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~zologica/Jouma/of thp Linnean Sucietv (1999). 66;463-479. LVith 4 figurcs
Article ID: bijl. 1998.0281, availahlc online at http://~rww.idealit)rar)-.rom011
Character displacement, frequency-dependent
selection, and divergence of shell colour in
land snails Mandarins (Pulmonata)
SATOSHI CHIBA
Institute
of Biology and Earth Science, Shizuoka University, 836 Oya, Shizuoka 422, Japan
Received 4 April 1998; accepted f o r publication 20 3unp 1998
Endemic land snails of the genus Mandurina of the oceanic Bonin Islands offer an exceptional
example of habitat and character divergence among closely related species. In this study,
microhabitat differences between sympatric ground-dwelling species were studied by distinguishing habitats on the basis of vegetation and types of litter. In all sites where two
ground species coexisted, se,gregation occurred with each species showing preference for the
microhabitat in which they were found. When they were in sympatry, one species was
predominant in relatively wet and sheltered sites and the other in relatively dry and exposed
sites. Although most species can live in both types of habitat, occupation by one species is
inhibited by occupation by another. This suggests that competitive interaction between
sympatric species caused segregation. Except for populations that have undergone interspecific
hybridization, no examples were found of sympatric populations of two ground species
sharing a similar shell colour. Species that were predominant in rclati\dy wet and sheltered
sites possessed shells with dark coloration and their colour patterns were mostly of one type.
Species that were predominant in relatively dry and exposed sites possessed shells with bright
coloration and their color patterns were polymorphic. Most populations from areas in which
single species were distributed had shells with medium coloration. Microhabitat differentiation
between sympatric species possibly caused diversification of shell colour, because bright shells
are advantageous in sites where snails are largely exposed, and dark shells are advantageous
in sites in where they are mostly sheltered from sunlight. In addition, frequency-dependent
selection by predators hunting by sight may have operated to maintain colour polymorphism
in the populations which are restricted to exposed habitats by competition with other
sympatric species. This reveals the importance of interaction among closely related species
as a cause of diversification in ecological and morphological traits.
0 1999 The Linnean Society of London
ADDITIONAL KEY WORDS:-adaptive
radiation
~-colour
patterns
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polymorphisms.
CONTENTS
Introduction . . . . . .
Material and methods
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Study species and sites .
Analysis of habitat . .
Analysis of shell colour .
Results
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Variations in habitat
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Variations in shell colour
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466
467
467
469
469
470
470
472
466
S. CHIBA
Discussion . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements
. . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . .
476
478
478
INTRODUCTION
Interaction and coevolution among species play important roles in promoting
ecological and morphological diversification. If there is competition with individuals
of other species, closely related species living in the same area may partition the
available resources to avoid direct competition with one another. This leads to
divergence of habitat and morphology between the sympatric species (competitive
character displacement). Many studies have been performed to detect evidence of
character displacement and its significance in evolution from both theoretical and
empirical aspects. However, there is still much debate and many unresolved issues
regarding the process of character displacement (for a recent review, see Taper &
Case, 1992). It is important to detect empirical evidence of character displacement
and to understand the causal relationship between morphological and ecological
diversification.
Studies of organisms within an archipelago have provided excellent examples of
the process of ecological diversification and have clarified the causes of speciation
and ecological diversification (e.g. Grant, 1986; Grant & Grant, 1989). The island
endemics provide a simpler situation in which to examine ,relationships between
ecological and evolutionary processes. Mundurinu (Camaenidae) is an endemic land
snail genus that has undergone remarkable radiation within the islands. This genus
shows great diversification in shell morphology and lifestyle, and 16 species have
been described (e.g. Minato, 1978). Microhabitat divergence among sympatric
species has been found in the arboreal species of this genus (Chiba, 1996).
The present study focuses on microhabitat divergence and variations in shell
colour for eight ground-dwelling species from the islands of Chichijima, Anijima,
Hahajima and Imotojima. Two of these species sometimes coexist at the same site.
Although incidental hybridization occurs between two sympatric species in several
sites, they can, in most sites, coexist without gene exchange (Chiba, 1993).
Variations in body colour of an organism can provide a model case for studying
the relationship between morphology and ecology. The study of colour patterns of
land snail shells is one such example. The relationship between colour patterns of
gastropods and the environmental conditions of their habitats has been studied from
the aspects of temperature (Cain & Currey, 1963; Jones, 1973; Jones, Leith &
Rawlings, 1977; Heath, 1975; Clarke et ul., 1978; Etter, 1988; Stine, 1989), rainfall
(Emberton, 1982), predation (Cain & Sheppard, 1950, 1952, 1954; Heller, 1975;
Hughes & Mather, 1986), and selection operating on characters closely linked to
shell colour (Ewers & Rose, 1965; Berry, 1983). However, even in the same
environment, the effects of direct or indirect interaction between coexisting land
snail species may cause differentiation of their colour patterns. For example, the
divergence of colour pattern between sympatric species caused by frequencydependent selection is a result of an indirect interaction between the sympatric
species through predators that hunt by sight (Clarke, 1962, 1979; Allen, 1988). In
this paper, on the basis of my ecological and morphological studies of Mundurinu,
evidence for the following is presented: (1) differentiation of shell colour resulting
-
0
CHARACTER DISPLACEMENT OF LAND SNAILS
800km
46 7
Hahajima
15
H
$.m
ahiaja
‘Imotojima
7 --
Bonin Islands
-
0
2km
Meijima
24
Imotojima
.
0
2km
Chichijima
\
- O
2km
25
Figure 1. Map of the Bonin Islands, indicating sampling sites.
from direct interaction between sympatric species; (2) divergence of microhabitat
due to competitive interaction between sympatric species, causing divergence of
shell colour in sympatry; (3) one species’ inhibition of the occupation of a particular
microhabitat by other species; and (4)interaction between species producing variation
in shell coloration.
MATERIAL AND METHODS
Study species and sites
This study was conducted on four islands (Fig. 1) from 1992 to 1995. Eight species
of Mandarina were examined: M. mandarina Sowerby and M. aniimana Chiba from
Anijima, M. mandarina and M. chichiimana Chiba from Chichijima, M. hahajimana
Pilsbry and M. conus Pilsbry from Imotojima, and M. aureola Chiba, A4.polita Chiba
468
S. CHIBA
TABLE
1. A list of samples used in this study. Numbers of live specimens collected from each sampling
site are indicated. Numbers of empty shells (dead snails) found in each sampling 4te are indicated in
parentheses
~~
~
Number of specimens
Locality
1
2
3
4
5
6
7
8
9
10
11
12
13
1-1
15
16
17
18
19
20
21
M anijirnana
,ZL mandun'nn
38 (40)
35 (40)
-11 (3-1)
34 (36)
40 (56)
38 (50)
3 2 (-18)
-13 (72)
.If. pohta
20 (50)
22 (53)
45 (56)
45 (65)
40 (27)
14 (36)
24 (17)
,it ponderosa
Al. aureula
3 (2.5)
4 (20)
15 (18)
4 (20)
36
35
36
25
(55)
(48)
(33)
(29)
22
23
24
25
.\I. chtchyzmana
.\I. hahaymana
38 (38)
35(40)
38
40
37
39
43
(35)
(46)
(43)
(53)
(62)
25 (27)
40 (53)
A t conus
37 (35)
32 (38)
35 (46)
and A4.ponderosa from Hahajima. M. mandarina is distributed in the northern part of
Chichijima and in most parts of Anijima, and coexists with M. aniimana in the
central part of Anijima. Distribution of M. aniimana is restricted to the central part
of Anijima. A4. mandarina and M. chichiimana produce a hybrid zone (Chiba, 1997)
and each of them coexist with no ground species of Mandarina in Chichijima. In
Imotojima, M. conus coexists with M. hahajimana. In some areas of the southern parts
of Hahajima, iW.ponderosa coexists with &I. aureola. In some areas of the northern
parts of Hahajima, M. ponderosa coexists with M. polita. M. ponderosa is abundant in
the southern part of Hahajima, but is quite rare in the northern part. M. aureola
and M. pol& are distributed parapatrically; the latter was tentatively treated as a
subspecies of M. aureola by Chiba (1993). However, they are morphologically and
genetically distinct and are treated as different species in this study.
The animals used in this study were all adult snails that were taken by searching
in a relatively large (30m x 30m) site. In each sample locality every species of
Mandarina that could be found on the ground was sampled and recorded to compare
habitats and colour pattern. A total of 1 108 individuals representing 35 populations
of the eight species as collected (records of occurrence and sample sizes are given
in Table 1). The presence or absence of empty shells was also recorded in each site
to distinguish whether one species had either become rare very recently or had been
absent for a long time (Table 1).
CHAR KTCR IiIsPL1c:EhrEin OF IASD SNAILS
Anahsib o f habitat
Snails were mostly found under leaves, rocks and trunks. As each snail was found
in the sample locality, the material to which it was adhering, whether it was exposed
or hidden, and vegetation and types of litter of the site where it was found were
recorded. Vegetation was categorized as either forest and bush. In this study, bush
was defined as poor vegetation with plants shorter than 1 m. Forest litter was divided
into three types based on the dominant type of leaves: (1) palm (Litistonu chinensir),
(2) pandanus (Pundunus boninensi.,), and (3) broad-leaved trees, henceforth designated
forest litter (FL) types 1, 2 and 3. The leaf of FI,l is very large (more than 50 cm
in width and 50 cm in length). The leaf of FL2 is long (more than 50 cm) but narrow
(width of the leaf is approximately 1/10 of its length). The leaves of most FL3
species from the Bonin Islands are smaller than 10 cm in both length and width.
The litter dominated by FL1 is the thickest and wettest, that by FL2 is moderately
thin and dry, and that by FL3 is generally the thinnest and driest.
T o compare the environmental conditions of the sample localities, all were
investigated in the afternoon (12:OO-15:OO h) of the dry season (July and August)
when the snails were generally inactive, so that all records refer to resting sites. The
number of snails found at each site are not indicative of the absolute density, but
they probably reflect the true proportions of the species. T o examine the microhabitat
differences between sympatric species statistically, the differences in the number of
snails between the species for each factor that characterizes microhabitat differences
were estimated statistically with a X’ test.
Anabsis o f shell colour
Shell colour was examined using the following two methods. First, colour pattern
and banding polymorphism were described with a coding system (Cain & Sheppard,
1957; Cook, 1967; Cain, 1988). Each shell is divided into seven sections from the
uppermost to the lowermost part of the whorl (a-g, Fig. 2). Each section is assigned
one of three values depending on the pigmentation: ‘1’ if it is present, ‘0’ if it is
absent, and ‘n’ if it is present but the width of a band is less than one tenth of the
width of the whorl. Second, video was used to record images of shells; the intensity
of the pigmentation was measured and expressed numerically. Photographic images
of shells were also taken with a CCD camera under the same conditions, and saved
as PICT files on an Apple Macintosh. Measurements of the intensity of pigmentation
were performed on the Macintosh using the public domain Image program developed
at the U S . National Institutes of Health. The average and heterogeneity of brightness
(density of white dots) were calculated from each shell image. A high average
brightness indicates a bright coloration as a whole. The values range from 0 (black)
to 255 (white). A shell with large heterogeneity of brightness is one with high
contrast. A shell with clear colour bands against a light background and one with
obscure colour bands against a dark background have similar values of average
brightness, but the heterogeneity is different: the former has a larger heterogeneity
than the latter. Differences of mean and heterogeneity of brightness between
populations were statistically tested with ANOVA.
S. CHIBA
470
b
c
d
e
f
’
/
g
a b c d e f g
1010101
1111111
Figure 2. Positions of colour bands that were used to examine colour polymorphisms. Three examples
of colour patterns and their description by the coding system are shown.
RESULTS
Kzriations in habitat
An analysis habitats of each of the samples showed that sympatric species divided
the microhabitat so that each predominated in its own characteristic environment
(Table 2). M. aniimana, coexisting with M. rnandarina in the central part of Anijima,
was found in bush or in FL2 and FL3, but was not found in FL1. M. mandarina was
foundtat, but it was relatively rare in shrubs and in FL3 when it coexisted with M.
aniimana. The differences in occurrences of the two species with different vegetation
and litter types were statistically significant (P<0.05).
Similar relationships were found between sympatric species pairs M. aureola-M.
ponderosa and M. polita-M, ponderosa in Hahajima (Table 2). In the southern part of
Hahajima, M. aureola and M. ponderosa showed significant differences (PC0.05) in
preference of microhabitat when they were in sympatry. M, aureola was predominant
in shrubs or in FL2 and FL3, while M. ponderosa was predominant in FL1. M. aureola
S.CHIRA
472
TABLE
3. Variations of colour patterns and their frequency in the population. Abbreviations: niand.,
mandarina; anij., anijimana; chir., chichijirnana; poli., polita; aure., aureola; pond., ponderosa; haha., hahajiniana;
con., conus
Colour pattern/lTrrquency
1.0~.
--
1
Species
1011 110
n01 I I10
1111111
1111101
1 I I 1 110
mand.
I 00
13
0.21
mand.
1 00
nzand.
mand.
chic.
chic.
I 00
I 00
16
17
18
19
20
21
22
23
~
~
poli.
poli.
poli.
,%nd.
poli.
~
~
0 33
puli
uure.
pond.
aure.
pond.
aure.
pond.
pond.
aun.
pond.
awe.
25
0.11
~
0.95
I .00
I .U0
1 .00
0.98
0.98
0.93
0.57
0 75
~
~
~
0 14
~
0 12
0.31
~
~
~
~
~
0.I1
0.63
0.08
0.01
0.80
0.08
0. I3
0.1 1
~
~
-
0.50
0.13
0.33
0.35
0 94
0 83
0 20
0 56
U 98
~
0.13
0.05
0. I 5
0 19
~
0. I 1
0.03
~
0.02
-
0.48
0.08
0.18
haha.
~
ron.
~
0 88
0 83
~
0.09
~
~
~
0.04
0 05
0.1 1
~
con.
0.05
0.05
~
0.03
~
0 89
0.16
~
~
haha.
~
~
0. I 1
0 86
~
0 09
0 11
~
0.05
1 00
~
nure.
aure.
0.34
0 67
~
0 25
~
~
~
pori.
con.
24
-
~
p01i.
poli.
~
0.1 1
-
~
0.20
poiid
11
1 .i
10nOn00
-
~
anij.
3
4
5
6
7
8
9
10
11
12
nOnOn00
nOnOn01
~
anij.
2
lOnOl00
IOnOlOl
0.08
~
~
~
0.13
0.09
~
~
~
continued
was rare or not found in the FLl except for two populations (locs. 21, 22) that were
hybridized with M. ponderosa. In the northern part of Hahajima, M. ponderosa was
also found in FL3, but was not found in shrubs where M. aureola or M. polita were
abundant. M. polita was found in all kinds of microhabitat, but was relatively rare
or absent in FL3 in the localities where M. ponderosa was found. M. conus was found
in FL1, FL2 and FL3, in Imotojima, but was relatively rare in FL2 and FL3 where
it coexisted with M. hahajimana, which was restricted to these types.
Variations in shell colour
There was a consistent correlation between the differences in colour pattern and
microhabitat. Examination of colour bands (Table 3) and brightness of the shell
CHARACTER UISPIhCEhlENT OF IAND SSAI1,S
473
TABLE
3. continued
Colour pattern/Frequenry
1On0000
00110 100
I,OC
-
1
2
3
4
5
6
7
8
9
10
mand.
am].
mand.
anij.
mand.
mand.
chic.
chic.
poli.
poll.
12
pu/i.
13
pond.
pol;.
pond
pol;
aure.
pond.
16
17
sure.
18
am.
19
20
21
22
23
24
25
~
~
~
~
po1i.
pol;.
poli.
15
10 I0 I00
-
11
14
I0 10000
aure.
pond.
nure.
pond.
pond.
aure.
pond.
sure.
haha.
con.
haha.
con.
con.
~
~
0.07
~
~
0.I 0
~
~
~
~
~
~
~
(Fig. 3) showed that the three species possessing dark coloration-M, mandarina, M.
ponderosa, and M. conus-preferred FL1 when they were in sympatry with other
species. O n the other hand, the four species possessing bright coloration-M.
aniimana, M. aureola, M. polita and iVl. hahajimana-preferred FL2 and FL3 when they
were in sympatry with other species.
The geographical variation in colour pattern showed a consistent relationship
with the presence or absence of coexisting species (Fig. 3). Populations of M. aureola
from locs. 15, 18 and 19, where they coexisted with M. ponderosa, had colour patterns
00 10000 and 0000000 in higher frequencies (13- 16% in total) than populations
from locs. 16 and 17 (0% and 10% in total) where they lived alone, and the former
had significantly higher values (P<0.05) of average brightness (76.1-80.4) than the
latter (71.4 and 71.5). Populations of M. polita from locs. 12 and 13, where they
coexisted with M. ponderosa, had colour pattern 00 10000 in frequencies of 4-1 4%,
but populations from locs. 7-1 1, where they lived alone, did not have this type of
colour pattern. In addition, the former had significantly higher values (P<0.05) of
average brightness (75.1-75.9) than the latter (64.4-67.8). This implies that the
S. CHIBA
474
TABLE
3. continued
Colour oattern/Freauencv
1006100’ nOlOl00
-
1
2
3
4
5
6
7
8
9
10
11
12
13
mand.
an$
mand.
an$
mand.
mand.
chic.
chic.
poli.
poli.
poli.
poli.
14
15
16
17
18
19
20
21
22
23
24
25
-
-
-
-
pond.
-
pond
poli
awe.
pond.
aure.
awe.
aure.
pond.
awe.
pond.
pond.
aure.
pond.
aure.
haha.
con.
haha.
con.
con.
Others
-
poli.
poli.
poli.
0010100 0000000
~
-
-
0.05
-
-
-
-
-
-
-
coloration of M. aureola and M. polita is brighter when they coexist with M. ponderosa
than when they live alone. The differences of colour pattern between the two species
become distinct when they are in sympatry. One exception is the population from
loc. 21, where two sympatric species shared similar colour patterns. However, the
colour patterns of this population and another from loc. 22 had unique features.
These populations showed exceptionally large variations in colour patterns and
average brightness, but with low values in heterogeneity of brightness.
Colour polymorphism and divergence of coloration within a population were
found in the populations of M. aureola, N. polita, M. hahajimana and M. aniimana, all
of which had preferences for FL2 and FL3 (Table 3 and Fig. 4). When M. polita
coexisted with M. ponderosa, colour polymorphisms were found within the population,
but when it lived alone, no or minor polymorphisms were found in the colour
patterns (Table 3 and Fig. 4). Segregation of the values of mean shell brightness into
three groups was observed in the populations of M. aureola, reflecting polymorphism in
colour patterns. This was clearer in the populations coexisting with M. ponderosa
than in the populations living alone (Fig. 4).
There was no consistent relationship between shell colour and height above sea
CHARACTER DISPLACEMENT OF LAND SNAILS
475
-
1234-
56-
78910 11 12 -
P
4
1
131415 16 17 18 19 -
20 21 22
-
23 24
-
25 -
30
50
70
Mean
A mandarina
A anijimana
V chichcimana
90
V polita
ponderosa
0 aureola
10
20 30 40
Heterogeneity
50
0 hahajimana
conus
0 aureola (hybrids)
Figure 3. Variations in average (left) and heterogeneity (right) of shell brightness among the samples.
Horizontal bars indicate two standard errors of the values within each sample.
level of each sample locality. For example, there were no significant differences in
colour bands and average brightness between samples of M. politu from coastal areas
(locs. 7, 8, 9, 10) and samples from highlands (locs. 1 1 and 14). Samples of M. politu
from locs. 12 and 13 had brighter coloration than samples from other localities, but
there were no consistent environmental differences between these localities and
others.
S. CHIBA
476
50
100
50
E
100
5
.3
0
0
0
n
5
I
I
I M. ponderosa
z
10
I
I
I
,
10
I
50
100
Brightness
,
,
,
,
,
I
I
50
100
Brightness
1
10
50
100
Brightness
Figure 4. Distribution of average brightness in representative samples. Shell brightness of hl.polita and
hl. aureola is higher and more segregated into groups in the sites where they coexist with other species
than in the sites where they live alone. Another two species with bright shells, M. an@nana and M.
hahajrnana, also show segregation in brightness, but species with dark shells show no segregation in
brightness.
DISCUSSION
The analyses of habitat performed in this study suggest that there are significant
ecological difference between the sympatric species of Mundum'na on the Bonin
Islands. When two species coexist, one was predominant in FL3 or FL2 and the
other in the bush or FLl/FL3. The differences are consistent over the representative
sites among the different islands and among all of the species studied. In the highland
areas of Hahajima, one species was predominant in the forest litter and another in
the bush or under rocks. The litter dominated by FL1 is thicker and wetter than
that dominated by FL2 and FL3 while that dominated by FL3 is the thinnest and
dryest. This implies that one species is predominant in relatively wet and sheltered
sites and the other in relatively dry and exposed sites when they live in sympatry.
Although most species can live in both of these microhabitats, the occupation of
one species is inhibited by the occupation of the other. This suggests that cornpctitive
interaction between sympatric species caused segregation in the microhabitat.
Although the sites chosen were the resting sites, the differences may reflect the
preferences of each population, because foraging and resting sites tend not to differ
greatly.
Several studies have shown that interspecific competition may be the major cause
of differences in habitat or activity pattern of land snails. Asami (1988) suggested
that interspecific competition causes differences in the daily pattern of activity
between coexisting species. Diversification of habitat preference between sympatric
CH4RZCI'EK DISI'WCEhlENT OF LAND SNAILS
47 7
land snail species has been reported in studies of the arboreal habitat of Partula
(Johnson, Clarke & Murray, 1977; Murray,Johnson & Clarke, 1982; Murray, Clarke
&Johnson, 1993;Johnson, Murray & Clarke, 1993). The ecological diversification in
Mandarina indicates that divergence of microhabitat can occur between grounddwelling species.
Land snail shells are notorious for their intraspecific plasticity in colour patterns.
The association of geographical variations in colour patterns and environmental
heterogeneity has been documented in many studies. However, there are no
consistent relationships between the climates of sample localities and the geographical
variations in colour patterns ofMandarina. The present study shows that the presence
or absence of other species in sympatry produces differences in shell coloration
among local populations within a species.
The distributions of colour and banding morphs within and between the species
are such that very rarely do sympatric populations of two species share the same
morph. In addition, the differences in shell coloration observed between the two
species arc larger in the sympatric populations than in the populations that do not
coexist. A population from loc. 21 is exceptional in that it shows convergence of
shell colour between sympatric species, but this has been derived from interspecific
hybridization (Chiba, 1993). Colour patterns of M. aureola from locs. 2 1 and 22 have
become similar to those of M. ponderosa due to hybridization between these species
(Chiba, 1993). The exceptionally low values of heterogeneity of brightness o f these
populations relative to the other populations of h
i'. aureola reflect the dark ground
colour and obscure colour bands of these populations produced by hybridization.
The most obvious candidates for divergence of shell colour in sympatry is character
displacement due to differentiation in microhabitat between sympatric species.
Species that are predominant in relatively wet and sheltered sites (Ad.mandarina, M.
ponderosa, A4.conzu)possess shells with dark coloration and species that are predominant
in relatively dry and exposed sites (M. aniimana, M. aureola, M. polita, M. hahajmana)
possess bright coloration. This suggests that the microhabitat differentiation between
sympatric species possibly caused the diversification o f shell colour, because bright
shells are advantageous to snails dwelling in sites in which they have a greater
chance of being exposed, while dark shells are advantageous to snails dwelling in
sites in which they are mostly sheltered from sunlight. A dark shell would warm
more rapidly under sunlight and reach the temperature required for activity, and a
bright shell would be less likely to reach lethal temperatures in exposed, sunny
habitats (Jones, 1973; Heath, 1975; Jones, Leith & Rawlings 1977; Stine, 1989).
This implies that divergence of microhabitat resulting from competitive interaction
between species causes divergence of shell coloration in sympatry.
Another candidate for divergence is predators hunting by sight. Negative selection
resulting from frequency-dependent predation can cause divergence between sympatric species (Clarke, 1962, 1979; Allen, 1988). It had been believed that grounddwelling land snails in the Bonin Islands were not preyed upon by birds or other
predators that could discriminate colour. However, Suzuki (199 1) has shown that a
bird, Turdus dauma, which had been recently introduced in the Bonin Islands, and
whose main foods are land snails and other ground-dwelling invertebrates, has
increased in numbers. This species has the same niche as Turdus terrestris, an extinct
endemic bird species o f the Bonin Islands (Suzuki, 1991) which may have been a
predator of Mandarina. Therefore, the effects o f frequency-dependent selection by
predators cannot be ignored. This process, however, cannot by itself explain why
478
S. CHIBA
colour polymorphisms are found in the populations of M. polita coexisting with M.
ponderosa but are not found in the populations of M. polita living alone. The absence
of colour polymorphism in these species preferring unexposed microhabitats (M.
ponderosa, M. conus, and M. mandarina) and its presence in the sympatric populations
of species preferring exposed microhabitats (M, aureola, M. polita, M. hahajimana, M.
an@nana) indicate that snails of the latter group have a greater chance of being
exposed and found by predators than snails of the former, and that frequencydependent predation may have produced the polymorphism.
Competitive character displacement in land snails has been reported by several
authors (Schindel & Gould, 1977; Tillier, 1981; Murray, Johnson & Clarke, 1982;
Murray, Clarke &Johnson, 1993),but there has also been much criticism of its role
in their evolution (Emberton, 1995). Nevertheless, the present observations suggest
that competitive character displacement may be a cause of morphological diversification and make it clear that interaction among species cannot be ignored as
a cause of the conspicuous diversity of Mandarina.
ACKNOWLEDGEMENI'S
I would like to thank Drs B. C. Clarke, I. Hayami, and K. Tanabe for valuable
advice and discussion on this study.
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