Springer 2006

Aquatic Ecology (2006)

DOI 10.1007/s10452-006-9032-8

Greening of the coasts: a review of the Perna viridis success story

S. Rajagopal1,*, V.P. Venugopalan2, G. van der Velde1 and H.A. Jenner3
1

Department of Animal Ecology and Ecophysiology, Institute for Water and Wetland Research, Radboud
University Nijmegen, Toernooiveld 1, 6525 ED Nijmegen, The Netherlands; 2Biofouling and Biofilm Processes
Section, Water and Steam Chemistry Division, BARC Facilities, Kalpakkam, 603 102 Tamil Nadu, India;
3
KEMA Power Generation and Sustainables, P.O. Box 9035, 6800 ET Arnhem, The Netherlands; *Author for
correspondence (e-mail: s.rajagopal@science.ru.nl; fax: +31-24-355-3450)
Received 29 June 2005; accepted in revised form 25 January 2006

Key words: Biofouling, Green mussels, Growth rate, Invasion, Perna viridis, Physiology, Reproduction,
Review

Abstract
The green mussel Perna viridis has been receiving a lot of attention from workers working in the research
areas of intertidal ecology, aquaculture, pollution monitoring, biofouling, zoogeography and invasion
biology. P. viridis is a remarkable species in terms of its ability to reach very high biomass levels, to
withstand environmental fluctuations, to concentrate a variety of organic and inorganic environmental
pollutants, to colonise artificial marine habitats and to invade new geographic territories. This review
collates data available on salient aspects of the distribution, biology and ecology of P. viridis. It is argued
that the remarkable success of P. viridis as an invasive species basically stems from its long larval duration,
fast growth rate, high fecundity, early maturity, high productivity and ability to withstand fluctuating
environmental conditions (temperature, salinity, water turbidity and pollutants). Relevant aspects of the
data are compared with the data available for a similar species Perna perna, which too is an invasive species,
but to a more limited extent.

Introduction
The green mussel Perna viridis (L.) (Syn. Mytilus
viridis, Mytilus smaragdinus, Mytilus opalus,
Chloromya viridis, Chloromya smaragdinus) (Siddall 1980) is the tropical and subtropical counterpart of the relatively better studied blue mussel
Mytilus edulis L., a mussel that is widely distributed in the higher latitudes (Bayne 1976). Both
species are dominant in many rocky littoral and
shallow sublittoral ecosystems and often contribute significantly to the productivity of coastal
benthos (Vakily 1989; Hickman 1992). The green
mussel has been attracting lot of attention not only

as a potential organism for commercial cultivation

(Parulekar et al. 1982; Hickman 1992; Rajagopal
et al. 1998a), but also as a serious pest organism
in cooling water conduits of marine industries
(Rajagopal et al. 1991a, 1996a, 2003a). The green
mussel is characterised by fast growth and relatively high tolerance to many environmental variables, making this species relatively difficult to
control using common antifouling techniques
(Rajagopal 1997; Rajagopal et al. 2003a). Very
high densities of P. viridis have been reported from
polluted harbours and submarine pipelines of
coastal power stations (Rajagopal et al. 1997,
1998b). The ability of this mussel to concentrate

heavy metals and other pollutants from surrounding waters has been used by many
researchers to employ these mussels as sentinel
organisms (Sukasem and Tabucanon 1993;
Sudaryanto et al. 2002; Monirith et al. 2003).
Recently, P. viridis has also received lot of attention as an invading species at new localities
(Agard et al. 1992; Kazuhiro and Sekiguchi 2000;
Hicks et al. 2001; Ingrao et al. 2001).
The Genus Perna
Classication
Mollusca
Bivalvia
Pteriomorphia
Mytiloida
Mytilidae Ranesque, 1815
Perna Retzius, 1788
Within the genus Perna usually four species are
distinguished, viz., the green mussel Perna viridis
(Linnaeus, 1758), the brown mussel Perna perna
(Linnaeus, 1758), the green-lipped mussel Perna
canaliculus (Gmelin, 1791) and the Spanish
mussel (Mediterranean green mussel) Perna picta
(Born, 1780) (Figure 1). P. canaliculus and
P. picta are geographically restricted to New
Zealand and the Mediterranean Sea, respectively.
However, the other two species enjoy wide distribution in several parts of the world (Siddall
1980; Vakily 1989; Hicks et al. 2001) and often
co-exist (Rajagopal et al. 1997, 1991b, 1998b).
They have been vigorously invading new geographical regions (Hicks and Tunnell 1993). The
introduction to new areas has been probably
caused by international shipping, either as adults
attached to ship hulls or as larvae in ballast water
tanks (Hicks and Tunnell 1995). P. perna was
first introduced to the Caribbean Sea for culture
purpose, which led to its successful establishment
in nearby areas (Hicks and Tunnell 1993).
P. viridis can potentially dominate its benthic
habitat and displace other Perna species
(Rajagopal et al. 1997).

Morphology of Perna viridis

There is much confusion in the literature regarding
the taxonomic status of species within the genus

Perna (Siddall 1980; Vakily 1989). P. viridis can

be distinguished from the other three species
(P. perna, P. picta and P. canaliculus) by a few
morphological characters (Siddall 1980; Rajagopal
1997). The shell of P. viridis is emerald green in
colour, but the colour can vary from blue-green to
brown, making it difficult to distinguish between
P. viridis and P. perna. The external shell colour of
P. viridis develops from green and blue-green in
juvenile into brown with patches in adult (Siddall
1980). P. perna adults are usually brown with
irregular areas of light brown and green. The distinguishing anatomical characteristic of P. viridis is
the presence of enlarged sensory papillae along the
edges of the mantle (Siddall 1980). The exhalent
siphon and the inner surfaces of the inhalent
aperture are outlined with a stripe darker than the
variably patterned dark brown mantle (Morton
1987). Moreover, P. viridis can be distinguished
from other species of the genus Perna in having 30
instead of 28 diploid chromosomes (Ahmed 1974).
The diagnostic characters of P. viridis and P. perna
are presented in Table 1.

Distribution
P. viridis is native of the Indo-Pacific region, primarily distributed along the Indian and the
Southeast Asian coasts. They generally inhabit
marine intertidal, subtidal and estuarine environments with high salinity. P. viridis is a characteristic species of the fauna of midlittoral and
sublittoral zones, where it often constitutes dense
populations. It is gregarious and its large numbers
cluster together with the aid of its well-developed
byssal apparatus. The mussels form a thick carpetlike growth on rocky surfaces and submerged
structures like wharves, pilings, breakwaters and
buoys (Huang et al. 1983; Rao 1990) and they play
a very important role in rocky shore ecosystems. These mussels attach to surfaces by byssus
threads colonizing submerged rocks, wood, concrete, metal, old submerged logs, boats, PVC
pipes, ropes, muddy sea bottoms and even seagrass
beds and mangrove prop roots (Vakily 1989;
Agard et al. 1992; Rajagopal et al. 1997). P. perna
is distributed along the southern tip of India, Sri
Lanka (Kuriakose and Nair 1976), the coasts of
the African continent up to Morocco (Siddall
1980; Shafee 1989) and in some parts of South

Figure 1. Photograph showing the four species of bivalve genus Perna: (1) the green mussel Perna viridis (Linnaeus, 1758) (Indonesia,
Madura island), (2) the green-lipped mussel Perna canaliculus (Gmelin, 1791) (New Zealand, Wellington, Lyall Bay) (3) the Spanish
mussel or Mediterranean green mussel Perna picta (Born, 1780) (Morocco, Immouzer) and (4) the brown mussel Perna perna
(Linnaeus, 1758) (South Africa, Durban). All shells are from the collection of the National Natural History Museum Naturalis, Leiden
(RMNH), The Netherlands.

Table 1. Diagnostic characters of green mussel, Perna viridis and the brown mussel, Perna perna (modified after Kuriakose 1980 and
Rajagopal 1997).
Conchological features

Perna viridis

Perna perna

Shells*

Thick, equivalve, inequilateral,

elongate and triangularly ovate in outline
Green or bluish green
230 mm (shell length reported)
Pointed, beak-like and down turned

Thick, equivalve, inequilateral,

elongate and triangularly ovate in outline
Brown (light or dark)
121 mm (shell length reported)
Pointed, umbonal beaks poorly developed
and slightly down turned
Straight
Straight
A distinct dorsal angle or hump present
Brown (light or dark)
Inner fold of the posterior mantle margin:
very thick, not extensible and provided
with 18-22 thick branching tentacles
Thick, narrow and terminal
One large on the left valve and a
corresponding depression on the right valve
Absent
Deeply impressed
Large and located close to the base of foot
Thick, white and highly pitted
Two short and thick bundles
Mouth and passage into the mantle
cavity are of same width; rectum and
posterior adductor prominently visible
through the opening

External colour of shells

Maximum size
Anterior side of the shell
Ventral shell margin
Dorsal ligamental margin
Mid-dorsal margin
Mantle margin colour
Ventral mantle margin

Size of hinge plate

Hinge teeth
Anterior adductor muscle*
Muscle scars*
Byssus apparatus
Resilial ridge*
Posterior byssal retractors*
Excurrent aperture opening

Highly concave
Curved
Arcuate
Yellowish-green or light green
Inner fold of the posterior ventral
mantle margin: thin, extensible, smooth,
tentacles or papillae absent
Thick, broad, extends slightly to the ventral border
Two small on the left valve and one on the right valve
Absent
Deeply impressed
Large and situated at the posterior base of the foot
Thick, white and highly pitted
Two short and thick bundles
Mouth oval and wide; passage into
the mantle cavity small;
rectum and posterior adductor
not visible through the opening

*Similarities.

America including Venezuela, Brazil and Argentina (Siddall 1980; Chung and Acuna 1981).
The native range of P. viridis stretches across the
Indo-Pacific encompassing the Persian Gulf, India, Malaysia, Papua New Guinea and the South
Pacific islands, and north to Japan (Sivalingam
1977; Siddall 1980; Vakily 1989; Cheung 1993).
According to Siddall (1980), P. viridis has the
potential to increase its geographical distribution
by Island hopping, a kind of step-wise larval
dispersal. Though it is not a part of the native
fauna of northern South America (Siddall 1980), it
has been recorded from Trinidad in the mid 1990s
(Agard et al. 1992). P. viridis further moved
southward to the Gulf of Paria, using the prevailing currents and is thought to have dispersed to
Venezuela by currents (Agard et al. 1992) as well
as by human activities (Rylander et al. 1996). The
mussel larvae are believed to have been transported via ballast water to Tampa Bay estuary,
Florida, where it is now well established (Tampa
Bay Estuary Program 2000).

Reproduction
In P. viridis, the sexes are separate, but males and
females are not distinguishable by external morphology. The animals become sexually mature at
15 30 mm shell length (i.e., about 2 3 months
old) (Siddall 1980; Vakily 1989). Males are distinguishable by the milky white gonads; females have
bright orange brick red coloured gonads (Rajagopal 1991). Gonadal tissues of P. viridis appear to
be invading the whole of body, filling the mantle
lobes, mesosoma and outer surface of the digestive
glands. Figure 2 shows the histological features of
ripe testes and ovaries in P. viridis. Fertilization is
external. The spawning behaviour of P. viridis
differs considerably (Vakily 1989; Rajagopal et al.
1998a). Spawning is initiated by either sex, resulting in the release of streams of gametes into the
water (Stephen and Shetty 1981). Spawning may
also be induced by the presence of other spawning
individuals in the area or also by a drop in salinity
(Stephen and Shetty 1981). Typically, in estuarine

Figure 2. Photomicrographs of male and female gonads at different stages in sexual cycle of Perna viridis (100
). (a c) indicate
developing/re-developing stages; (d) shows ripe gonads; (e) shows spawning in progress and (f) shows spent/resting gonads.

environments inhabited by P. viridis, the salinity

drops to about 20& after heavy monsoon rainfall
(Rajagopal et al. 1989). The timing and duration of
the reproductive cycle of mussels are believed to be
controlled by an interaction of environmental and
endogenous factors (Seed 1976; Sastry 1979; Kautsky 1982; Rajagopal 1991). Barnes (1957) has
shown that synchronization of spawning in marine
epibenthic communities is particularly tuned to the
main phytoplankton blooms and only indirectly to
temperature. Kautsky (1982) reported that food
availability is the primary controlling factor for
gonad growth in Baltic M. edulis. Relatively stable
environments may promote year-round spawning,
with a couple of identifiable peaks (Parulekar et al.
1982; Walter 1982). For example, in tropical waters
of the Bay of Bengal, Rajagopal et al. (1998a, b)
reported two spawning peaks. In subtropical
environments the spawning is restricted to warmer
months (Shafee 1989).
In M. edulis, signs of sexuality and gonad
development were noted in mussels of shell length
2.0 mm (Seed 1969; Atlantic mussels), 2.1 mm
(Kautsky 1982; Swedish Baltic mussels) and
2.2 mm (King et al. 1989; Ballynahown mussels,
Galway Bay, west coast of Ireland). In comparison, Rajagopal (1991) recorded signs of sexuality

in P. viridis living in the cooling conduits of a

power station located on the east coast of India,
when the mussels were 7 mm in shell length.
However, in natural habitats in coastal waters,
Rajagopal (1991) observed signs of sexuality and
gonad development in 12 mm long green mussels.
The possible influence of unfavourable conditions
(e.g., chemical stress from chlorine residuals) in
the cooling water systems on the reproduction
and growth of P. viridis has been emphasised
(Rajagopal et al. 1998b). Based on experimental
work on gonadal conditions of Atlantic and Baltic
M. edulis over a period of 2 years, Seed (1969) and
Kautsky (1982) concluded that sexual maturity
was not related to size but rather to age and
growth rate of mussels. Thus, it is possible that
signs of sexuality and gonad development may be
observed in P. viridis even in specimens \7 mm in
shell length, especially when they are growing
under unfavourable conditions. In such cases, the
possibility of the mussels being older than what
their shell size would indicate, must be considered.
Gonadal development
Based on histological and gonad squash preparations, Rajagopal (1991) distinguished four main

stages in the reproductive cycle of P. viridis (Figure 2). The stages are described below:
Stage 1 (developing/redeveloping gonad): This
includes (a) immature gonads, characterised by a
thin, transparent and colourless mantle; hardly
distinguishable sexes; follicles distinguishable as
small opaque areas and sometimes not visible;
gametogenesis initiated, but ripe gametes not yet
visible and (b) developing gonads, specimens with
a relatively thick mantle; male and female gonads
are distinguishable; creamy white in case of males
and orange in case of females; follicles larger and
denser; gametogenesis is still progressing but
follicles contains mainly ripe gametes.
Stage 2 (ripe gonad): Mantle much thicker than in
stage 1; male mantle milky white in colour and
female bright orange brick red in colour; entirely
packed with follicles and little connective tissue
seen between follicles; ova are compacted into
polygonal configurations; male gonad is distended
with morphologically ripe sperm.
Stage 3 (spawning gonad): Gonad tissues become
dull; reduction in sperm density; appearance of
empty spaces along with full follicles; the follicles
are about one third full of ripe gametes.
Stage 4 (spent/resting gonad): This stage includes
animals that have completed spawning; mantle
semi-transparent; follicle wall ruptures and few
signs of residual gametes.
Gonad index (GI) can also be determined based on
the method described by King et al. (1989):
GI Number in each stage

numerical ranking of that stage
100=
Number of animals in the sample
where, gonad index of the sample may vary from 0
(all mussels resting) to 300 (all mussels ripe or
redeveloping). According to Seed (1976), the ranks
are allotted as follows: 0 resting; 1 immature
and/or spent; 2 developing and/or spawning;
3 ripe and/or redeveloping.

Breeding seasons
Rajagopal et al. (1998b) reported that gonadal
development and spawning activity of P. viridis
at Kalpakkam (east coast of India) were linked

to water temperature which showed two clear

peaks, one in April June (30.9 C) and another
in October (31.3 C) (Figure 3). Gonadal index
matched with the temporal distribution of temperature, though larval abundance in the coastal
waters was determined largely by food availability (Rajagopal 1991). Chlorophyll-a values
showed only a single summer peak in April June
and an increase in water temperature in October
was not associated with a matching phytoplankton increase. Therefore, it was hypothesised
that, following the second spawning in October,
food acted as a limiting factor for the growing
larvae, resulting in low numbers of mussel larvae
in the coastal waters. Narasimham (1980) and
Selvaraj (1984) also reported two main spawning periods for P. viridis from the east coast of
India, which were seemingly associated with the
seasonal distribution of temperature. Previous
studies on gonadal conditions of P. viridis indicated that spawning was largely influenced by
temperature, salinity and food availability (Rao
et al. 1975; Nagabhushanam and Mane 1975;
Qasim et al. 1977; Selvaraj 1984; Parulekar et al.
1982; Rivonker et al. 1993; Rajagopal et al.
1998a). Correlations among spawning periodicity, availability of food resources and salinity
have been demonstrated by Myint and Tyler
(1982) and Walter (1982). Low et al. (1991)
observed two spawning peaks in P. viridis in the
Eastern Johore Strait water (Singapore) during
the inter-monsoon months of November and
April. These correlated with the bimodal patterns
for salinity, dissolved oxygen and total plankton
biomass. In Hong Kong waters, peak spawning
was reported to occur only once a year (Lee
1986). Cheung (1993), working on the population
dynamics of P. viridis in the Tolo Harbour,
Hong Kong, reported two breeding periods per
year: one from July to September and another
from November to March. Lee (1985) reported
for the Victoria Harbour (Hong Kong) P. viridis
population, a single breeding period that
extended from June to September. Yoshiyasu
et al. (2004) reported that in the Sagami Bay,
Japan, P. viridis reproduces successfully and
spawns from summer to early autumn.
In the Indian coast, the breeding activity of
P. viridis can vary substantially within narrow
geographical regions, as was observed in Hong
Kong waters by Lee (1985 and 1988) and Cheung

Figure 3. Seasonal variations of different gonadal maturity stages (in percent) and gonad index of Perna viridis and seasonal occurrence of mussel larvae in coastal waters of Kalpakkam on the east coast of India (modified after Rajagopal et al. 1998b).

(1993). Published literature on reproductive

behaviour of P. viridis on the east coast of India is
based mainly on spat settlement data (Godwin
1980; Nair et al. 1988), which may not give a
correct picture regarding gonadal activity because
successful spat settlement is dependent on a number of environmental factors. Rajagopal et al.
(1998b) showed that hydrographic conditions
(especially salinity) even in closely located places
on a given coast (e.g., Kovalam, Edaiyur backwaters and Kalpakkam) could significantly differ
from one another. This could probably explain the
differences in reproductive behaviour of P. viridis
at these sites. For blue mussel M. edulis, also,
Bayne and Worrall (1980) have reported two

spawning periods at Lynher and a single one at

Cattewater in UK. Obviously, local hydrographical conditions and food availability may act
as key factors that influence the timing of spawning by a population (Lee 1985; Rajagopal 1997).
Larval development
The early development of P. viridis has been
described by Tan (1975), Rao et al. (1976) and
Sreenivasan et al. (1988). The spawned eggs of
P. viridis become spherical and after fertilization
cleavage takes place. About 7 8 h after fertilization, the blastula transforms into a mobile,
trochophore larva (Siddall 1980; Rajagopal 1991).

The veliger larval stage is developed after 16 19 h

when it has a shell covering the internal body parts
and a strong ciliated velum (Sivalingam 1977). The
larvae secrete the initial byssal threads in 10
12 days and remain in plankton for another 15
20 days (Siddall 1980), until they find a suitable
substratum (Sivalingam 1977; Appukuttan et al.
1984; Rajagopal 1997). Plantigrades attach to a
variety of natural objects using byssus threads and
are transported far and wide (Hicks et al. 2001).
Widdows (1991) has reviewed the effects of
environmental factors, such as food availability,
temperature, oxygen concentration, salinity and
pollutants, on the processes of feeding, metabolism
and growth of mussel larvae. The planktonic larval
stage and the immediate post-settlement stage in
mussel larvae are characterised by high mortality
rates. Factors that reduce growth rate, and thereby
extend larval duration in the water column, will
significantly reduce the chances of survival of the
larvae to the settlement stage. In the coastal waters
of Kalpakkam (east coast of India), Rajagopal
et al. (1998b) reported a maximum mussel larval
density of 39,500 larvae m)3 in May (Figure 3),
which is comparable with densities reported from
elsewhere for other mussel species. Schram (1970)
recorded a similar density (40,000 larvae m)3) for
M. edulis from the Oslo fjord. Hopkins (1977)
observed the lamellibranch larval densities in
Tampa Bay to range from 1200 to 15,500 larvae m)3, with an annual mean of 8000 larvae m)3.
Fish and Johnson (1937) reported peak abundance
of more than 25,000 larvae m)3 in Bay of Fundy.
Settlement
For benthic marine invertebrates like mussels,
planktonic larvae represent the rather limited
mechanism available for dispersal. Settlement
represents the transient phase between the pelagic
life of the larvae and the benthic existence of the
adult. According to Abelson (1997), flow of water
affects settlement in different ways: (a) it can act
by exerting hydrodynamic forces on the settling
larvae, influencing their encounter with the substratum and their behaviour following encounter;
(b) it may provide a settlement cue that could
induce active behaviour of the larvae and (c) flow
may act to mediate various settlement cues
(e.g. sediment load and the concentration of
attractants). Rajagopal et al. (1998b) reported

increased settlement of P. viridis under high flow

conditions. The high settlement intensity was
attributed to enhanced propagule flux rate to the
substratum, because of increased water flow.
High velocity would permit settlement of only
those larval forms, which have the ability to
withstand high shear force. Mussel larvae are
capable of settling at high water velocities (Neitzel et al. 1984; Rajagopal 1997), and it is reported
that at velocities as high as 3.5 m s)1, mussels
could settle and colonise new surfaces (Neitzel
et al. 1984). Rajagopal et al. (1998b) also studied
depth-related variation in green mussel settlement
(Figure 4). Plantigrades preferred intermediate
depth (4 m) to near-surface (1 m) or near-bottom
(7 m), which is probably related to the subtidal
habitat of the mussels. Depth-wise differences in
spat fall are likely if the larvae are non-uniformly
distributed in the water column or alternatively,
the settling larvae prefer discrete light regimes
(Figure 5). However, this depth-related feature
was not apparent at high flow conditions as was
observed at the intake point of a power station,
owing probably to turbulent water flow, which
would disturb any vertical distribution of larvae
or prevent the larvae from exercising their light
preferences.
Apart from ow, settlement pattern in marine
mussels is inuenced by other factors such as
substratum (Rajagopal 1991; Lasiak and Barnard
1995; Rajagopal et al. 1998a, b). P. viridis selects a
favourable surface prior to the secretion of byssus
(Nishida et al. 2003). According to Widdows
(1991), settlement-ready pediveliger larvae of
mussels can delay the process of settlement and
metamorphosis for several weeks until a suitable
substratum is found, though such a delay may
result in a decline in the number of offspring
surviving. Alfaro et al. (2005) studied early settlement patterns of P. canaliculus within water tanks
exposed to different water flow regimes and oxygen concentrations. Hatchery-reared larvae and
wild juvenile mussels (0.5 3.0 mm shell length)
were used for the experiments. Settlement of larvae
increased with increasing water flow; also higher
oxygen concentrations appeared to enhance larval
settlement but not in juveniles. Interestingly, the
experiments suggested that exploratory behaviour
(i.e., settlement and re-settlement) takes place
within low and medium water flows, but not under
high water flows. This study clearly pointed to the

Figure 4. Monthly variations of spat settlement of Perna viridis at different depths in Kalpakkam coastal waters and on the intake
screens of cooling conduits of a power station (from Rajagopal et al. 1998b).

complexity of larval and juvenile settlement and

re-settlement processes in P. canaliculus. It would
be interesting to investigate if similar mechanisms
operate for P. viridis as well.
There is not much information on the response
of mussel plantigrades to environmental cues.
While similar information is being accumulated on
the larval response of other fouling species (e.g.,
barnacles, polychaetes and hydroids), progress in
the case of mussels have been hampered largely
due to the diculty in consistently and successfully
rearing mussel larvae under laboratory conditions
(Bidwell et al. 1999). Interestingly, De Vooys
(2003) showed that in blue mussels (M. edulis)
environmental chemical stimuli could cause their
aggregation. Individual mussels were attracted
and moved actively upstream, in response to a

tripeptide (glycine glycine arginine) at concentrations as low as 0.56)3.78
10)10 M. That the

chemical cues play any significant role in the
aggregation of P. viridis needs further investigation.

Growth rate
P. viridis is capable of high growth rates, especially
under favourable conditions (Vakily 1989).
Rajagopal et al. (1998b) reported that on the
southeast coast of India, the mussel could reach
119 mm shell length in the first year and 152 mm
in the second year (Figure 6). However, such rates
were observed at higher than normal flow conditions i.e., on the screen walls of a power station
intake. Interestingly, the mean value in the first

Figure 5. (a) Seasonal variations of wet weight per m)2of Perna viridis and other fouling species at different depths on experimental
concrete surfaces and (b) Relationship between total weight of fouling settlement and weight of Perna viridis in coastal waters of
Kalpakkam on the east coast of India (redrawn from Rajagopal et al. 1997).

year is very much higher than those reported from

elsewhere in India: 93 mm year)1 from Kakinada
on the east coast (Narasimhan 1980) and 96 mm
year)1 from Goa on the west coast (Rao et al.
1975; Rivonker et al. 1993). Such a high growth
rate was attributed to increased food flux rate
caused by the high flow (Rajagopal et al. 1998b).
The overriding importance of food supply in
mussel growth rate has been emphasised by Seed
(1976), Seed and Suchanek (1992) and Wildish and
Kristmanson (1997). Other authors who studied

growth rates of P. viridis include Lee (1985, 1986)

and Cheung (1993). In many studies, the influence
of season was highlighted. Chatterji et al. (1984)
recorded maximum growth rate at Goa (west coast
of India) during March May, coinciding with the
phytoplankton maximum. Mussels in polluted
waters generally show a low growth rate: Lee
(1986) recorded low growth rates (5 mm month)1
in the first year of their existence) in the polluted
Victoria Harbour, Hong Kong. Similarly, Cheung
(1993) reported a growth of 49.7 mm in the first

Figure 6. Growth of Perna viridis in Kalpakkam after settlement in coastal waters and on the intake screens of cooling
conduits of a power station. Data are presented as meanSD
(n=27 30).

year of their existence from Tolo Harbour, another polluted harbour in Hong Kong. Compared
with values reported by Vakily (1989) and Tomalin
(1995), the growth rate recorded at Kalpakkam,
southeast coast of India (Rajagopal et al. 1998b),
stands apart, being 10 mm month)1 a rate that is
the highest ever reported for P. viridis.

survive in salinities as low as 20&. Combined

thermohaline tolerance of P. viridis is shown
graphically in Figure 8. Turbulent coastal waters
often contain substantial amounts of suspended
particulate matter, which can be an impediment to
the growth of filter-feeding organisms such as
mussels. Shin et al. (2002) investigated the lethal
and sublethal effects of suspended particulate
matter on the survival and physiological, behavioural and morphological features of P. viridis
collected from Tolo Harbour, Hong Kong. They
found P. viridis to tolerate a high level of suspended particulate matter (up to 1200 mg l)1).
However, there were dose-dependent effects of
suspended particulate matter on the morphology
of gill filaments. The observations that P. viridis
colonise even muddy sediments, point to the high
level of tolerance of the green mussels to high
suspended particulate matter (Segnini de Bravo
pers. comm.).

Byssus thread production

Mussels are tethered to the substratum by means
of a byssus, an extracorporeal collagenous structure secreted by the foot. The byssus consists of

Environmental tolerance
One of the main reasons for the extraordinary
invasive ability of the green mussel is its tolerance
to a wide range of environmental conditions. The
mussel is quite hardy and individuals have been
reported to do well in articial seawater for more
than 6 months (Nishida et al. 2003). P. viridis
tolerates a temperature range of 15 32.5 C
without much problem (Rajagopal et al. 1995a).
The species can survive a temperature of 39 C for
about 200 min (Figure 7). The thermal tolerance
of P. viridis becomes very conspicuous compared
with that of P. perna (Figure 7). P. viridis thrives
well at winter water temperatures as low as 12 C
(Benson et al. 2001). Segnini de Bravo (2003)
reported that P. viridis has a higher degree of
adaptability to salinity changes and, therefore, a
greater potential for aquaculture than P. perna
(Romero and Moreira 1980; Salomao et al. 1980).
Sivalingam (1977) reported that the normal fluctuation in salinity (27 33&) observed in estuarine
habitats was well within the lower and upper
tolerance limits of P. viridis. However, it can

Figure 7. Exposure time required for 100% mortality of Perna

viridis (Rajagopal et al. 1995a) and Perna perna (Rajagopal
et al. 1995b) at several high temperatures. Mortality data are
expressed as meanSD (n=36) of six replicate experiments
(n=6 in each experiment). The criterion for mortality of
mussels was valve gaping with no response of exposed mantle
tissues to external stimuli.

Figure 8. Exposure time required for 100% mortality of Perna

viridis subjected to the combined effect of salinity and temperature (modified after Rajagopal et al. 1995a). Mortality data
are expressed as mean SD (n=36) of six replicate experiments (n=6 in each experiment).

three distinct parts, viz., root, stem and thread

(Bayne 1976). Each thread, in turn, consists of a
proximal part, a distal part and an attachment
plaque. The byssal thread functions like a shock
absorber in its mechanical design: it is strong and
stiff at one end and pliably elastic at the other
(Waite et al. 1998). Cheung et al. (2004a, b) have
shown that byssus production is a plastic response,
influenced by exposure to chemical signals from
predators and damaged conspecifics. Nishida
et al. (2003) observed that byssus production in
P. viridis was significantly influenced by the nature, especially, surface free energy as well as dispersion and polar components of the attachment
surface. They observed a correlation between the
dispersion component and mussel attachment,
while the polar component did not correlate with
the mussel attachment. In fact, individual blue
mussels, M. edulis, can express at least 20 variants
of a small protein (Mefp3), which is a component
of the adhesive plaque of the byssus (Warner and
Waite 1999). Evidence suggests that selection of
protein variants for deposition onto a given surface might be determined at the level of translation. Such a flexibility would provide great

adaptability to mussels by enabling production of

byssus threads with characteristics that match the
substratum being fouled. However, no published
work is available on the expression of corresponding proteins in P. viridis.
Several authors have investigated the environmental inuence on byssal thread generation in
mussels. Seasonal cycles, mussel size, spawning,
temperature, salinity, wave action, tidal regime, air
exposure, mechanical agitation, divalent cations
are factors that have been shown to inuence
byssogenesis (Young 1985; Rajagopal et al.
1996b). In most studies, wave action and
mechanical effects proved to be the most important factors that affected the rate of byssus production (refer to Rajagopal 1997 for review).
Young (1985) showed that M. edulis produced up
to 15 threads per mussel within a day when agitated every 4.5 s, while P. viridis produced up to 68
threads per mussel within a day, when agitated
every 3 s (i.e. 20 cycles min)1) (Figure 9). Thread
production, under increasing mechanical agitation, showed an initial increase followed by drastic reduction (Figure 9). Cheung et al (2004a, b)
observed that longer and thicker byssal threads
were produced by P. viridis, when exposed to
damaged conspecifics and predators compared
with control. It was surmised that stronger byssal
attachment would reduce predation as well as nonpredation mortality. In the laboratory, cumulative
byssus threads production by P. viridis, shows a
continuous increase with time and within seven
days, a mussel (12 mm size group) produces on an
average about 90 threads (Figure 10), which is
about twice the figure for P. perna.

Figure 9. Effects of agitation on the byssus thread production

of Perna viridis and Perna perna (redrawn from Rajagopal,
1991). Old byssus threads were removed before the experiments
started.

In mussels gills and ciliary mechanisms associated

with them serve to pump water and collect,
transport and sort food particles (Morton 1983).
Food particles are entrapped in mucus strings and
transferred to labial palps, which regulate entry of
food into the mouth. The labial palps also help in
rejection of excess material as pseudofaeces. Oxy-

gen consumption is also closely linked with the

pumping of water. Filtration and feeding in mussels have been extensively dealt with by Bayne
(1976). Rajagopal (1991) has estimated the filtration rate in P. viridis as a function of mussel size,
temperature, salinity and light dark cycle. To
estimate the amount of water filtered through the
gills, he used the dye absorption technique
(Coughlan 1969), which is based on absorption of
neutral red by actively filtering mussels. The data
show that filtration rate (expressed as volume of
water filtered per mussel) increases with mussel
size. Optimum filtration rates of P. viridis were
observed at a temperature and salinity of 30 C
and 30 35&, respectively (Rajagopal 1991). The
filtration rates were significantly higher in mussels
kept in complete darkness, compared with those
maintained in day light or light/dark conditions
(Figure 11). It is generally observed (Rajagopal,
unpublished data) that shadows falling on them
disturb the feeding of P. viridis, probably as a
defence mechanism against predators. Defence
against predation could be the reason for
higher filtration in darkness. Figure 12 shows
oxygen consumption rates as a function of temperature. Optimum oxygen consumption occurred
at 30 C, while at 40 C oxygen consumption
declined to nil.
Rajesh et al. (2001) showed that in P. viridis,
increasing algal concentrations resulted in an increase in the filtration and ingestion rate, until a
concentration of 1
105 cells ml)1 was reached, at
which pseudofaeces production started. Wong and
Cheung (2001) investigated food availability and

Figure 10. Cumulative byssus thread production of Perna perna

and Perna viridis over a period of 7 days. Data are presented as
meanSD (n=20). Old byssus threads were removed before
the experiments started.

Figure 11. Effects of light and darkness on the mean filtration

rate (n=18; experimental duration=3 h) of Perna viridis and
Perna perna.

Byssal thread production in post larvae takes

place for the purpose of drifting. These threads
dier from the attachment threads: the drifting
threads secreted by young post-larval mussels of
M. edulis are simple monofilaments, distinct in
structure and function from the attachment byssus
threads. The attachment threads are relatively
short and have a terminal attachment plaque,
drifting threads are longer and exceed the postlarva in length by more than two orders in magnitude and are without plaques or any other
structures (Lane et al. 1985). The drifting threads
help in the dispersal of young mussels over wide
geographical areas. Calculations by the authors
showed that the drifting threads would increase
the fluid drag experienced by the post-larvae of
M. edulis in the water column. In fact, the theoretical viscous drag force on the threads would be
sufficient to significantly reduce the sinking rate of
drifting post-larvae and effectively enhance their
dispersal. Very little work has been done on byssogenesis in P. viridis and more focussed research
in this area is due.

Filtration

feeding responses of P. viridis for two complete

tidal cycles, covering both spring and neap tides.
Feeding rates and absorption efficiency were
highest at low tides and lowest at high tides.
The clearance rate of the mussels was influenced
by the tides and was a negative power function of
total particulate matter and a positive linear
function of organic content in water. Pseudofaeces
were produced only during spring tide but not
during neap tides. Wong and Cheung (2001)
observed that by adjusting feeding rates and
enzymatic activities, food absorption in P. viridis
remained constant, irrespective of the changes in
food availability. Hawkins et al. (1998) compared
the suspension feeding behaviour of different
tropical bivalve molluscs (P. viridis, Crassostrea
belcheri, C. iradelei, Saccostrea cucullata and
Pinctada margaritifera) under natural seston concentrations. As seston availability increased, a
minimum average of 71% of the filtered material
was rejected by each species as pseudofaeces.
Interestingly, all species preferentially rejected as
pseudofaeces particles with higher average inorganic content, which resulted in a net organic
enrichment of the ingested material. P. viridis has
been shown to be capable of selectively capturing
particles from the water filtered (Ke and Wang
2002). Using radiotracers to label diatoms and
natural sediment, they showed that P. viridis could
selectively ingest diatom particles from a suspension. However, no significant particle selection was
observed at concentrations below the level of
pseudofaeces production. Hawkins et al. (1998)
showed that the fast growth in P. viridis resulted
from a higher average clearance rate, a higher

Figure 12. The oxygen consumption of Perna viridis and Perna

perna at different temperatures. Data are expressed as
meanSD (n=12).

average organic enrichment of filtered relative to

available matter and a higher average organic
enrichment of ingested relative to filtered matter
than have so far been recorded for any species of
filter-feeding bivalve.
Filter-feeding bivalves can assimilate various
kinds of suspended food like plankton, including
dissolved substances (Jorgensen 1983; Gorham
1988; Roditi et al. 2000), bacteria (Crosby et al.
1990; Langdon and Newell 1990; Kreeger and
Newell 1996), and heterotrophic nanoflagellates
(Sherr et al. 1986; Kreeger and Newell 1996).
Detritus also forms an important part of the diet
of P. viridis (Rao 1990). Based on data from
experimental feeding of Mytilus edulis with rotifers, Wong et al. (2003), argued that dense populations of mussels could exert a strong top down
effect on planktonic food webs. Rajagopal et al.
(1991a) have shown that P. viridis are capable of
forming extremely dense populations in coastal
waters. The effect of such massive filter feeder
communities on coastal plankton dynamics and
planktonic-benthic energy transfer need to be
examined in greater detail. For example, Kimmerer et al. (1994) showed that naupliar stages of
copepods could be vulnerable to bivalve grazing. It
may be possible that instead of feeding solely on
phytoplankton, which would reduce food for
herbivorous zooplankton, bivalves may exert a
top down effect by preying directly on zooplankton (Wong et al. 2003).

Excretion
Nitrogenous compounds, end products of protein
and amino acid catabolism, are the major excretory products in mussels. Among the nitrogenous
wastes, ammonia is the major excretory product
(Bayne et al. 1976). Masilamoni et al. (2001)
presented data on excretion of nitrogen and
phosphorus by different size groups of P. viridis
at different salinities (15, 20, 25, 30 and 34&).
Salinity was found to influence the rate of excretion. Ammonia excretion in different size groups
of mussels increased as the salinity was lowered
up to 25&. On further decrease of salinity, there
was a decrease in the excretion rate, which stopped completely at 15&. Apart from ammonia,
animals excrete nitrite and nitrate as part of a
mechanism for detoxification of ammonia and

maintenance of internal ionic stability. Masilamoni et al. (2001) reported that nitrite and nitrate
excretion in P. viridis showed increase with
decrease in salinity. Phosphate excretion, on the
other hand, decreased significantly with decrease
in salinity.
Release of nitrogenous (ammonia, nitrite and
nitrate) and phosphorus (phosphate) wastes by
large mussel communities may signicantly aect
the nutrient dynamics of the receiving water body
(Kuenzler 1961; Richard and Dankers 1988).
There have been reports of mussel activities
(especially, selective filtering and nutrient excretion) promoting algal blooms in bays and lakes
(Vanderploeg et al. 2001). Discharge of condenser
effluents from cooling water systems of coastal
power plants that harbour massive mussel communities (e.g., see Venugopalan et al. 1991) into
inshore areas need to be studied from this point of
view (Masilamoni et al. 2001). In view of the
dramatic population increase of P. viridis in many
coastal localities, bays and harbours, it is suggested that nutrient loading by mussels be given
due attention by researchers.

for example, the gastropods opted for mussels

previously unexposed to predator cues. Apart
from predator gastropods, other organisms also
damage mussel shells by boring into them.
Microbial phototrophic endoliths (mostly cyanobacteria) bore into P. viridis shells and cause
considerable shell degradation (Kaehler and
McQuaid 1999). The authors reported that by
attacking the shell such borers reduce the longevity
and reproductive output of the mussels.
Pea crab (Pinnotheres sp.) is reported to be a
commensal in P. viridis. Recently, Jose and
Deepthi (2005) reported the prevalence of Pinnotheres placunae in green mussels along the Malabar
Coast of India. Male and female (egg bearing)
crabs were observed in the mantle cavity of about
6% of the mussels sampled over a one year period.
The infected mussels had significantly lower shell
size and live weight and were characterised by gill
damage (gill erosion and malformation). Koya
and Mohandas (1982) reported the presence of
adults of a digenetic trematode of the genus
Gorgoderina in P. viridis.

Cultivation
Pest and predators
According to Bayne (1976), natural enemies of
mussels fall into four categories: predators, competitors, parasites and shell borers. Algae, hydroids, free and tubiculous polychaetes, barnacles,
amphipods and ascidians are important pests
which colonise the outer surface of shell valves of
P. viridis and compete for space. The main predators include crabs, fishes, starfish and octopus
(Rao 1990). The mud crab Scylla serrata is considered a major predator of P. viridis, while among
fishes snapper, silver bream and black tail have
been mentioned (Vakily 1989). However, there are
not many studies on the effects of predation on
P. viridis. Cheung et al. (2004a, b) studied the
defensive responses of P. viridis on being
challenged with two predators, the muricid gastropod, Thais clavigera, and the portunid crab,
Thalamita danae. They observed that responses of
the mussels were predator-specific. Mussels raised
in the presence of crabs developed thicker shell at
the umbo and lip margin, while those raised in the
presence of gastropods had a thicker shell lip.
Predators also were shown to choose their prey;

Commercial cultivation of Perna mussels

(P. viridis, P. perna and P. canaliculus) is extensively carried out in several countries and the
subject has been reviewed by Vakily (1989). In
mussel farming, harvesting phase commences
when the mussels reach minimum marketable size.
This varies significantly according to species,
geographic region and cultivation method. In
temperate waters, the mussels (e.g., M. edulis)
reach marketable size only after a long culture
period viz., 12 24 months (Hickman 1992).
However, in the tropical/subtropical marine mussel P. viridis, marketable size is achieved after a
relatively short culture period, i.e., about 6 months
(Sivalingam 1977; Parulekar et al. 1982; Vakily
1989; Rivonker et al. 1993; Rajagopal et al.
1998a). This confers a potential advantage to
farmers of P. viridis over their counterparts in
other parts of the world.
A few values are available for the increases in
meat and shell mass of cultivated P. viridis from
the different parts of world. An increase of
1.13 g month)1 for first 6 months and thereafter a
rate 0.11 g month)1 were reported from the east

coast of India (Rajagopal et al. 1998a). A general

increase in meat and shell mass coincided with the
latter half of the post monsoon and early summer
period, when plentiful food material and optimum
hydrographic conditions prevailed. Spawning
during April May and September October
resulted in a sharp decline in the meat weight
(Figure 13). The rates of seasonal increase in shell
and meat growth were uncoupled during the
period from May to November, exhibiting little
correlation between them, partly due to loss in soft
tissue weight resulting from spawning (Figure 13).
Similar results were also reported from eastern
Long Island Sound, USA (Hilbish 1986) and
Beggars Island, southwest England (Salkeld 1995)
for populations of M. edulis. For P. viridis, an
inverse relationship between density and production was found: mussel production increased with
decreasing density (Figure 13). Rajagopal et al.
(1998b) reported that the increase in the weight of
individual mussels compensated for the decrease in
the density of population, thereby resulting in a
progressive increase in production and biomass
(Loo and Rosenberg 1983; Rivonker et al. 1993).
However, higher production and biomass rates
were observed for the first six months (P=5.23
kg m)1 month)1; B=2.48 kg m)1 month)1), and
they were significantly lower for the later
6 months (P=2.73 kg m)1 month)1; B=1.18
kg m)1 month)1). In general, older mussels have a
poor growth rate due to reduced metabolic activity
(Cheung 1993), filtration rate (Bayne et al. 1976),
feeding rate (Seed and Suchanek 1992) and
increased gamete production (Hilbish 1986).
Although commercial cultivation of P. viridis
has a bright future, the recent reports regarding
shell fish poisoning in P. viridis are disconcerting.
Paralytic and diarrhetic shellfish poison (PSP and
DSP), caused by harmful algal blooms (HAB)
were detected in P. viridis from Singapore and
Trinidad (Holmes et al. 1999; Yen et al. 2004).

Green mussels and biofouling

Bivalves are a key component of the fouling
community that develops inside the cooling circuits of coastal power plants. Previous studies
showed that out of 94 species collected from within
the seawater intake system of a tropical power
station, more than 17 were bivalve species (Ra-

jagopal et al. 1991a, b). Among them green mussels were the most dominant species, in terms of
biomass. The green mussels have proven to be a
successful fouling species in a variety of maritime
and industrial environments. Their widespread
distribution and their ability to attach to different
surfaces even at high flow rates and to make use of
water flow to achieve fast growth rates and high
population densities, make them highly suited to
colonise cooling water systems (Rajagopal 1997).
Their characteristic ability to survive extremes of
environmental conditions (salinity 0 64& and
temperature 6 37.5 C), thrive well in turbid
coastal waters (Morton 1987) and survive under
prolonged biocide dosing that gets rid of most of
their competitors (Rajagopal et al. 2003a), has
contributed to their extraordinary success as fouling species. In fact, P. viridis can withstand harsh
environmental conditions better than its temperate
counterpart Mytilus edulis (Morton 1987) or its coexisting species P. perna (Rajagopal 1997).
Uncontrolled growth of the green mussels can
create problems for power plants using seawater as
the condenser coolant. With continuous ow of
water that brings in sucient quantity of food
and oxygen, apart from fresh stock of larvae, the
exposed surfaces like intake tunnel, screens, pipes
and culverts are quickly colonised by young mussels (Rajagopal et al. 1996a). Economic aspects of
fouling-induced effects on electric power plants
can be very significant, such as reduced flow of
cooling water for steam condensation, causing
increased condenser backpressure and belowoptimum performance (Rajagopal 1997). Live
mussels or empty shells can cause mechanical
damage to pumps and block the flow of water in
condenser tubes and reduce the heat transfer efficiency (Neitzel et al. 1984; Rajagopal et al. 1994).
Mussel shells can also cause accelerated corrosion
of the condenser tubes (Fischer et al. 1984). There
are reports of extensive growth of green mussels
in the condenser cooling systems of power stations
in India (Rajagopal et al. 1991a, b).
Over the years, P. viridis has been able to
expand its geographical territory into new areas.
Today, it is recognised as a potential fouling
organisms in countries such as Malaysia, Hong
Kong, Japan, China, USA (Florida), Trinidad and
Venezuela, making it a truly global player (Morton
1987; Agard et al. 1992; Kazuhiro and Sekiguchi
2000; Rajagopal et al. 2003b). Fouling biomass

Figure 13. (a) Seasonal variations of total, shell and meat weights of Perna viridis on ropes in Edaiyur backwaters, east coast of India
and (b) Changes in total production, biomass and density estimates of Perna viridis in Edaiyur backwaters east coast of India (redrawn
from Rajagopal et al. 1998a).

build-up rates as high as 211 kg m)2 year)1 have

been reported (Rajagopal et al. 1997). With more
and more power stations being built in tropical, third
world countries, where seawater will be used as
condenser coolant owing to shortage of fresh water,
it is anticipated that problems due to green mussel
fouling will aggravate and need to be tackled.

Mussel control
The type of fouling control measures adopted by
an industry depends on the system being fouled.
Antifouling paints have been the method of choice
for combating biofouling on ship hulls. However,
paints have only limited service life and require

re-application at regular intervals. Hence they are

of not much use in the case of power plant cooling
systems. Biocides used for biofouling control are
of two major categories: oxidizing biocides and
non-oxidizing biocides (Rajagopal 1997). The
former include chlorine (gas or sodium/calcium
hypochlorite), bromine, active halogen compounds, ozone, hydrogen peroxide and chlorine
dioxide, while the latter include aldehydes, amines
and quaternary ammonium compounds, organobromines and organo-metals (Jenner et al. 1998).
The mechanisms by which the various biocides
bring about mortality of the organisms are not
fully understood. However, the major causes are:
(1) damage of the cellular organization, particularly damage of the semipermeable cell membrane
or nucleic acids, (2) interference with the energy
production mechanism by inactivation of enzymes
or the oxidative phosphorylation process that
generates cellular energy and (3) interference with
the biosynthesis of proteins and nucleic acids
(Jenner et al. 1998).
Power plant biofouling control has traditionally
been achieved by either continuous or intermittent
chlorination (Rajagopal et al. 2003b, c). Chlorination still remains the most preferred mode of
biofouling control in cooling water circuits, owing
to economy, easy availability and wide-spectrum
efficacy. Although effective control of all types of
fouling can be achieved by chlorination, there are
inherent problems involved in the use of chlorine:
hazards of handling chlorine gas cylinders, difficulty in maintaining chlorination plants and
non-uniform distribution of chlorine residual at
required sites. Often, it is prudent to adopt suitable
preventive measures to avoid or reduce the intensity of mussel fouling, rather than to get rid of it,
after the mussels established themselves within the
cooling circuits. This is because prevention of
settlement by young green mussels can be achieved
at much lower biocide levels than that required for
killing attached adult populations (Rajagopal
et al. 1991b). Accordingly, the developed methods
are based on continuous dosing of chlorine, which
creates an environment inside the cooling circuit that is unattractive to the incoming larvae
(Rajagopal et al. 1991a). A term exomotive
chlorination has been coined to describe this
method of chlorination, which exploits the fact
that incoming mussel larvae are selective about the
environment in which they settle (Lewis 1985).

Consequently, the larvae do not settle inside the

system, but return to the sea along with the outgoing water (Rajagopal et al. 1991b). Lower concentrations of chlorine ( \0.5 mg l)1) are known
to produce changes in swimming and crawling
behaviour of mussel larvae (Jenner et al. 1998).
Moreover, growth rate of adult mussels under
continuous low-dose chlorination is substantially
lower than that of an untreated population
(Rajagopal 1991, 1997). Several power stations
have successfully employed low-dose continuous
chlorination to control mussel fouling, including
that by P. viridis (Rajagopal et al. 1996a). However, the main disadvantage of this method is that
interruptions in chlorination will allow mussels to
settle, which on resumption of chlorination are not
easily dislodged (Rajagopal et al. 2003c).
Mussels by nature are relatively quite tolerant
to chlorination. The resistance of adult mussels to
chlorination partly comes from their ability to
tightly close their bivalve shells and isolate
themselves from the ambient water conditions for
long periods of time, and switching from aerobic
to anaerobic metabolism. This allows the mussels
to withstand extreme high chlorination concentrations of [5 mg l)1 (Rajagopal 1997). At a
power station in India, it was necessary to employ
shock-dose chlorination (2 3 mg l)1) for several
weeks at a stretch to get rid of the a mussel
population that had established in spite of intermittent chlorination at a level of 1 2 mg l)1
residuals (Rajagopal et al. 1996a). Data by Masilamoni et al. (2002) show that the green mussels
can sense residual chlorine levels \0.15 mg l)1
and complete valve closure occurs only at
0.55 mg l)1. Recent research has shown that
operational costs associated with chlorine dosing
can be brought down by judicious dose reduction.
Research carried out at KEMA, The Netherlands,
has shown that efficient mussel control could be
achieved by rapidly pulsed chlorination called
Pulse-Chlorination. This technique leads to 40
70% reduction in chlorine use. The method
makes use of the lag time (recuperation time)
between stoppage of chlorination and full opening
of the shells by mussels and, in effect, fools the
mussels into ,thinking that the dosing is continuous (Polman and Jenner 2002; Rajagopal et al.
2003c). However, such a technique will only be
feasible if the dosing system is reliable and if the
Total Residual Oxidant or Free Oxidant concen-

tration is monitored accurately and continuously.

Moreover, simultaneous spat settlement monitoring (e.g., using spat monitors) is also required
to determine the efficacy of the treatment. This
can be done by simple biofouling monitors. PulseChlorination is adapted as BAT (Best Available
Technique) in Europe (Polman and Jenner 2002).
Increasing awareness of the carcinogenic eects
of chlorination by-products has led to stricter
limitations being placed on euent limits of
residual chlorine (Jenner et al. 1998). Consequently, there has been a search for alternate
methods of fouling control, which are cheap,
effective and safe. In this context, heat treatment, a
potential alternative, is being practised by several
utilities (Rajagopal et al. 1994, 2005a, b). Steam
electric power plants generate waste heat and,
therefore, heat treatment can be a viable fouling
control measure in cooling water circuits of
power plants. This method entails a power penalty
due to increased condenser vacuum loss during
the treatment period. Nevertheless, it has been
reported to be economical under tropical conditions, owing to the rather narrow difference
between ambient and lethal temperatures in the
case of tropical fouling organisms, as compared
with their temperate counterparts (Rajagopal
1997). Several plants in Europe and North
America are presently using heat treatment to
control mussel fouling in their cooling water
systems (Jenner et al. 1998).

Mussels as biomonitors
The use of bivalves, especially mussels, as sentinel
organisms (the Mussel Watch concept) for marine pollutants has been proposed by Goldberg
(1986) and Bayne (1989). This method served to
monitor the pollution in the world oceans in the
1980s and 90s (Goldberg and Bertine 2000). Using
this method, mussels have been used as bioindicators to study contamination of coastal waters by
a variety of organic and inorganic pollutants,
including heavy metals, organochlorines and
PCBs. Biomonitoring of persistent organochlorines in the coastal marine environments of the
Asia pacific region, carried out using P. viridis, can
be found in recent work by Monirith et al. (2003).
Sukasem and Tabucanon (1993) used P. viridis to
monitor heavy metals such as zinc, manganese,

copper, chromium, nickel and cadmium in the

Gulf of Thailand (see also Sudaryanto et al. 2002;
Blackmore and Wang 2003; Bayen et al. 2004).
However, byssus threads of mussels accumulate
heavy metal better than meat (Van der Velde et al.
1992, and literature therein). Recently, Yap et al.
(2003) used byssus threads of P. viridis as reliable
indicators of heavy metal pollution in the environment. They observed that concentrations of
Cu, Cd, Pb and Zn in the attachment plaques of
P. viridis were higher, compared with the other
parts of byssus, foot and total soft tissue. They
inferred that different protein composition could
be the reason for the different heavy metal levels
observed in the different parts of the byssus.
However, more work is needed to to find out how
accurately byssal levels of heavy metals could
reflect environmental concentrations.
Biomarkers are increasingly being employed to
ascertain the health of marine mussels exposed to
polluted environments. They provide meaningful
information on the potential impact of a variety of
pollutants on the health of mussels, before the
eects are manifested externally. Depending on
the eect of dierent kinds of contaminants,
dierent categories of biomarkers have been
identied (Narbonne et al. 1999; Lau and Wong
2003; Damiens et al. 2004). Biomarkers generally
have higher sensitivity and specificity at molecular
levels. Often, it is necessary to use a number of
biomarkers (multimarker approach) to get a realistic picture of the overall response of mussels to
degradation in water quality. The suitability of
antioxidant enzymes, e.g. glutathione S-transferase, super oxide dismutase, catalase, glutathione
peroxidase and glutathione reductase, have been
examined in P. viridis (Cheung et al. 2001; Lau
and Wong 2003). Recently, Nicholson and Lam
(2005) have reviewed the status regarding the use
of biomarkers in P. viridis from the view point of
pollution monitoring. We now know that mantle
and gills are relatively more biomarker-responsive
than the rest of the body (Prakash and Rao 1995).
Since gills are directly involved in filter-feeding
and respiration, they form the frontline organs
exposed to water-borne contaminants (Lau and
Wong 2003).
Lawrence and Nicholson (1998) have shown
that stress proteins are sensitive biomarkers of
environmental stress in mussels. They observed
induction of stress proteins in mussels at chlorine

residuals as low as 0.01 0.07 mg l)1. Nicholson

(1999) discussed the utility of physiological biomarkers (e.g., cardiac activity) for pollution monitoring using P. viridis. Studies by Siu et al. (2004)
demonstrated that induction of micronuclei (MN)
in the gill cells of P. viridis could be used as a
sensitive and stable biomarker of exposure to relatively low levels of genotoxicants. They observed
an increase in MN frequency with continued
addition of genotoxicants, which did not decrease
significantly when the external exposure was
decreased or completely stopped for one to two
weeks. Their studies also showed that chronic
exposure could lead to a greater genotoxic impact
than acute exposure.

Perna viridis the great invader

P. viridis is credited with considerable success as an
invading species, conquering new geographical
locations in the east and the west. In general, the
life history traits that make a successful invader
are: a short life span, rapid growth rate, rapid
sexual maturity, high fecundity, greater ability to
colonise a wide range of habitats, wide physiological tolerance, gregarious behaviour, suspension feeding and ability to repopulate following a
population crash (Morton 1997). In the opinion of
Bayne (1976), the competitive superiority of mussels basically stems from their rapid recruitment
and growth, their ability to detach and re-attach
with byssus and their ability to quickly migrate to
vacant spaces thrown open by natural forces. It is
obvious that P. viridis is endowed with several
characteristics that qualify it for a successful
invader (Figures 3 6).
It is generally perceived that transport of the
mussels far and wide has been aided by modern
shipping operations. Adult mussels could be carried to newer geographical locations as part of the
hull fouling community. Alternatively, larvae or
young ones could be transported via ship ballast
water. P. viridis was discovered in the Tampa Bay,
Florida, in 1999. Prior to that, it was reported at
Point Lisas, Trinidad (in 1990), Gulf of Paria,
Venezuela (in 1992) and Kingston Harbor, Jamaica (in 1998). Mussel beds along the Indian
coasts are known to occur only in those coastal
belts where natural rock formations are present.
But going by the reports from the Gulf of Mexico,

the presence of natural hard substrata does not

seem to be necessary for large scale colonization of
P. viridis. As a result, the population densities of
P. viridis in the Gulf of Mexico have exceeded
those of native mussel species (Ingrao et al. 2001).
It is imperative that further spread of the mussel be
monitored on a regular basis.
Warming of worlds oceans can be expected to
increase the geographical distribution of tropical
and subtropical species, especially of the eurythermal type. According to data available from the
U.S. National Climatic Data Centre, the average
global surface temperature is expected to rise by
0.6 2.5 C in the next 50 years and by 1.4 5.8 C
in the next century, with signicant regional variations. Such expected increases in seawater temperature would denitely have a signicant
inuence on the distribution of species such as
P. viridis. More studies on these lines are urgently
warranted.

Perna viridis vs. Perna perna

From the foregoing account, it is clear that P. viridis
has not only ecological and economic impacts but
also significant human health impacts. P. viridis can
out-compete many other benthic species, causing
changes in community structure and food web
relationships. For example, since the appearance of
P. viridis, in the Golfo de Paria in 1993, the habitat
of the brown mussel, Perna perna, has been altered
(Segnini de Bravo et al. 1998). Subsequently,
P. viridis has driven out P. perna from its natural
beds in La Esmeralda, Guatapanare and El Morro
de Chacopata, Sucre State, Venezuela. Hicks et al.
(2001) have reported that the green mussel has
greater thermohaline tolerance limits than the
brown mussel and this is why P. viridis could
displace P. perna in such a short time. The latter
species is characterised by relatively narrow incipient thermal limits and limited capacity for temperature acclimation, and as a result, its near extinction
was observed in the summer of 1997 in the Texas
Gulf of Mexico, when mean surface temperature
reached 30 C (Hicks et al. 2000). Thermal as well
as combined temperature-salinity tolerances of
P. perna are significantly lower than those of
P. viridis (Figures 7 and 8).
The increasing interest evinced by the scientic
community on P. viridis has created the need for

comprehensive information on various aspects of

its ecology, biology and culture. However, several
aspects of the ecology and biology of P. viridis still
remain poorly understood. Future research efforts
(see further), therefore, need to be directed to
narrowing the information gaps that have been
identified in this paper.
Future research needs
We list here the important gaps in information on
the various ecological and biological aspects of
P. viridis. The points that deserve greater attention
are:
1. Population ecology of the mussel, especially in
relation to the impact of the activity of
large mussel beds on the nutrient dynamics of
restricted environments such as bays and
harbours.
2. A more detailed understanding of the factors
influencing settlement of mussels on hard surfaces, with particular attention to the role of
water-borne or surface-associated cues on
gregarious settlement.
3. Standardization of a laboratory protocol for
the rearing of P. viridis larvae and settlement
bioassays using them, on lines similar to the
available information for barnacles.
4. Studies on molecular aspects of byssogenesis in
P. viridis.
5. Data on effect of predators, parasites and diseases on mussel community development for
developing biological control methods.
6. Data on the utility of byssus threads to reflect
environmental heavy metal concentrations.
Acknowledgements
We thank J. Goud, Naturalis Museum, Leiden for
kindly providing excellent photographs of various
species of Perna. This is publication number 395 of
the Centre of Wetland Ecology.
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