrestrial
molluscs it is likely that they are considerable (Pomeroy, 1969; Yom Tov, 197 1 ) . A
rather consistent feature of C. nemoralis is the increased frequency of the darker
brown colour morph in areas likely to experience cooler temperatures, particularly
at dawn. Bantock (1980) showed that selective mortality favouring this morph
occurred under cooler conditions. The experiments described in this paper ir dicate
that behavioural differences may also contribute to distributional patterns. For
example if increased activity at dawn were beneficial to overall fitness of the morph
by increasing mate-finding, ovipositioning success or by improving the quality of
food consumed, the darker morphs would be at an advantage in habitats likely to
experience lower dawn temperatures and this would be reversed in areas subjected
to increased insolation and higher ambient temperatures. However, the effect of
activity on overall fitness remains obscure and the nature of the interaction
between all major components of fitness will need to be investigated further before
generalized and predictive conclusions can be drawn.
ACKNOWLEDGEMENTS
I am grateful to Dr Cuillin Bantock for suggesting the field of study and for
assistance in the preparation of the manuscript. Thanks are due also to Mr D. R.
Perkins for helping in the running of the experiments, to Mr J. H . Crothers,
Warden of The Leonard Wills Field Centre, and to the staff of the Centre at
Nettlecornbe for their patience. This work was supported by a Science Research
Council grant (No. G/A/29227) awarded to Dr C. Bantock.
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