J. Moll. Stud. (1999), 65, 355–370
© The Malacological Society of London 1999
INDIRECT EVIDENCE FOR ECOPHENOTYPIC PLASTICITY
IN RADULAR DENTITION OF LITTORARIA SPECIES
(GASTROPODA: LITTORINIDAE)
DAVID G. REID 1 and YIU-MING MAK 2
1
Department of Zoology, The Natural History Museum, London SW7 5BD, U.K. e-mail: [email protected]
2
Department of Ecology and Biodiversity, University of Hong Kong, Hong Kong.
Present address: Agriculture and Fisheries Department, 13/F, Canton Road Government Offices,
393 Canton Road, Kowloon, Hong Kong.
(Received 20 July 1998; accepted 10 November 1998)
ABSTRACT
In examination of radulae from all but one of the 36
species of the littorinid genus Littoraria we found
extraordinary intraspecific variation in those occurring on a range of substrates. Radulae from rock
showed a less well developed ‘hood’ on the rachidian
tooth, a strikingly enlarged major cusp on each of the
five central teeth, fewer cusps on the outer marginal
teeth and the radular ribbon was longer, when
compared with radulae of conspecifics from plant
substrates. The radulae of species found exclusively
on rock differed in similar ways from those restricted
to plant substrates (mangroves, driftwood and saltmarsh). We suggest that this may be an example of
phenotypic plasticity of radular form, induced by
substrate and/or diet, as recently shown experimentally in another littorinid genus. The mechanism
of inducible plasticity deserves further study.
Ecotypic variation in the radula may be widespread
in littorinids, and radular characters should therefore
be used with caution in studies of taxonomy,
phylogeny and adaptation.
INTRODUCTION
The radula has traditionally been used as an
important source of characters in gastropod
systematics, both for taxonomy and for phylogenetic reconstruction. The scanning electron
microscope is now routinely used for examining radulae, and systematists recognize the
need to assess variation in systematic characters of this kind. As a result, there has been a
growing appreciation of the extent of intraspecific variation in radular dentition and, in
some cases, an understanding of its causes.
For example, ontogenetic variation has been
described in Conus (Nybakken, 1990) and
in trochoideans (Warén, 1990), and intra-
individual variation in Peristernia has been
suggested as a case of fluctuating asymmetry
(Taylor & Lewis, 1995). Extreme variation
between individuals has been described in
littorinids (Reid, 1989, 1999) and lottiids
(Simison & Lindberg, 1999), and sexual dimorphism in dentition has been found in muricids
(Fujioka, 1985). The discovery in a sacoglossan
of two adult radular types correlated with
alternative algal foodplants suggested the
possibility that radular morphology might be
induced by diet (Bleakney, 1990). Recently,
this has been demonstrated experimentally in
Lacuna (Padilla, 1998). Consequently, the use
of radular characters in systematics must be
carefully assessed. Here we report a study of
the littorinid genus Littoraria, which suggests
both ecophenotypic plasticity and phylogenetic
constraint in radular form.
The Littorinidae possess a radula of the
taenioglossate type, with seven teeth in each
row, typical of many caenogastropods. In this
family, characters of the radula have been
employed at various taxonomic levels. The
basal notch of the lateral tooth has been used
to define the family itself (Troschel, 1858;
Rosewater, 1970, 1980; Arnaud & Bandel,
1978; but see Reid, 1989). Radular characters
have also been used in definitions of generic
and subgeneric groups (Powell, 1951; Rosewater, 1981, 1982; Bandel & Kadolsky, 1982),
and some have been suggested as synapomorphic characters of littorinid clades, as a
result of phylogenetic analyses (Reid, 1986,
1989, 1996). However, within clades of generic
and subgeneric rank, radular morphology is
often relatively uniform, and in only a few
cases have differences in dentition been
reported between closely related littorinid
species (Goodwin & Fish, 1977) or been used
356
D.G. REID & Y.-M. MAK
as diagnostic characters of species (Powell,
1951; Bandel & Kadolsky, 1982).
So far, only a few studies have attempted to
describe or quantify intraspecific radular variation among littorinids. These have demonstrated that both the form and number of cusps
of the radular teeth can show surprising variation, which again militates against the use of
radular characters for taxonomic purposes in
this family (Goodwin & Fish, 1977; Reid, 1988,
1996). The basis of this variation has been
largely unknown. In the genus Littorina the
tooth cusps of both juveniles and small adults
are narrower and more numerous than in
larger individuals, and it has been suggested
that an allometric effect may explain some of
the intraspecific variation in the radulae of
adults (Raffaelli, 1979; Rolán-Alvarez et al.,
1996; Reid, 1996).
It is generally assumed that there is likely to
be a close functional association between
radular form and diet. In herbivorous, grazing
gastropods this may extend to an association
with substrate type. However, only rarely has
radular function been tested by mechanical
studies of the action of teeth on algal substrates
(Padilla, 1985). In littorinids the functional
significance of radular design has instead been
inferred from interspecific comparisons and
correlations with substrate and diet. Rosewater
(1980) pointed out that littorinid species associated with macroalgae have a broad central
tooth and blunt cusps, while those grazing
microalgae from rocks in the littoral fringe
have a narrow central tooth and long, pointed
cusps. In the most well-studied genus,
Littorina, similar suggestions have been made
as a result of detailed comparison of dietary
components (Voltolina & Sacchi, 1990; Behrens
Yamada, 1992) and algal food preference
(Watson & Norton, 1985, 1987). Mapping of
radular characters together with diets on to a
phylogenetic tree has also supported an adaptive interpretation of radular cusp shape in
Littorina (Reid, 1996).
Against this background, the recent study of
radular variation in two species of the littorinid
genus Lacuna (Padilla, 1998) has produced an
extraordinary finding. According to the substrate on which they live, these snails graze
either the thallus of kelp, or the epiphytic film
on the leaves of eelgrass; snails from the former
have pointed tooth cusps, whereas those from
the latter have blunt cusps. By maintaining
adult snails in the laboratory on either substrate, it was shown that the cusp form of
newly-grown teeth changes according to diet.
The radula of Lacuna therefore shows inducible phenotypic plasticity. This has important
implications for the use of the gastropod radula
as a source of taxonomic and phylogenetic
characters, and for the interpretation of tooth
form as an adaptive response to natural selection.
Littoraria is a genus of 36 littorinid species,
distributed throughout the tropics (Reid, 1986,
1989, 1999). Many are found exclusively on the
roots, branches and foliage of mangrove trees,
but others can be found on saltmarsh plants,
driftwood and rocks in the littoral fringe, or on
a range of substrates. On wood and plant
substrates their diet is known to include a high
proportion of fungal hyphae (Kohlmeyer &
Bebout, 1986; Newell & Bärlocher, 1993), and
also some leaf material (Reid, 1986). The diets
of rock-dwelling species have not been investigated, but presumably include epilithic and
endolithic microalgae and lichens, as in other
littorinids of the littoral fringe (Reid, 1996).
Although not used for taxonomic purposes, the
radulae of Littoraria species have frequently
been illustrated (Reid, 1986, and review
therein). A recent taxonomic account of the six
Littoraria species of the Eastern Pacific
province (Reid, 1999) described two remarkable cases of intraspecific variation; in one case
(L. pintado pullata) this was correlated with a
substrate of algal or bare rock. The majority of
Littoraria species share a radular feature that is
unique in the family, an additional sharp edge
(or ‘hood’) anterior to the cusps of the central
(rachidian) tooth (Fig. 1). Rosewater (1980)
suggested that this functioned in connection
with grazing on substrates of wood and vegetation; however, some of the typically rockdwelling species have also been reported to
possess this type of rachidian (Reid, 1986). As
a result of cladistic analyses it has been
suggested that the hooded rachidian is a
synapomorphy of a large clade within the
genus (Reid, 1986, 1989).
In the light of the recent report of phenotypic plasticity in the radula of Lacuna (Padilla,
1998) the use of radular characters in phylogenetic analyses of littorinids must be reassessed.
In the present study we have examined radular
variation throughout the genus Littoraria, in
species found only on wood and plants, only on
rock, and in those that can be found on both. In
particular we have investigated the interspecific and intraspecific correlation between
the hooded rachidian and a habitat on plant
substrates, to test two competing hypotheses. If
the hooded central tooth is a synapomorphy
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
within the genus, no intraspecific correlation
with substrate is predicted, and interspecific
correlation will suggest that the character is
adaptive in relation to substrate. Alternatively,
if the hooded rachidian is environmentally
induced, both intraspecific and interspecific
correlations are predicted.
MATERIAL AND METHODS
Radulae of 191 individuals were examined, representing 35 of the 36 recognized species of Littoraria
(Table 1; following taxonomy of Reid, 1986, 1989,
1999); the only species for which no samples were
available was L. flammea (Philippi, 1847). In almost
all cases information was available on the substrates
from which the specimens were collected, whether
rock or plant material (mangroves, saltmarsh, driftwood, or algae). For those species occurring on both
rock and plant substrates, samples were taken from
both. All material was taken from the collection of
the Natural History Museum, London. A full list of
the localities of the samples is available on request.
The material includes 75 radulae studied by Reid
(1986), and 27 by Reid (1999).
Specimens preserved in alcohol were used for
extraction of radulae. Shell height (maximum dimension parallel to axis of coiling) was first measured
with calipers and the sex noted; the radula was then
dissected from the buccal mass, uncoiled, and its
length measured with an ocular micrometer (to 1
mm). In a few cases the radular ribbon was incomplete, so that length could not be measured. Only
adult specimens were used, close to maximum size
for the sample. Radulae were cleaned by soaking in a
bleaching solution (1% w/v sodium hypochlorite, 8%
w/v sodium chloride) at room temperature for up to
5 minutes, followed by gentle cleaning with fine
needles and thorough rinsing in distilled water. Each
radula was mounted damp on a thin layer of polyvinyl acetate glue on a glass coverslip, and the outer
marginal teeth quickly folded outwards with needles
before the radula had dried completely. Specimens
were coated with gold and palladium before examination in a scanning electron microscope. Only fully
formed and unworn teeth from the central part of the
radula (about 80% of total length) were examined.
Within this range, all teeth were inspected to check
for uniformity, but only a small part was photographed. Photographs were taken in three standard
orientations: flat view from vertically above (to
show shapes of teeth), at 45° from front end (to show
shapes of tooth cusps), and at 45° from side (to
show relief).
Each photograph included 5–12 tooth rows, and
counts and tooth descriptions were restricted to
these. For each radula, development of the ‘hood’ of
the rachidian tooth was recorded on a four-point
scale: absent (Fig. 1A, B), vestigial (Fig. 1C, D),
medium (Fig. 1E, F) and large (Fig. 1G, H). The
degree of enlargement of the major cusp (relative to
357
the smaller cusps) on each of the five central teeth
was recorded in four categories: subequal (Fig. 2A),
large (Fig. 2B), elongate (Fig. 2C) and very large
(Fig. 2D). The numbers of cusps on the outer
marginal teeth were counted on all visible teeth on
both left and right sides of each radula, and the
modal number noted for each side separately. Relative radular length was calculated as actual length
divided by shell height.
The relationships of both cusp number of the outer
marginal teeth and of the relative radular length
were tested against the substrate type (rock or plant)
by either one-way analysis of variance (ANOVA)
or (when either normality or homogeneity tests
were failed) by Kruskal-Wallis one-way analysis of
variance. Analyses were performed only on those
Littoraria species inhabiting both substrates. Tests
were first carried out within species (where sample
sizes were greater than 2), and the data from all
species inhabiting both substrates were then combined for an overall comparison between substrates.
For all these tests (both conspecific and combined),
balanced data sets were randomly selected for three
repeats of each test. Thirteen species were included
in the combined test for cusp number (Table 1) with
data from 22 individuals from each substrate type.
For the analysis for relative radular length, 11 species
were tested (Table 2) with 19 pairs of data. Owing to
variation in cusp number between the right and left
column of marginal teeth, analyses were carried out
separately on the two columns (counts from
either side could not be used as replicates in a single
analysis, since they were highly correlated).
RESULTS
Of the 35 Littoraria species included in the
study, 18 were available solely from mangrove
(or other plant) substrates, three were available only from rock, and 13 were found on
both plant and rock substrates. The substrate
was not recorded for the single specimen of
L. tessellata; this species is known to occur on
both rock and wood (locality information in
museum collections), and since the form of the
radula was similar to that of other wooddwelling species, it was tabulated accordingly
(Table 1).
Striking correlations were found between
radular form and substrate of collection, when
comparisons were made both within and
between species (Table 1). Of the three species
sampled solely from rocks, in L. glabrata (Fig.
1A, B) and L. mauritiana (Fig. 2C) the ‘hood’
of the rachidian tooth was vestigial or absent,
and the major cusps on the five central teeth
were elongate. In the third, L. cingulifera, a
medium-sized hood was present, and cusp form
varied from large to elongate. In all species
358
D.G. REID & Y.-M. MAK
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
359
Figure 2. Shape and size of the major cusp on each of the five central teeth of Littoraria species, showing four
classes used in descriptions. All radulae viewed at 45° from front. A. Cusps subequal, L. filosa (on mangroves,
Cockle Bay, Magnetic Island, Queensland, Australia; shell height 5 20.3 mm). B. Major cusps large,
L. carinifera (on mangroves, Lim Chu Kong, Singapore; shell height 5 20.9 mm). C. Major cusps elongate,
L. mauritiana (on rock, Pointe des Trois Bassins, Réunion; shell height 5 16.1 mm). D. Major cusps very large,
L. varia (on mangroves, Punta Morales, Golfo de Nicoya, Costa Rica; shell height 5 19.1 mm). Scale bars 5
100 mm.
available only from plant substrates the rachidian showed a large hood, and the major cusps
of the five central teeth were subequal or large.
Of the 13 species found on both rock and plant
substrates, the hood was less well developed
(absent, vestigial or medium) on rock in six
species, and equally developed on both substrates in the rest. In all but one of these 13
species the samples from rock showed more
unequal cusps of the five central teeth (i.e.
elongate cf. large; very large cf. large; large cf.
subequal). The exception was the single specimen of L. vespacea from rock, which did not
differ from conspecifics from mangroves. Only
one other anomalous radula was found; one of
the five radulae of L. varia from mangroves
Figure 1. Development of the ‘hood’ (arrowed) of the rachidian tooth of Littoraria species, showing four-point
scale used in descriptions. A, B. Hood absent, L. glabrata (on rock, Weligama, Sri Lanka; shell height 5 14.4
mm); two views of radula, flat (A) and at 45° from side (B), C, D. Hood vestigial, L. pintado (on rock, Baten,
Okinawa, Japan; shell height 5 17.7 mm); two views of radula, flat (C) and at 45° from front (D). E, F. Hood
medium, L. pintado (on green algae in rock pools, Bahia Santa Maria, Baja California, Mexico; shell height 5
8.8 mm); two views of radula, flat (E) and at 45° from front (F). G, H. Hood large, L. angulifera (on mangroves,
Twin Cays, off Dangriga, Belize; shell height 5 18.5 mm); two views of rachidian tooth, flat (G) and at 45° from
side (H). Scale bars 5 20 mm.
3
3
3
1
2
3
2
2
1
11
2
3
4
2
L. glabrata (Philippi, 1846)
L. mauritiana (Lamarck, 1822)
L. angulifera (Lamarck, 1822)
L. ardouiniana (Heude, 1885)
L. articulata (Philippi, 1846)
L. coccinea (Gmelin, 1791)
L. flava (King & Broderip, 1832)
L. intermedia (Philippi, 1846)
L. nebulosa (Lamarck, 1822)
L. pintado (Wood, 1828)
L. rosewateri Reid, 1999
L. scabra (Linnaeus, 1758)
L. undulata (Gray, 1839)
L. variegata (Souleyet, in
Eydoux & Souleyet, 1852)
L. vespacea Reid, 1986
L. aberrans (Philippi, 1846)
L. albicans (Metcalfe, 1852)
L. carinifera (Menke, 1830)
L. cingulata (Philippi, 1846)
L. conica (Philippi, 1846)
L. delicatula (Nevill, 1885)
L. filosa (Sowerby, 1832)
L. irrorata (Say, 1822)
1
3
N
L. cingulifera (Dunker, 1845)
Species
large
2 absent,
1 vestigial
absent
large
large
medium
absent
medium
medium
medium
2 absent,
9 vestigial
medium
large
2 absent,
2 vestigial
large
medium
Hood
subequal
very large
large
large
elongate
elongate
large
large
elongate
elongate
elongate
elongate
large
elongate
1 large,
2 elongate
elongate
Major
cusps
4
2
3.5 (3–4)
5 (4–6)
3 (2–3)
4 (3–4)
5 (4–5)
4
5 (3–5)
3
3
4
6.5 (6–7)
6 (5–8)
3 (3–4)
5 (2–7)
Outer marginal
cusps
Rock substrate
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
saltmarsh
mangrove
mangrove
mangrove
mangrove
driftwood
mangrove
mangrove
mangrove
algae in
rockpools
saltmarsh
mangrove
mangrove
Substrate
8
4
6
6
10
6
1
5
1
2
2
6
1
2
6
8
2
1
7
1
2
N
large
large
large
large
large
large
large
large
large
large
large
large
large
large
large
large
medium
medium
large
medium
medium
Hood
subequal
subequal
large
large
subequal
large
large
subequal
subequal
large
subequal
subequal
large
subequal
subequal
large
subequal
subequal
subequal
subequal
large
Major
cusps
Plant substrate
4 (4–6)
4.5 (4–5)
4 (3–5)
3 (3–4)
4 (4–6)
2
4 (4–5)
5
4
3*
5
6 (5–6)
4
6 (6–7)*
4 (3–5)
4 (4–6)
6 (4–6)*
4.5 (4–5)
5 (4–6)*
7
7 (6–7)
Outer marginal
cusps
Table 1. Radulae of Littoraria species examined, listed according to substrate of collection. The species are listed in three groups, first the three
species found only on rock substrates, then the 13 species found on both rock and plant substrates, and lastly those found only on plant substrates.
The substrate of collection for the specimen of the final species, L. tessellata, was not recorded, but from the radular form we predict that it was found
on a plant substrate. N 5 number of specimens. For states of hood of central tooth see Fig. 1, and of development of major cusps see Fig. 2. For the
outer marginal cusps, the overall modal number (mode of left and right modes of each individual) and overall range (of all tooth counts) are listed.
For intraspecific analyses of variance comparing numbers of outer marginal cusps on rock and plant substrates, significant results in any tests are
indicated by an asterisk; all other intraspecific comparisons of cusp number were non-significant (see text for details).
360
D.G. REID & Y.-M. MAK
2.5 (2–3)
6
large
large
mangrove
?
L. zebra (Donovan, 1825)
L. tessellata (Philippi, 1847)
3
1
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
mangrove
L. lutea (Philippi, 1847)
L. luteola (Quoy & Gaimard, 1833)
L. melanostoma (Gray, 1839)
L. pallescens (Philippi, 1846)
L. philippiana (Reeve, 1857)
L. strigata (Philippi, 1846)
L. subvittata Reid, 1986
L. sulculosa (Philippi, 1846)
L. varia (Sowerby, 1832)
3
5
9
8
5
5
6
6
5
large
large
large
large
large
large
large
large
large
large
subequal
large
subequal
subequal
large
subequal
large
1 subequal,
3 large,
1 v. large
large
subequal
3
4 (3–5)
3 (2–3)
4 (3–4)
5 (5–6)
4
5 (4–6)
4
2 (2–3)
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
361
showed very large major cusps (Fig. 2D), differing from the others with subequal to large
cusps. In neither these anomalous radulae, nor
in any others, did the development of hood or
tooth cusps change along the length of the
radula. The contrast of radular form on rock
and plants is clearly shown in Figures 3 and 4.
The shape of the tips (e.g. blunt or pointed) of
the major cusps of the five central teeth did not
show any correlation with substrate.
Possible correlation between the number of
cusps on the outer marginal teeth and the substrate type was confounded by variation both
within individuals and within species. Variation
within a column of teeth was uncommon, thus
justifying use of the modal number in analyses;
in only 4.3% of observed columns of outer
marginal teeth did cusp number vary by 1
within the column, and in 0.9% the number
varied by 2 (note that counts were restricted to
the 5–12 rows on the photographs). Variation
between left and right columns was more
common; of 162 radulae for which counts of
outer marginal cusps were available for left and
right sides, in 20% of cases the modal numbers
for the two sides varied by 1, and in 0.6% by 2.
The number of outer marginal cusps ranged
from 2 to 8, and the total range of variation
within each species is given in Table 1. Considering those species found on both rock and
plant substrates, in 10 of the 13 species the
overall modal number of cusps was smaller in
the sample from rock. Of the intraspecific tests,
only the following were significant: in the left
column, two out of three tests for L. angulifera
(ANOVA, d.f. 5 1,3, P , 0.001), and all three
tests for L. intermedia and L. variegata
(ANOVA, d.f. 5 1,3, P , 0.001); in the right
column, one out of three tests for L. scabra
(ANOVA, d.f. 5 1,5 P , 0.001), and all tests
for L. coccinea and L. variegata (ANOVA, d.f.
5 1,3, P , 0.001). For the combined data, all
tests were significant (Kruskal-Wallis, d.f. 5 1;
left test, H 5 8.225, P 5 0.004; left test 2, H
5 6.684, P 5 0.009; left test 3, H 5 5.252, P
5 0.022: right test 1, H 5 6.18, P 5 0.013; right
test 2, H 5 5.673, P 5 0.017; right test 3, H
5 5.566, P 5 0.018), showing that individuals
from plant substrates possess more cusps on
the marginal teeth than those from rock
substrates.
In the 18 species found only on plant substrates the mean relative length of the radula
ranged from 0.594 to 1.783, and in the three
found only on rocks from 1.43 to 4.50 (Table 2).
Comparing conspecific samples from rock and
plants (Table 2), in 10 of 11 cases the mean
362
D.G. REID & Y.-M. MAK
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
363
Table 2. Relative radular lengths (length/shell height) of Littoraria species according to substrate of
collection. Species are arranged in three groups (found on rock only, found on rock and plants, found
on plants only) as in Table 1. Note that radular length was not available for all the specimens listed in
Table 1. N 5 number of specimens. s.d. 5 sample standard deviation.
Species
Rock substrate
N
L. cingulifera
L. glabrata
L. mauritiana
L. angulifera
L. ardouiniana
L. articulata
L. coccinea
L. flava
L. intermedia
L. nebulosa
L. pintado
L. rosewateri
L. scabra
L. undulata
L. variegata
L. vespacea
L. aberrans
L. albicans
L. carinifera
L. cingulata
L. conica
L. delicatula
L. filosa
L. irrorata
L. lutea
L. luteola
L. melanostoma
L. pallescens
L. philippiana
L. strigata
L. subvittata
L. sulculosa
L. varia
L. zebra
L. tessellata
1
3
1
3
1
2
3
1
2
1
11
2
2
4
2
1
Relative radular length
(mean 6 s.d.)
1.43
2.177 (6 0.347)
4.503 (6 1.09)
1.267 (6 0.186)
0.94
1.320 (6 0.057)
1.840 (6 0.286)
1.75
1.345 (6 0.191)
1.74
2.710 (6 0.875)
1.285 (6 0.544)
1.125 (6 0.120)
2.428 (6 0.487)
2.000 (6 0.198)
?
Plant substrate
N
Relative radular length
(mean 6 s.d.)
3
6
8
2
1
6
1
2
2
8
1
2
7
3
6
6
6
6
1
5
1
3
5
9
8
5
5
5
5
4
3
1
0.967 (6 0.057)
0.800 (6 0.156)
1.095 (6 0.230)
?
1.16
0.977 (6 0.128)
0.87
2.250 (6 0.198)
0.950 (6 0.071)
1.154 (6 0.221)
1.14
1.470 (6 0.085)
1.217 (6 0.245)
0.680 (6 0.053)
0.702 (6 0.093)
1.050 (6 0.167)
0.772 (6 0.088)
1.195 (6 0.258)
0.76
0.770 (6 0.143)
1.45
0.910 (6 0.036)
0.594 (6 0.069)
0.887 (6 0.167)
0.850 (6 0.188)
0.690 (6 0.060)
1.362 (6 0.221)
0.836 (6 0.065)
0.800 (6 0.089)
1.253 (6 0.394)
1.783 (6 0.208)
?
Figure 3. Contrasting form of radular tooth cusps in pairs of conspecific Littoraria from rock (A, C, E, F) and
from plant substrates (B, D, F, H). Two of these four species are frequently found on both substrates (L. coccinea, L. nebulosa), whereas the others (L. pintado, L. undulata) mainly occur on rock. All radulae viewed at
45° from front. A, B. L. coccinea (A. On rock, Manono-uta, ‘Upolu, Western Samoa; shell height 5 18.1 mm.
B. On driftwood, Green Island, Queensland, Australia; shell height 5 10 mm). C, D. L. nebulosa (C. On rock,
20 km south of Campeche, Mexico; shell height 5 14.4 mm. D. On mangroves, Blue Ground Range, off
Dangriga, Belize; shell height 5 28.9 mm). E, F. L. pintado (E. On rock, Bahia Santa Maria, Baja California,
Mexico; shell height 5 7.2 mm. F. On green algae in rock pools; Bahia Santa Maria, Baja California, Mexico;
shell height 5 8.8 mm). G, H. L. undulata (G. On rock, Xi Zi Bay, Kaoshing, Taiwan; shell height 5 17.9 mm.
H. On mangroves, Ishigaki, Okinawa, Japan; shell height 5 10.5 mm). Scale bars 5 100 mm.
364
D.G. REID & Y.-M. MAK
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
length was greater on rocks, although none of
the individual comparisons was significant.
However, all three analyses of the combined
data from these 11 species showed that the
relative radular length on rock was longer
than that on plant substrates (Kruskal-Wallis,
d.f. 5 1; test 1, H 5 5.527, P 5 0.019; test 2,
H 5 5.459, P 5 0.019; test 3, H 5 6.603, P
5 0.01; similar results were obtained if the ratio
data were first arcsine transformed).
No sexual dimorphism in the characters
described was seen in the radular morphology
of the Littoraria species.
In summary, there is not a single radular type
on rock and another on plant substrates across
the entire genus Littoraria, but rather a range
of radular types occurs on each, with some
overlap between them. Within species the
radulae from the two substrates are strikingly
different: radulae from rock substrates show a
less well developed rachidian hood, conspicuously enlarged or elongated major cusps on the
five central teeth, and the radular ribbon is
longer. The same trends are found when interspecific comparisons are made between species
occurring solely on one or other substrate. In
intraspecific comparisons, radulae from rock
also show fewer cusps on the outer marginal
teeth.
DISCUSSION
There are several possible explanations for the
striking correlation between substrate and
radular morphology within species of Littoraria. (1) The distinct radular types might
belong to pairs of cryptic species within each of
the 13 taxa recorded from both rock and plant
substrates. However, closely related species of
this genus are almost always distinguished by
the shape of the penis (Reid, 1986, 1999), and
no such anatomical difference has been found
between animals from alternative substrates.
(2) The 13 species might be polymorphic for
radular morphology, with geographically or
ecologically segregated populations genetically
365
adapted to rock or plant habitats. At least in
three species (L. articulata, Fig. 4C, D; L. intermedia; L. scabra) the distinct radular types
were found on their respective substrates at the
same locality. Ecological segregation of populations remains a possibility, although since all
Littoraria species have planktotrophic development and are probably widely dispersed during
a pelagic phase of about 4–10 weeks (Reid,
1986), this would require settlement of larvae
on appropriate substrates, and/or strong postlarval selection. (3) Again assuming genetic
control of radular form, there might be intrapopulation polymorphism combined with
substrate preference and/or strong selection, to
achieve matching of radular morphology with
substrate. (4) The radula may be phenotypically plastic, and the appropriate morphology induced by the substrate or diet.
Possibilities (2) to (4) cannot be unequivocally
distinguished without experimental transfer of
individuals between substrates, as used by
Padilla (1998) to demonstrate inducible plasticity in the littorinid Lacuna. In this study we
have not found any direct evidence for change
in radular form within an individual (but, as
discussed below, natural transfer between substrates is likely to be a rare event). Nevertheless, we suggest that inducible plasticity may
explain the near-perfect correlation of radula
and substrate (2 exceptions in 191 radulae
examined) that we have reported.
If this is indeed the case, and assuming that
radular plasticity is a heritable trait, then it may
be subject to natural selection and may be an
adaptive character (sensu Gould & Vrba,
1982). Padilla (1998) suggested that a plastic
radular morphology was adaptive for a species
in a temporally or spatially variable environment, in which individuals regularly experience
shifts of habitat during their lifetime. This may
well be so in the studied Lacuna species, which
are regularly found on both kelp and eelgrass
substrates, and probably frequently disperse
between the two, both as a result of planktotrophic development and their habit of drifting on mucous threads as juveniles and adults.
Figure 4. Contrasting form of radular tooth cusps in pairs of conspecific Littoraria from rock (A, C, E, G) and
from plant substrates (B, D, F, H). These four species are all most frequently found on mangroves, and less
commonly on rock. All radulae viewed at 45° from front. A, B. L. angulifera (A. On rock, Jupiter Inlet,
Florida, USA; shell height 5 17.1 mm. B. On mangroves, Twin Cays, off Dangriga, Belize; shell height 5 18.5
mm). C, D. L. articulata (C. On rock, St John’s Island, Singapore; shell height 5 10.4 mm. D. On mangroves, St
John’s Island, Singapore; shell height 5 13.5 mm). E, F. L. intermedia (E. On rock, Inoda Harbour, Ishigaki,
Japan; shell height 5 12.2 mm. F. On mangroves, St John’s Island, Singapore; shell height 5 17.9 mm). G, H. L.
variegata (G. On rock, Topolobampo, Sinaloa, Mexico; shell height 5 15.9 mm. H. On mangroves, Punta
Morales, Golfo de Nicoya, Costa Rica; shell height 5 20.3 mm). Scale bars 5 100 mm.
366
D.G. REID & Y.-M. MAK
However, this argument does not apply so
convincingly to most Littoraria species. The
majority of these are found exclusively (or
almost so) on mangrove or other vegetation,
or (less commonly) are restricted to rock
substrates (Reid, 1986, 1999). Furthermore,
although larval dispersal is probably widespread, that of adults may be restricted, since
the snails occupy habitats above the water
level, usually on shores sheltered from strong
wave action. Of the species recorded from both
substrate types in our study, only six (L.
angulifera, L. articulata, L. coccinea, L. flava,
L. intermedia, L. nebulosa) are known to be
found frequently on each (Reid, pers. obs.). It
is remarkable that dimorphism of the radula is
found not only in these eurytopic species, but
also in such stenotopic species as L. pintado
and L. undulata, both found almost exclusively
on rocks, and in typically mangrove-associated
species such as L. scabra and L. variegata. In
these stenotopic species the potential to modify
the radular teeth according to the substrate
must seldom be realized.
As defined by Coddington (1988), adaptation in a phylogenetic context is ‘apomorphic
function promoted by natural selection, as
compared with plesiomorphic function’. It is
therefore a relative concept (like apomorphy
and plesiomorphy), depending upon the level
in the phylogenetic hierarchy at which it is
considered (Coddington, 1988, 1994). Assuming that the radula is indeed plastic in those
Littoraria species in which we have found
dimorphism, and if this character is superimposed on the available phylogenies of this
genus (Reid, 1986, 1989), parsimonious reconstruction suggests that this is a plesiomorphic
trait in the whole generic clade. If so, the interspecific differences between Littoraria species
restricted to one or other substrate may be
ascribed to the same cause. Furthermore,
according to Reid’s (1989) phylogeny of the
Littorinidae, the most recent common ancestor
of Littoraria and Lacuna is also the ancestor of
the entire family Littorinidae. Perhaps, then,
this trait is plesiomorphic within the family, and
might be predicted to occur in other littorinids.
(Note that the state of this character in appropriate outgroups would have to be known
before it could be argued at what level it is a
synapomorphy). Striking intraspecific variation
of radular cusps has been recorded in several
other littorinid genera, but there is only a little
evidence to indicate a connection with substrate, and the possibility has not previously
been discussed. For example, in Bembicium
auratum specimens from mangroves had
shorter and more rounded cusps than those
from rocky shores (Reid, 1988: fig. 19g from
mangroves, others from rocks; habitat data not
recorded in original publication). In Littorina
subrotundata some specimens from sheltered
shores (including salt marshes) had bluntly
rounded cusps and those from exposed rocky
shores had pointed cusps, but substrate details
were seldom available (Reid, 1996: 171–174,
fig. 64). Examination of specimens of Cenchritis muricatus from both wood and rock substrates has revealed a small rachidian hood only
in the former (Reid, unpublished). If plesiomorphic within the Littorinidae, radular plasticity cannot be considered adaptive in either
Lacuna or Littoraria alone (although it may
still be functional). Instead, if plasticity were
shown to be a synapomorphy of the Littorinidae, the character might be considered as an
adaptation of the family-level clade; Padilla’s
(1998) adaptive hypothesis might then apply to
the common ancestor in which the trait was
first selected. In functional terms, ecophenotypic induction of radular form is probably
selectively advantageous in those many littorinids which occur in the spatially and temporally variable environment of shallow-water
and intertidal hard substrates. The trait has
apparently persisted in Littoraria species of
more stenotopic habit.
Little is known about the mechanism of
radular induction. In Lacuna the teeth are
generated at the rate of about three rows per
day, so that two to six weeks are required for
replacement of the entire radula, consisting of
47 to 99 rows (Padilla et al., 1996). In the laboratory, adult snails transferred to a different
substrate modified their radular teeth within
eight weeks (Padilla, 1998). The rate of
replacement in three Littorina species is five to
six rows per day at 20°C, and is strongly dependent on temperature (Isarankura & Runham,
1968). The replacement rate in Littoraria is not
known, but the number of tooth rows varies
from 220 in L. luteola to 1800 in L. mauritiana,
so that replacement of the entire radula is
likely to be a slow process. The time required
for effective induction of tooth morphology
must be at least as long as this. (Recent transfer
between substrates, with insufficient time for
induction, might possibly account for the two
observed cases of tooth morphology apparently inappropriate to the substrate). In littorinids the length of the radula relative to that of
the shell shows considerable variation within
species (Padilla et al., 1996; Reid, 1996). This
ECOPHENOTYPIC PLASTICITY IN RADULA OF LITTORARIA
ratio is likely to be influenced by several
variables (e.g. shell growth rate, wear and
replacement rates of radula), and is known
to change during ontogeny (James, 1968;
Seshappa, 1976) and according to the rate of
feeding and consequent wear (Kizaki, 1987).
Despite this potential variability, we have
found (as in previous studies: Peile, 1937;
Marcus & Marcus, 1963; Reid, 1986, 1989) that
littorinid species from rocks exhibit relatively
longer radulae than those from plant substrates, perhaps because the faster wear on
rock substrates requires a more rapid rate of
tooth replacement. Interestingly, we have
found some evidence that this is also the case in
intraspecific comparisons of those species
found on both plant and rock substrates
although, owing to the potential variability of
this ratio and our small sample sizes, further
study is required to confirm and quantify the
trend. Conceivably, a linkage between the rate
of tooth replacement and tooth morphology
might be responsible for the correlation of
radular form with substrate.
Another interesting and poorly known
aspect of radular development is the ontogenetic change in cusp number and form. In
Littorina species juveniles show sharper, more
elongate cusps on all teeth, and more numerous cusps on the outer marginals (Seshappa,
1976; Rafaelli, 1979; Reid, 1996). Intriguingly,
the relative length of the radula is also greatest
in juveniles (James, 1968; Seshappa, 1976), and
again points to a possible link between rate of
tooth formation and the number and form of
tooth cusps. It is not known if the radulae of
Littoraria or Lacuna show ontogenetic change
similar to those of Littorina. It is striking that
the radular types associated with rock and
plant substrates in Littoraria somewhat resemble the juvenile and adult forms of the
radula of some Littorina species (e.g. L. littorea;
Reid, 1996: fig. 34). A notable difference is that
in the juvenile form of Littorina with elongate
cusps, the outer marginals show more numerous
cusps than in the adult form, whereas in the
rock form of the Littoraria radula the elongate
cusps are combined with less numerous cusps
on the outer marginals.
As discussed by Padilla (1998), the plasticity
of the radula of Lacuna (which we now
suggest occurs also in Littoraria, and perhaps in
all littorinids), is unique among invertebrates.
Plasticity of feeding structures has been
reported in many taxa, but in other examples
the modification is always a consequence of
mechanical use. Owing to the mode of forma-
367
tion of the radula, however, modification
occurs to the newly formed teeth, distant from
those in use, and there is a significant time
delay before the modified teeth reach the anterior end of the radula. Further work on the
mechanism of this unique system would therefore be of great interest.
Regardless of whether the correlation of
radular form with substrate in Littoraria is
achieved by ecophenotypic plasticity, or some
other mechanism, our finding of extreme intraspecific variability of the radula in this genus
has implications for the use of the character in
phylogenetic reconstruction. Reid (1986, 1989)
recorded the hood of the rachidian tooth as
absent in four Littoraria species (L. coccinea,
L. glabrata, L. pintado, L. mauritiana), and
from cladistic analyses concluded that presence
of the hood was a synapomorphy of the
remaining members of the genus. Here, we
have shown that the hood is in fact present in at
least two of these four species (L. pintado, L.
coccinea) in those individuals found on plant
substrates. Furthermore, a small hood has been
found in a specimen of Cenchritis muricatus
collected from wood (Reid, unpublished).
Depending upon resolution of the phylogeny
of Littoraria and its relationship with Cenchritis, the potential to develop a hood may well be
a synapomorphy of the entire clade Littoraria,
or of a more inclusive clade. Despite the
apparent plasticity of radular form, some of its
characters may still be phylogenetically informative, if appropriately coded for analysis. For
example, the character state ‘hood absent or
vestigial on rock substrates, but developed on
plant substrates’ is present in at least three
species (L. coccinea, L. pintado, L. undulata),
contrasting with the ten species which develop
a hood on both substrates. Other characters
may be found in, for example, the shape of the
base of the central tooth, which does not
change according to substrate, and appears to
show some correlation with the phylogenetic
groupings found by Reid (1986).
There are also implications for the possible
function of the radula in Littoraria. Rosewater
(1980) first suggested that the function of the
hood of the rachidian tooth was in some way
connected with grazing on the algal flora of
plant substrates. Reid (1986) pointed out that
since a hood was also present in some rockdwelling species, it was more likely of phylogenetic, rather than immediate functional,
significance. Our finding of a strong intraspecific correlation between the degree of
development of the hood and substrate renews
368
D.G. REID & Y.-M. MAK
the possibility of a functional interpretation.
The trend (both intraspecific and interspecific)
towards unequal development of the cusps of
the five central teeth (i.e. enlargement and/or
elongation of one cusp on each tooth) on rock
substrates parallels observations on other
littorinids, in which species grazing on epilithic
and endolithic microalgae have a few long
pick-like (Rosewater, 1980), enlarged (Rosewater, 1982; Reid & Geller, 1997) or chisel-like
(Reid, 1996) cusps. Mechanical considerations
suggest that this design, concentrating application of force at fewer points, should be more
effective at grazing a hard substrate (Padilla,
1985). These suggestions might be investigated
by examining grazing traces (Hawkins et al.,
1989), patterns of tooth wear, or by direct
mechanical tests, as pioneered by Padilla (1985).
Without such studies, any discussion of radular
function must remain highly speculative, for
radulae of quite different form can effectively
exploit similar diets (Hawkins et al., 1989).
In her description of the radular dimorphism
of Lacuna, Padilla (1998) remarked only on the
difference in shape of the cusps, classifying
them as blunt or pointed, and speculating that
the former were more effective at scraping
epiphytes from eelgrass blades, while the latter
were more suited to excavation of algal thallus.
Her figure of Lacuna variegata does, however,
suggest that more unequal development of
cusp sizes may also have been a feature of the
‘blunt’ category. In Littoraria the strongly
unequal cusp development was the most
striking feature of the dimorphism, and we
found it impossible to quantify consistently the
shape of the cusp tips. The smallest cusps were
almost always pointed, and here we consider
only the major cusps (i.e. the largest cusp on
each of the five central teeth). In the radulae
from plant substrates these major cusps varied
from all sharply pointed (Fig. 2A) to all bluntly
truncate (Fig. 2B); these correspond to the
‘saw-toothed’ and ‘chisel-toothed’ types of
Reid (1986), who also noted both, and a range
of intermediate shapes, on mangrove substrates. On rock, the major cusps were usually
bluntly rounded at the tip (Fig. 2C), and no
very acutely pointed cusps were seen. Conceivably, the shape of the cusp tip may be of less
functional significance than the size of the cusp
itself, because the cusp tips of functioning teeth
are rapidly abraded during use.
Interestingly, the small reduction in number
of outer marginal cusps on rock substrates
shown in intraspecific comparisons of Littoraria is not repeated in interspecific ones. The
number of outer marginal cusps is quite variable even within species restricted to plant
substrates (2–7 cusps) or rock substrates (2–8
cusps), as it is within single species, and within
individuals (see Table 1 and Results). Perhaps
this feature is not of strong functional significance. As has been noted before (Reid, 1988,
1996; Padilla, 1998), the cusp form of all seven
teeth in each row of the littorinid radula tend
to covary in the same way within species, possibly through a developmental constraint. The
reduction in number of cusps on the outer
marginal in radulae from rocks might therefore
be simply a developmental consequence of the
more unequal sizes of the cusps of the five
central teeth.
In conclusion, our report of extreme intraspecific variation in the radulae of Littoraria
adds to the growing evidence for radular variability in gastropod species, and may prove to
be a second example of the inducible phenoypic
plasticity recently demonstrated by Padilla
(1998). We suggest that such variability and its
possible causes should be carefully assessed
before radular characters are used in future
studies of taxonomy, phylogeny and adaptation.
ACKNOWLEDGEMENTS
This study was done while Y-MM was in receipt of a
post-doctoral fellowship from the Croucher Foundation, Hong Kong. For assisting Y-MM with field collecting we thank K.S. Tan (National University of
Singapore), Fu-xue Li (Xiamen University), C.K.
Tseng (Institute of Oceanography, Qingdao), Huang
Shong (National Taiwan Normal University),
Michael Hin-kiu Mok (National Sun Yat-sen University, Taiwan), S. Yamato and S. Ohgaki (Kyoto University, Shirahama), Y. Takada (Ishigaki Tropical
Station) and all their colleagues. We thank A. Ball
and C. Jones for assistance with electron microscopy,
and N. Hayes for expert printing of the photographs.
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