South Pacific Studies Vol.40, No.2, 2020

Shell Color Polymorphism in Populations of the Intertidal
Gastropod Nerita plicata (L., 1758) from the Cook Islands
KAWAI Kei1*, MORIWAKI Hiroshi2, OKUNO Mitsuru3, FUJIKI Toshiyuki4,
MCCORMACK Gerald5, COWAN George6 and MAOATE T. Paul6

1*: Kagoshima University, International Center for Island Studies, Korimoto 1-21-24,
Kagoshima 890-8580, Japan
2: Kagoshima University, Faculty of Law, Economics and Humanity, Korimoto 1-2130, Kagoshima 890-0065, Japan
3: Fukuoka University, Faculty of Science, Nanakuma 8-19-1, Jonan Fukuoka 8140180, Japan
4: Okayama University of Science, Faculty of Science, Kitaku Ridaichou 1-1, Okayama
700-0005, Japan
5: Cook Islands Natural Heritage Trust
6: Cook Islands Government*Corresponding author: e-mail: kkawai@cpi.kagoshima-u.ac.jp

Abstract
The gastropod Nerita plicata is widely distributed across the Indo-Pacific Ocean’s upper intertidal zone
and exhibits shell color polymorphism. This study examined Nerita plicata’s shell color diversity according
to substrate type (i.e., basalt or beach rock). This study was performed on the Rarotonga (in August 2008
and August 2018) and Aitutaki (September 2009) Islands, which belong to the Cook Islands. Three different
shell color morphs (fully white, partially black-spotted, and fully black-spotted) were recorded on basalt
and beach rocks with a different frequency of distribution in the two habitats. The frequency of shell color
distribution in N. plicata is closely related to the type of habitat, with white shells occurring more frequently
in the light-colored beach rocks than in the dark-colored basalt rocks. The relationship between shell color
polymorphism and environmental and genetic factors is discussed in this study, as well as the possible roleof humans in habitat changes that drive shell color polymorphisms.
Key words: basalt, beach rock, color polymorphism, Indo-Pacific, Nerita plicata, substrate

Received: 06 September, 2019
Accepted: 30 December, 2019

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Introduction
Polymorphisms can be driven both by environmental fluctuations and genetic
diversity (FALCONER and MACKAY 1996). In marine gastropods from intertidal regions,shell shape and color pattern polymorphisms are common (LITTLE and KITCHING
1996, JOHANNESSON 2016). Intertidal gastropods live in a variable habitat, influenced
by many environmental factors, such as temperature, salinity, wave action, prey type,desiccation, and predation risk (H UGHES 1986, L ITTLE and K ITCHING 1996). The
juvenile muricid snail Concholepas concholepas, for example, exhibits shell color
plasticity according to the presence of different prey species (MANRÍQUEZ et al. 2009).
Visual selection by predators has been suggested as a driving force of shell color
polymorphism in the intertidal snails Littorina saxatilis (BYERS 1990) and Littorina
filose (M CKILLUP and M CKILLUP 2002). Distinct shell colors and morphologies
across populations are a result of various genetic factors. (e.g. J OHANNESSON and
JOHANNESSON 1996).
The gastropod Nerita plicata, which dwells on the rocky shores of the Indo-Pacific
Ocean’s upper intertidal zone, exhibits shell color polymorphism (ABBOTT and DANCE
1985, NEVILLE 2003). This species inhabits substrates with different background colors,
such as beach rocks, limestone, and basalt rocks (VERMEIJ 1971a).
The Cook Islands, located in the tropical Pacific Ocean, comprise volcanic islands
and atolls. The islands contain several tropical intertidal substrates of different colors,
such as basalt rock (black), limestone (white/gray), and beach rock (white/gray).
The present study aimed to investigate the shell color polymorphism of N. plicata on
different substrate types in two of the Cook Islands. Also discussed is the underlying
mechanism of shell color polymorphism in this species.

Materials and Methods
Study Sites
This study was performed in two of the Cook Islands: Rarotonga Island (21°14′54′′
S/159°47′7′′ W), during August 2008 and August 2018; and Aitutaki Island (18°51′0′′
S/159°45′0′′ W), during September 2009 (Fig.1). Rarotonga is a volcanic island withboth beach and basalt rocks scattered throughout its sandy beaches, and Aitutaki isa lagoon island located approximately 260 km north of Rarotonga Island. Aitutaki
presents basalt rocks scattered throughout its beaches, whereas its north shore has manybeach rocks. In Rarotonga Island, research stations were located at four sites containing
beach rocks (stations a, c, e, and f) and at three sites containing basalt rocks (stations b, d,and g). In Aitutaki Island, research stations were located at four sites containing basalt
rocks (stations h, i, j, and l) and one site containing beach rocks (station k) (Fig.1). N.

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65

plicata’s shell color polymorphism was studied on seven stations (stations a, b, c, d, e,f, and g) in Rarotonga Island in 2008, five stations (stations h, i, j, k and l) in Aitutaki
Island in 2009, and on two stations (stations e and d) again in Rarotonga Island in2018.
In N. plicata’s existing sites, salinity and air and water temperature were measured
using an environmental measurement device (YSI 63/ Ohio 45387 USA) during
daylight hours from 10:00 to 15:00, on 25 August 2008 on Rarotonga Island (stationb) and on 21-24 September 2009 on Aitutaki Island (stations h, k, and l) (Fig. 1). In
both islands the air and water temperatures ranged from 24℃-30℃. Salinity wasapproximately 36‰ in stations b, h, and k, which faced open sea, and 25‰ in station l,located in Aitutaki Island’s interior lagoon.

Fig.1. Research stations in (A) the Cook Islands, (B) Rarotonga Island, and (C) Aitutaki Islands.
Substrates were basalt rock (black circles: stations b, d, g, h, i, j, and l) and beach rock (whitecircles: stations a, c, e, f, and k). The narrow line in C indicates the reef edge.

66South Pacific Studies Vol.40, No.2, 2020

Shell color polymorphism
Over 30 individuals of N. plicata (shell length > 15 mm) were collected fromeach station. The specimens were fixed with 70% ethyl alcohol, and transported to thelaboratory for further examination of shell color patterns. Shell surfaces were carefully
observed, and the features of these surfaces were recorded.
Shell pattern distribution was compared between different islands with the same
substrate, between different substrates on the same island, and between 2008 and 2018
on the same substrate (stations e or d). Statistical analysis was performed using logistic
regression. All statistical tests were performed using SPSS version 25.

Results
Three shell color morphs were observed within the study areas: fully white (Fig.
2A and D); partially black-spotted (Fig. 2B and E); and fully black-spotted (Fig. 2C
and F). The fully white morph was defined as a completely white from the outer lip tothe apex. The partially black-spotted morph was defined as having discontinuous orincomplete small black spots pattern on the shell surface and the fully black-spotted

Fig.2. Shell color morphs: (A, D) fully white; (B, E) partially black-spotted; and (C, F) fully blackspotted.

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67

morph was defined as having the continuous and complete small black spots pattern on
the shell surface from the outer lip to the apex.
In 2008, in Rarotonga Island, the rocks at stations a, c, e, and f were white-grayand the fully white morph comprised approximately 60% of the observed individuals.
Partially and fully black-spotted morphs, on the other hand, comprised approximately
20% of observed individuals each (Fig. 3A). In contrast, on the basalt rocks of stations b,d, and g, the three morphs were distributed at nearly equivalent frequencies.
In 2009, in Aitutaki Island’s basalt rocks of stations h, i, j, and l, approximately
70% of the individuals were fully black-spotted, whereas almost all other individuals
were partially black-spotted. Fully white morphs were rare (Fig. 3B). In contrast, on
the beach rocks of station k, the three morphs were observed at almost equivalentfrequencies.
In both Rarotonga Island (2008) and in Aitutaki Island (2009) significant
differences were found between the morph frequencies of beach and basalt rocks(Rarotonga Island: χ2 = 52.81, df = 1, p < 0.001, Fig. 3A; Aitutaki Island: χ2 = 548.92,
df = 1, p < 0.001, Fig.3B). Significant differences were also found between the morph

Frequency (%)

100
80

33

77 145

60

74

204

90

53

st. a st. c st. e st. f st. b st. d st. g

st. e

96

60
40
20
0

Frequency (%)

100

45

45

83

64

39

80

Stationst. d

Fully white
Fully black-spotted
Partially black-spotted

60
40
20
0

st. k

st. h

st. i

st. j

st. l

StationFig.3. Frequency distributions of fully white, fully black-spotted and partially black-spotted morphson (A) Rarotonga Island in 2008, (B) Aitutaki Island in 2009, and (C) Rarotonga Island in 2018.
Numbers indicate sample size. The basal rock’s research areas indicate presence of blackbands above the number of sample size within each station.

68South Pacific Studies Vol.40, No.2, 2020

frequencies of Rarotonga Island in 2008 and Aitutaki Island in 2009 regarding bothbeach (χ2 = 16.63, df = 1, p < 0.001) and basalt rocks (χ2 = 139.66, df = 1, p < 0.001) (Fig.
3A and B).
In 2018, on Rarotonga Island’s basalt rocks of station d, the fully white, fully
black-spotted, and partially black-spotted morphs comprised 51%, 36%, and 13% of
individuals, respectively (Fig. 3C). No significant differences were found between
the morph frequencies observed in 2008 and 2018 at that station (χ2 = 0.009, df =1, p > 0.05). On Rarotonga Island’s beach rocks of station e, the fully white, fully
black-spotted, and partially black-spotted morphs comprised 64%, 2%, and 34% ofindividuals, respectively (Fig. 3C). No significant differences were found between
2008 and 2018 regarding the morph frequencies observed at station e (χ2 = 0.007, df = 1,
p > 0.05).

Discussion
The present study showed that in Nerita plicata, the shell color distribution wasclosely related to the type of habitat. In fact, for snails on the same island, individuals
with fully white shells occurred at a higher frequency on light-colored substrates(beach rocks) than on dark-colored substrates (basalt rocks; Fig. 3). Similarly, blackcolored shells occurred at a higher frequency in dark-colored habitats than in lightcolored habitats (Fig. 3). This shell color polymorphism may be explained by the visual
selection of the snails’ predators (BYERS 1990, MCKILLUP and MCKILLUP 2002). Bothbirds and fish are important visually selective predators of intertidal snails (HUGHES
and M ATHER 1986, J OHANNESSON and E KENDAHL 2002, R EIMCHEN 1979, 1989).
Crabs are also thought to prey on these species (HUGHES 1986, LITTLE and KITCHING
1996), although predation by the crab, Carcinus maenas, does not influence the color
frequency of Littorina saxatilis (EKENDAHL 1998). Crabs such as Chlorodiella cytherea
and Grapsus tenuicrustatus (GIBBS et al. 1975), and birds such as Pluvialis dominica(HOLYOAK 1980), are common predators found on the shores of the Cook Islands.
The present study suggests that conspicuous differences between substrate and shellcolor (for example, a white shell on a dark substrate) would put the gastropods at a
disadvantage by making them more easily recognizable. It was therefore suggested
that the frequency distribution of shell colors observed in the present study may havebeen driven by the visual selection of predators. Further studies using both field andexperimental observations are required to understand the effect of selective predationon other ecological characteristics such as size distribution.
In some gastropods, shell color polymorphisms have been shown to result
from complex interactions between selection forces (JONES et al. 1977). Although
predation may be an important selection force, predator densities generally fluctuate(ITO et al. 1992), which suggests that the intensity of the selection by the predators
may also fluctuate. However, at the observed study sites, the morph frequencies

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69

remained relatively stable for 10 years (Fig. 3), indicating that other selection forces
may also act upon shell color polymorphism. Temperature is usually an importantfactor influencing marine gastropods’ survival rates and thermal selection is known
to drive shell color polymorphism in different microhabitats (COWIE and JONES 1985,
H ARRIS and J ONES 1995). However, V ERMEIJ (1971b), W ARBURTON (1973), andCOLEMAN (1976) have suggested that N. plicata is highly adaptable to temperaturechanges. Other environmental factors such as salinity (SOKOLOVA and BERGER 2000),
insolation (HEATH 1975), wave exposure (ETTER 1988), coloration of prey species(M ANRÍQUEZ et al. 2009), and parasite tolerance (S CHEIL et al. 2014) may also
affect shell color polymorphism in N. plicata. Continued, long-term monitoring ofintertidal environments may provide an excellent opportunity to understand the causal
relationships between environmental changes and shell color polymorphism.
In the present study, the frequencies of shell color morphs were similarly
distributed for snail populations from the same island and rock type (Fig.3). Nerita
plicata are planktotrophic organisms and their larvae disperse over long distancesacross the Indo-Pacific Ocean (CRANDALL et al. 2008). This suggests that there is alow level of genetic differentiation underlying the shell variation between the studied
populations of N. plicata from nearby locations. It also suggests that N. plicata
maintains a relatively similar genotype between populations inhabiting the sameisland. However, despite the putative genetic similarities, there are likely to be different
selection forces acting upon the shell morphology of snails inhabiting different rocktypes on the same island. In addition to the differences between populations on thesame island, differences were also observed between the populations of Rarotonga
and Aitutaki Islands regarding the distribution of shell color morph frequencies on
the same type of substrate (Fig. 3). Aitutaki Island is located approximately 260 km
north of Rarotonga Island and a current flow between the two islands. Together withother environmental selection forces, both the distance and the current may increase
the genetic differentiation between the N. plicata populations of Rarotonga Island andAitutaki Island. Further studies with detailed molecular analyses using DNA markers,
such as microsatellites, are required to elucidate the effect of genetics on shell color
polymorphism.
The Pacific Ocean comprises several types of island, including atolls, almostatolls, uplifted islands, and young volcanic islands. Many beach rocks on islands suchas Rarotonga and Aitutaki, are composed of beach sediments that have been chiefly
cemented by calcium carbonate deposits in a process influenced by temperature andseawater (TANAKA 1983). Previous studies have reported that some beach rocks wereformed only several decades ago, indicating that beach rocks may have a comparatively
short formation time (see TANAKA 1990, for review), although it sometimes takes
hundreds or thousands of years to form beach rocks. Basalt rocks exist naturally on the
coast, however, their positions are occasionally altered by people residing on volcanicislands. In recent years, climate change has been widely discussed (IPCC 2014) and is
expected to increase the frequency of typhoons and lead to a rise in the sea level. This

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would lead to a flow of seawater inland with subsequent coastal erosion, especiallyin island regions. As defense against the rising sea levels and coastal erosion, people
construct cement walls and deposit stones along coastal areas. For this reason, many
basalt rocks have been deposited along the coastlines of volcanic islands. Therefore,
beach rocks have been formed along the coast in a short time and basalt rocks havebeen deposited relatively recently on the Pacific Islands. This scenario may havegreatly influenced the native substrates and habitats of intertidal organisms. Therefore,
in addition to any genetic and environmental factors, human-induced changes to coastal
areas may also affect shell color morph frequencies in intertidal organisms.

Acknowledgments
We would like to thank Dr. R. C ROCOMBE and the staff of the Cook Island
Government for their kind support, Dr. H. S HONO for his statistical advice. This
research was supported by two Grant-in-Aid for Scientific Researches (B) (20401004:
MORIWAKI) and (18H00768: FUJIKI) from the Japan Society for the Promotion of
Science.

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