Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2005?

2005
854
543548
Original Article

SHELL COLOUR POLYMORPHISM IN

ISCHNOCHITON
L. GONÇALVES RODRIGUES and R. SILVA ABSALÃO

Biological Journal of the Linnean Society, 2005, 85, 543–548. With 6 figures

Shell colour polymorphism in the chiton Ischnochiton

striolatus (Gray, 1828) (Mollusca: Polyplacophora) and
habitat heterogeneity
LETÍCIA RIBEIRO GONÇALVES RODRIGUES 1* and RICARDO SILVA ABSALÃO1,2
1
Departamento de Zoologia, Instituto de Biologia, CCS, Universidade Federal do Rio de Janeiro, Ilha do
Fundão, Rio de Janeiro, RJ 21941-570, Brazil
2
Departamento de Zoologial, Instituto de Biologia, Universidade do Estado do Rio de Janeiro, Rua São
Francisco Xavier 524, Maracanã, Rio de Janeiro, RJ 20550-900, Brazil

Received 12 March 2004; accepted for publication 7 October 2004

Shell colour polymorphism was examined in a population of the polyplacophoran Ischnochiton striolatus (Gray, 1828)
living on intertidal rocks in Búzios, Rio de Janeiro State, Brazil. Nine shell colours were identified: green (most com-
mon), grey, pink, cream, brown, orange, white, black and purple. The species habitat was also examined using three
rock characteristics: volume; turnover frequency, caused by hydrodynamic disturbance; and chromatic composition.
Chitons were most frequently encountered on the undersides of rocks of intermediate volume which experienced
medium-intensity hydrodynamic disturbance, and which harboured a chromatically rich biotic community. These
findings were in agreement with the Intermediate Disturbance Hypothesis. As chitons depend on the biotic com-
munity on rocks for food and shelter, a greater variety of colours could increase the chances of camouflage of the mor-
phs against the background, favouring crypsis. It is likely that the frequency at which intermediate-volume rocks are
overturned - thus exposing the chitons on them to light - would be sufficient for visual predators to act as selective
agents. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548.

ADDITIONAL KEYWORDS: crypsis – hydrodynamic disturbance – negative phototaxia – rocky bottom –

south-east Brazil.

INTRODUCTION Ischnochiton striolatus (Gray, 1828) is a common

polyplacophoran species in intertidal zones along the
Colour polymorphism is a characteristic that can be
Brazilian coast (Rios, 1994) that exhibits consider-
defined by the coexistence, within a population, of two
able shell colour polymorphism. A bibliographical
or more colour morphs genetically determined and
search revealed no other instances of colour polymor-
segregated, where the frequency of the rarest morph is
phism in its class. In studies on marine gastropods
not maintained only by mutation (Ford, 1940; Robin-
and bivalves, visual selective predation is often sug-
son & Davinson, 1996). It is common in natural pop-
gested as a contributing factor to the maintenance
ulations and has been studied in both vertebrates
of polymorphism (Whiteley, Owen & Smith, 1997;
(Ballinger & McKinney, 1967; Gill, 1977; Tordoff,
Ekendahl, 1998). However, I. striolatus is negatively
1980) and invertebrates (Sheppard & Cook, 1962;
phototaxic, living attached to the undersides of rocks;
Benham, Lonsdale & Muggleton, 1974). In the phylum
on face value, this would appear to negate a possible
Mollusca there is often an association between the
adaptive role of shell colour. However, the intertidal
shell colour and the dominant background colour
boulder field it inhabits is exposed to wave action
(Cain, 1977).
that can turn rocks over and thus expose the chitons
to visual predators. This hydrodynamic disturbance
is also one factor that determines the algal communi-
*Corresponding author. E-mail: leticia_ufrj@hotmail.com ties living on the rocks (Sousa, 1980). Ischnochiton,

© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548 543

544 L. GONÇALVES RODRIGUES and R. SILVA ABSALÃO
as a grazer, is dependent on algal communities for
food. Some of the morphs may also be dependent on
the algal communities for crypsis. Thus I. striolatus
is an excellent candidate for an analysis of polymor-
phism in relation to substratum because both chiton
and substratum, can be readily scored and quanti-
fied. The objectives of the work were first to charac-
terize the colour polymorphism in a population of
I. striolatus from Manguinhos Beach, Armação dos
Búzios (Rio de Janeiro, Brazil), and then to relate
this to characteristics of the substrat where the pop-
ulation live. These characteristics include the size
of the rocks, the frequency these rocks were over-
turned by hydrodynamic action, as well as their
colour composition.
MATERIAL AND METHODS
STUDY AREA
The region of Armação dos Búzios is a peninsula
on the south-eastern Brazilian coast, between 22∞45¢
and 22∞49¢S, and 41∞51¢ and 41∞57¢W (Fig. 1) influ-
enced by the Current of Brazil and the South Atlan-
tic Central Waters (Gonzalez-Rodriguez, 1994). The
local tide amplitude varies between 0 and 0.9 m
(DHN, 2001).
Manguinhos Beach is on the west coast of the pen-
insula and is characterized by warm waters and a low
hydrodynamism (L.R.G. Rodrigues, pers. observ.). At
this beach there is a boulder field that enters the sea
and gets exposed at low tides. All the fieldwork was
carried out in a 25 m2 area of this boulder field, in peri-
Peninsula of
Armaçao
˜ dos Buzios
´ 22∞45’S
Study area
2.0 km
Figure 1. Map of Armação dos Búzios, Rio de Janeiro State, Brazil. Black dot shows study area.
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548
10958312, 2005, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1095-8312.2005.00513.x by UFC - Universidade Federal do Ceara, Wiley Online Library on [11/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ods of low tide between July and December 2001, and
by a single observer.
SHELL COLOUR POLYMORPHISM
The specimens of I. striolatus were collected manually
after visual inspection of turned over rocks. Each spec-
imen had its shell colour scored in accordance to its
predominant colour, and against a colour atlas (Küp-
pers, 1979). Note that the shell coloration of this spe-
cies does not change through life.
ROCK
Only those rocks where chitons were found were con-
sidered in the study. Because the rocks had irregular
shapes, making measurements of surface area very
difficult, we characterized their size using volume
instead. This was measured by water displacement in
graduated containers. The rocks were separated into
five volume classes: I, very small (£20 ml); II, small
(21–40 ml); III, medium (41–80 ml); IV, big (81–
160 ml); and V, very big (≥161 ml).
HYDRODYNAMIC DISTURBANCE OF ROCKS
In order to determine the frequency at which rocks
were turned over, 15 rocks of each volume class were
taken at random and numbered individually by first
scraping clear one of its surfaces, drying it, painting on
its number in enamel, and finely covering the whole
surface with varnish. The rocks were then returned to
041∞52’W
Atlantic Ocean
Brazil
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SHELL COLOUR POLYMORPHISM IN ISCHNOCHITON 545

the habitat with the numbered surfaces facing rocks was the same as that used for the chitons. The
upwards and were monitored weekly for hydrody- total number of discrete colours in each rock was also
namic disturbance. estimated to determine whether chromatic richness
varied with volume class.

ROCK COLOUR
The colours of the study rocks, characterized by their
biological covering and mineralogical composition,
were determined using the visual estimate method
(Jones et al., 1980). This method uses different sized
squares, each one divided into four equal parts (rep-
resenting 25% of the total area) that allow the
observer to estimate colour proportions in sample
areas. The scale of colours used to characterize the
RESULTS
SHELL COLOUR POLYMORPHISM
We observed 606 specimens and identified nine differ-
ent shell colours: cream, grey, white, orange, brown,
green, pink, purple and black (Fig. 2). The species sta-
tus of each specimen was confirmed on the basis of
shell form and ornamentation (Rios, 1994).

A B C

D E F

G H I

5 mm

Figure 2. Shell colours of Ischnochiton striolatus from Manguinhos Beach: A, cream; B, grey; C, white; D, orange; E,
brown; F, green; G, pink; H, purple; I, black.

© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548
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546 L. GONÇALVES RODRIGUES and R. SILVA ABSALÃO

30

Frequency (%)
20

10

0 n

nk

ge

te

le
re
e

ow

ac

rp
hi
a

n
re

Pi
G

re

ra

Bl
W

Pu
G

Br
C

O
Colour Patterns

Figure 3. Relative frequencies of Ischnochiton striolatus shell colours (grey, N = 606) and rock colours (white, N = 484)
they inhabited. Bars show confidence intervals (a = 0.05).

The natural variation of colour within each morph

40
made it difficult to find two identical individuals. In
order to allow future comparisons with other studies, Frequency (%)
30
each colour was referred to a colour atlas (Küppers,
1979) as follows: green, N30 C50 A99; grey, N70 C10 20
A30; pink, N20 A00 M50; cream, N20 A40 M20;
10
brown, N80 A90 M70; orange, A60 M50 C10; white,
N10 A00 M00; black, N80 C40 A20; and purple, 0
N70 M90 C30. These values represent combinations of I II III IV V
colours in different proportions (N, black; A, yellow; M, Rock Volume Classes
magenta; and C, cyan).
The nine colours occurred unequally in the popula- Figure 4. Relative frequencies of rock volume classes
tion, with green the commonest and purple the rarest inhabited by Ischnochiton striolatus. Bars show confidence
intervals (a = 0.05).
(Fig. 3) (c28 = 38.1; P < 0.001).

ROCK There is not good agreement among colour frequencies

The specimens of I. striolatus were found on a total
of 484 rocks that were not smaller than 10 ml and
not bigger than 350 ml. Figure 4 shows the rela-
tive frequencies of rock volume classes, which also
did not occur equally (c24 = 41.6; P < 0.001). The
chitons tended to be found on rocks with a medium
volume.
HYDRODYNAMIC DISTURBANCE OF ROCKS
As predicted, the total number of turnovers was
inversely proportional to the rock volume (r = –0.94;
P < 0.001).
ROCK COLOUR
All nine colours identified in the chitons were also
found in the rocks. Figure 3 shows the relative fre-
quencies of rock colours; green is the most abundant
(21.94%) and black the least abundant (1.36%) colour.
of chitons and rocks (c28 = 43.15; P = 0.0000).
The chromatic or colour richness of the rocks varied
among the five volume classes (Fig. 5). Class III pre-
sented the highest chromatic richness: 66.14% of these
rocks exhibited 6, 7 or 8 colours.
DISCUSSION
The polyplacophoran Ischnochiton striolatus (Gray,
1828) is clearly polymorphic, with nine major shell
colours. Similar polymorphisms are also common in
other species of intertidal molluscs, such as the
bivalve Donacilla cornea (Poli, 1791) (Whiteley et al.,
1997), the gastropod Neritina virginea (Linnaeus,
1758) (Aron, 1989) and several species of Littorina
(Reid, 1996).
Many authors (Cain & Sheppard, 1950; Sheppard,
1951; Allen, 1988; Gardner, 1995; Jormalainen, Mer-
ilaita & Tuomi, 1995; Bond, 1998) have suggested
that natural selection acts on colour polymorphism

© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548

80
Frequency of Rocks (%)
60
40
20
0 I
1 2 3 4 5 6
Total Number of Colours
Figure 5. Chromatic richness of each rock volume class: I
(£20 ml, N = 53), II (21–40 ml, N = 146), III (41–80 ml,
N = 189), IV (81–160 ml, N = 79) and V (≥161 ml, N = 17).
through the action of visual predators. However, it
would be pertinent to question whether visual preda-
tors can affect morph frequencies of prey with nega-
tive phototaxia, since they live in sheltered places
protected from light.
Our results showed that I. striolatus was most likely
to be found on the underside of rocks of intermediate
volume (classes II and III). This agrees with the Inter-
mediate Disturbance Hypothesis of Connell (1978),
which predicts that rocks of intermediate volume
should harbour the greatest biological diversity. The
constant turnovers of small rocks would result in
intense physical stress, sufficient to limit the number
of taxa. At the other extreme, big rocks almost never
overturn, allowing competitively superior taxa to
exclude the others, causing a decrease in diversity.
Sousa (1980) showed that the successional stage of an
algal community and the turnover frequency of the
rocks where it lives, caused by hydrodynamic action,
determines not only recovery speed, but also commu-
nity composition. Thus, the taxonomic and also
chromatic diversity of algae does not increase
monotonically with time: it peaks in the middle of
recolonization and declines later when one or few spe-
cies dominate the substratum. Our data on the chro-
matic richness of rock volume classes fit well with the
Intermediate Disturbance Hypothesis (Connell, 1978),
with intermediate volume classes of rock having the
most diverse biotic (and chromatic) communities.
Despite being negatively phototaxic, chitons are
exposed to visual predators when the rocks they are
found on frequently turn over. Notwithstanding the
influence of selective predation, the colour frequencies
© 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 543–548
10958312, 2005, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/j.1095-8312.2005.00513.x by UFC - Universidade Federal do Ceara, Wiley Online Library on [11/10/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
SHELL COLOUR POLYMORPHISM IN ISCHNOCHITON 547
80
Frequency (%)
60
40
20
Class
0
V
Class Grey I Grey II Grey III
IV
Class Grey Tones
III
Class
II Figure 6. Relative frequencies of rock (white) and chiton
Class
(grey) colours after conversion to greyscale (Grey I: refers
7 8 9 to the original white colour; Grey II: green, pink, grey,
cream and orange; Grey III: brown, purple and black).
of shells and rocks are not even. This partially agrees
with the prediction of Endler (1978, 1984) that the
more complex the background, the greater the level of
colour polymorphism. Furthermore, the rock classes
where the specimens were mostly found had the high-
est colour richness.
Our study design does not evaluate whether preda-
tors actually maintain polymorphism in I. striolatus
by frequency-dependent (apostatic) selection (Clarke,
1962; Allen, 1988), but we should consider which spe-
cies are potential predators of chitons. Crabs, together
with birds and fishes seem to be the most important
predators on intertidal littorinid snails (Pettit, 1975;
Cook & Garbet, 1992). Birds are known to feed selec-
tively upon terrestrial polymorphic molluscs (Shep-
pard, 1951; Cameron, 1969). According to Reimchen
(1979), fish such as bleniids use visual orientations to
select their prey. Heller (1975) determined an ability
to discriminate yellow from blue in the active predator
Carcinus maenas Linnaeus. In the boulder field of
Manguinhos, the decapods Arenaeus cribarius (Lama-
rck, 1818) and Panopeus austrobesus Williams, 1983,
are very common. Even without information on the
visual acuity of these predator species, we may sug-
gest that successful predation does not rely on colour
vision. If the different colour morphs of I. striolatus
are converted into grey tones, they have a practical
cryptic effect against greyscale substrata. When
viewed without colour, the match among frequencies
of grey tones in rocks and shells are almost perfect
(Fig. 6; c22 = 1.068, P < 0.58).
ACKNOWLEDGEMENTS
We are grateful to the Laboratory of Malacology, Uni-
versidade Federal do Rio de Janeiro, to Helena Passeri
for her important comments on this paper, and also to
Eduardo Rodrigues for logistical support. Special

548 L. GONÇALVES RODRIGUES and R. SILVA ABSALÃO
thanks to Paulo Márcio Costa, Renata Gomes and
Alexandre Pimenta for their great support in this
study. Financial assistance was provided by Conselho
Nacional de Desenvolvimento Científico e Tec-
nológico—CNPq.
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