Aquatic Ecology (2006) Ó Springer 2006 DOI 10.1007/s10452-006-9032-8

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

S. Rajagopal1,*, V.P. Venugopalan2, G. van der Velde1 and H.A. Jenner3 1Department of 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; 3KEMA Power Generation and Sustainables, P.O. Box 9035, 6800 ET Arnhem, The Netherlands; *Author for correspondence (e-mail: [email protected]; fax: +31-24-355-3450)

Received 29 June 2005; accepted in revised form 25 January 2006

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

Abstract

The green 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 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 , which too is an invasive species, but to a more limited extent.

Introduction as a potential organism for commercial cultivation (Parulekar et al. 1982; Hickman 1992; Rajagopal The green mussel Perna viridis (L.) (Syn. Mytilus et al. 1998a), but also as a serious pest organism viridis, Mytilus smaragdinus, Mytilus opalus, in cooling water conduits of marine industries Chloromya viridis, Chloromya smaragdinus) (Sid- (Rajagopal et al. 1991a, 1996a, 2003a). The green dall 1980) is the tropical and subtropical counter- mussel is characterised by fast growth and rela- part of the relatively better studied tively high tolerance to many environmental vari- Mytilus edulis L., a mussel that is widely distrib- ables, making this species relatively difficult to uted in the higher latitudes (Bayne 1976). Both control using common antifouling techniques species are dominant in many rocky littoral and (Rajagopal 1997; Rajagopal et al. 2003a). Very shallow sublittoral ecosystems and often contrib- high densities of P. viridis have been reported from ute significantly to the productivity of coastal polluted harbours and submarine pipelines of benthos (Vakily 1989; Hickman 1992). The green coastal power stations (Rajagopal et al. 1997, mussel has been attracting lot of attention not only 1998b). The ability of this mussel to concentrate heavy metals and other pollutants from sur- Perna (Siddall 1980; Vakily 1989). P. viridis can rounding waters has been used by many be distinguished from the other three species researchers to employ these mussels as sentinel (P. perna, P. picta and P. canaliculus) by a few organisms (Sukasem and Tabucanon 1993; morphological characters (Siddall 1980; Rajagopal Sudaryanto et al. 2002; Monirith et al. 2003). 1997). The shell of P. viridis is emerald green in Recently, P. viridis has also received lot of atten- colour, but the colour can vary from blue-green to tion as an invading species at new localities brown, making it difficult to distinguish between (Agard et al. 1992; Kazuhiro and Sekiguchi 2000; P. viridis and P. perna. The external shell colour of Hicks et al. 2001; Ingrao et al. 2001). 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 The Genus Perna irregular areas of light brown and green. The dis- tinguishing anatomical characteristic of P. viridis is Classification the presence of enlarged sensory papillae along the edges of the mantle (Siddall 1980). The exhalent siphon and the inner surfaces of the inhalent Pteriomorphia aperture are outlined with a stripe darker than the Mytiloida variably patterned dark brown mantle (Morton Rafinesque, 1815 1987). Moreover, P. viridis can be distinguished Perna Retzius, 1788 from other species of the genus Perna in having 30 Within the genus Perna usually four species are instead of 28 diploid chromosomes (Ahmed 1974). distinguished, viz., the green mussel Perna viridis The diagnostic characters of P. viridis and P. perna (Linnaeus, 1758), the brown mussel Perna perna are presented in Table 1. (Linnaeus, 1758), the green-lipped mussel (Gmelin, 1791) and the Spanish mussel (Mediterranean green mussel) Perna picta Distribution (Born, 1780) (Figure 1). P. canaliculus and P. picta are geographically restricted to New P. viridis is native of the Indo-Pacific region, pri- Zealand and the Mediterranean Sea, respectively. marily distributed along the Indian and the However, the other two species enjoy wide dis- Southeast Asian coasts. They generally inhabit tribution in several parts of the world (Siddall marine intertidal, subtidal and estuarine environ- 1980; Vakily 1989; Hicks et al. 2001) and often ments with high salinity. P. viridis is a character- co-exist (Rajagopal et al. 1997, 1991b, 1998b). istic species of the fauna of midlittoral and They have been vigorously invading new geo- sublittoral zones, where it often constitutes dense graphical regions (Hicks and Tunnell 1993). The populations. It is gregarious and its large numbers introduction to new areas has been probably cluster together with the aid of its well-developed caused by international shipping, either as adults byssal apparatus. The mussels form a thick carpet- attached to ship hulls or as larvae in ballast water like growth on rocky surfaces and submerged tanks (Hicks and Tunnell 1995). P. perna was structures like wharves, pilings, breakwaters and first introduced to the Sea for culture buoys (Huang et al. 1983; Rao 1990) and they play purpose, which led to its successful establishment a very important role in rocky shore ecosys- in nearby areas (Hicks and Tunnell 1993). tems. These mussels attach to surfaces by P. viridis can potentially dominate its benthic threads colonizing submerged rocks, wood, con- habitat and displace other Perna species crete, metal, old submerged logs, boats, PVC (Rajagopal et al. 1997). 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 Morphology of Perna viridis is distributed along the southern tip of India, Sri Lanka (Kuriakose and Nair 1976), the coasts of There is much confusion in the literature regarding the African continent up to Morocco (Siddall the taxonomic status of species within the genus 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 , 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, Thick, equivalve, inequilateral, elongate and triangularly ovate in outline elongate and triangularly ovate in outline External colour of shells Green or bluish green Brown (light or dark) Maximum size 230 mm (shell length reported) 121 mm (shell length reported) Anterior side of the shell Pointed, beak-like and down turned Pointed, umbonal beaks poorly developed and slightly down turned Ventral shell margin Highly concave Straight Dorsal ligamental margin Curved Straight Mid-dorsal margin Arcuate A distinct dorsal angle or hump present Mantle margin colour Yellowish-green or light green Brown (light or dark) Ventral mantle margin Inner fold of the posterior ventral Inner fold of the posterior mantle margin: mantle margin: thin, extensible, smooth, very thick, not extensible and provided tentacles or papillae absent with 18-22 thick branching tentacles Size of hinge plate Thick, broad, extends slightly to the ventral border Thick, narrow and terminal Hinge teeth Two small on the left valve and one on the right valve One large on the left valve and a corresponding depression on the right valve Anterior adductor muscle* Absent Absent Muscle scars* Deeply impressed Deeply impressed Byssus apparatus Large and situated at the posterior base of the foot Large and located close to the base of foot Resilial ridge* Thick, white and highly pitted Thick, white and highly pitted Posterior byssal retractors* Two short and thick bundles Two short and thick bundles Excurrent aperture opening Mouth oval and wide; passage into Mouth and passage into the mantle the mantle cavity small; cavity are of same width; rectum and rectum and posterior adductor posterior adductor prominently visible not visible through the opening through the opening

*Similarities.

America including Venezuela, Brazil and Argen- Reproduction tina (Siddall 1980; Chung and Acunˇ a 1981). The native range of P. viridis stretches across the In P. viridis, the sexes are separate, but males and Indo-Pacific encompassing the Persian Gulf, In- females are not distinguishable by external mor- dia, Malaysia, Papua New Guinea and the South phology. The become sexually mature at Pacific islands, and north to Japan (Sivalingam 15 –30 mm shell length (i.e., about 2 –3 months 1977; Siddall 1980; Vakily 1989; Cheung 1993). old) (Siddall 1980; Vakily 1989). Males are distin- According to Siddall (1980), P. viridis has the guishable by the milky white gonads; females have potential to increase its geographical distribution bright orange brick red coloured gonads (Rajag- by ‘Island hopping’, a kind of step-wise larval opal 1991). Gonadal tissues of P. viridis appear to dispersal. Though it is not a part of the native be invading the whole of body, filling the mantle fauna of northern (Siddall 1980), it lobes, mesosoma and outer surface of the digestive has been recorded from Trinidad in the mid 1990s glands. Figure 2 shows the histological features of (Agard et al. 1992). P. viridis further moved ripe testes and ovaries in P. viridis. Fertilization is southward to the Gulf of Paria, using the pre- external. The spawning behaviour of P. viridis vailing currents and is thought to have dispersed to differs considerably (Vakily 1989; Rajagopal et al. Venezuela by currents (Agard et al. 1992) as well 1998a). Spawning is initiated by either sex, result- as by human activities (Rylander et al. 1996). The ing in the release of streams of gametes into the mussel larvae are believed to have been trans- water (Stephen and Shetty 1981). Spawning may ported via ballast water to Tampa Bay estuary, also be induced by the presence of other spawning Florida, where it is now well established (Tampa individuals in the area or also by a drop in salinity Bay Estuary Program 2000). (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 in P. viridis living in the cooling conduits of a drops to about 20& after heavy monsoon rainfall power station located on the east coast of India, (Rajagopal et al. 1989). The timing and duration of when the mussels were 7 mm in shell length. the reproductive cycle of mussels are believed to be However, in natural habitats in coastal waters, controlled by an interaction of environmental and Rajagopal (1991) observed signs of sexuality and endogenous factors (Seed 1976; Sastry 1979; Ka- gonad development in 12 mm long green mussels. utsky 1982; Rajagopal 1991). Barnes (1957) has The possible influence of unfavourable conditions shown that synchronization of spawning in marine (e.g., chemical stress from chlorine residuals) in epibenthic communities is particularly tuned to the the cooling water systems on the reproduction main blooms and only indirectly to and growth of P. viridis has been emphasised temperature. Kautsky (1982) reported that food (Rajagopal et al. 1998b). Based on experimental availability is the primary controlling factor for work on gonadal conditions of Atlantic and Baltic gonad growth in Baltic M. edulis. Relatively stable M. edulis over a period of 2 years, Seed (1969) and environments may promote year-round spawning, Kautsky (1982) concluded that sexual maturity with a couple of identifiable peaks (Parulekar et al. was not related to size but rather to age and 1982; Walter 1982). For example, in tropical waters growth rate of mussels. Thus, it is possible that of the Bay of Bengal, Rajagopal et al. (1998a, b) signs of sexuality and gonad development may be reported two spawning peaks. In subtropical observed in P. viridis even in specimens \7mmin environments the spawning is restricted to warmer shell length, especially when they are growing months (Shafee 1989). under unfavourable conditions. In such cases, the In M. edulis, signs of sexuality and gonad possibility of the mussels being older than what development were noted in mussels of shell length their shell size would indicate, must be considered. 2.0 mm (Seed 1969; Atlantic mussels), 2.1 mm (Kautsky 1982; Swedish Baltic mussels) and Gonadal development 2.2 mm (King et al. 1989; Ballynahown mussels, Galway Bay, west coast of Ireland). In compari- Based on histological and gonad squash prepara- son, Rajagopal (1991) recorded signs of sexuality tions, Rajagopal (1991) distinguished four main stages in the reproductive cycle of P. viridis (Fig- to water temperature which showed two clear ure 2). The stages are described below: peaks, one in April –June (30.9 °C) and another in October (31.3 °C) (Figure 3). Gonadal index Stage 1 (developing/redeveloping gonad): This matched with the temporal distribution of tem- includes (a) immature gonads, characterised by a perature, though larval abundance in the coastal thin, transparent and colourless mantle; hardly waters was determined largely by food avail- distinguishable sexes; follicles distinguishable as ability (Rajagopal 1991). Chlorophyll-a values small opaque areas and sometimes not visible; showed only a single summer peak in April –June gametogenesis initiated, but ripe gametes not yet and an increase in water temperature in October visible and (b) developing gonads, specimens with was not associated with a matching phyto- a relatively thick mantle; male and female gonads plankton increase. Therefore, it was hypothesised are distinguishable; creamy white in case of males that, following the second spawning in October, and orange in case of females; follicles larger and food acted as a limiting factor for the growing denser; gametogenesis is still progressing but larvae, resulting in low numbers of mussel larvae follicles contains mainly ripe gametes. in the coastal waters. Narasimham (1980) and Stage 2 (ripe gonad): Mantle much thicker than in Selvaraj (1984) also reported two main spawn- stage 1; male mantle milky white in colour and ing periods for P. viridis from the east coast of female bright orange brick red in colour; entirely India, which were seemingly associated with the packed with follicles and little connective tissue seasonal distribution of temperature. Previous seen between follicles; ova are compacted into studies on gonadal conditions of P. viridis indi- polygonal configurations; male gonad is distended cated that spawning was largely influenced by with morphologically ripe sperm. temperature, salinity and food availability (Rao Stage 3 (spawning gonad): Gonad tissues become et al. 1975; Nagabhushanam and Mane 1975; dull; reduction in sperm density; appearance of Qasim et al. 1977; Selvaraj 1984; Parulekar et al. empty spaces along with full follicles; the follicles 1982; Rivonker et al. 1993; Rajagopal et al. are about one third full of ripe gametes. 1998a). Correlations among spawning periodic- Stage 4 (spent/resting gonad): This stage includes ity, availability of food resources and salinity animals that have completed spawning; mantle have been demonstrated by Myint and Tyler semi-transparent; follicle wall ruptures and few (1982) and Walter (1982). Low et al. (1991) signs of residual gametes. observed two spawning peaks in P. viridis in the Eastern Johore Strait water (Singapore) during Gonad index (GI) can also be determined based on the inter-monsoon months of November and the method described by King et al. (1989): April. These correlated with the bimodal patterns for salinity, dissolved oxygen and total plankton GI ¼½Number in each stage biomass. In Hong Kong waters, peak spawning numerical ranking of that stage 100= was reported to occur only once a year (Lee ½Number of animals in the sample 1986). Cheung (1993), working on the population dynamics of P. viridis in the Tolo Harbour, where, gonad index of the sample may vary from 0 Hong Kong, reported two breeding periods per (all mussels resting) to 300 (all mussels ripe or year: one from July to September and another redeveloping). According to Seed (1976), the ranks from November to March. Lee (1985) reported are allotted as follows: 0 – resting; 1 – immature for the Victoria Harbour (Hong Kong) P. viridis and/or spent; 2 – developing and/or spawning; population, a single breeding period that 3 – ripe and/or redeveloping. extended from June to September. Yoshiyasu et al. (2004) reported that in the Sagami Bay, Japan, P. viridis reproduces successfully and Breeding seasons spawns from summer to early autumn. In the Indian coast, the breeding activity of Rajagopal et al. (1998b) reported that gonadal P. viridis can vary substantially within narrow development and spawning activity of P. viridis geographical regions, as was observed in Hong at Kalpakkam (east coast of India) were linked 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 occur- rence 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 spawning periods at Lynher and a single one at behaviour of P. viridis on the east coast of India is Cattewater in UK. Obviously, local hydrog- based mainly on spat settlement data (Godwin raphical conditions and food availability may act 1980; Nair et al. 1988), which may not give a as key factors that influence the timing of spawn- correct picture regarding gonadal activity because ing by a population (Lee 1985; Rajagopal 1997). successful spat settlement is dependent on a num- ber of environmental factors. Rajagopal et al. Larval development (1998b) showed that hydrographic conditions (especially salinity) even in closely located places The early development of P. viridis has been on a given coast (e.g., Kovalam, Edaiyur back- described by Tan (1975), Rao et al. (1976) and waters and Kalpakkam) could significantly differ Sreenivasan et al. (1988). The spawned eggs of from one another. This could probably explain the P. viridis become spherical and after fertilization differences in reproductive behaviour of P. viridis cleavage takes place. About 7 –8 h after fertiliza- at these sites. For blue mussel M. edulis, also, tion, the blastula transforms into a mobile, Bayne and Worrall (1980) have reported two trochophore larva (Siddall 1980; Rajagopal 1991). The veliger larval stage is developed after 16 –19 h increased settlement of P. viridis under high flow when it has a shell covering the internal body parts conditions. The high settlement intensity was and a strong ciliated velum (Sivalingam 1977). The attributed to enhanced propagule flux rate to the larvae secrete the initial byssal threads in 10 – substratum, because of increased water flow. 12 days and remain in plankton for another 15 – High velocity would permit settlement of only 20 days (Siddall 1980), until they find a suitable those larval forms, which have the ability to substratum (Sivalingam 1977; Appukuttan et al. withstand high shear force. Mussel larvae are 1984; Rajagopal 1997). Plantigrades attach to a capable of settling at high water velocities (Neit- variety of natural objects using byssus threads and zel et al. 1984; Rajagopal 1997), and it is reported are transported far and wide (Hicks et al. 2001). that at velocities as high as 3.5 m s)1, mussels Widdows (1991) has reviewed the effects of could settle and colonise new surfaces (Neitzel environmental factors, such as food availability, et al. 1984). Rajagopal et al. (1998b) also studied temperature, oxygen concentration, salinity and depth-related variation in green mussel settlement pollutants, on the processes of feeding, metabolism (Figure 4). Plantigrades preferred intermediate and growth of mussel larvae. The planktonic larval depth (4 m) to near-surface (1 m) or near-bottom stage and the immediate post-settlement stage in (7 m), which is probably related to the subtidal mussel larvae are characterised by high mortality habitat of the mussels. Depth-wise differences in rates. Factors that reduce growth rate, and thereby spat fall are likely if the larvae are non-uniformly extend larval duration in the water column, will distributed in the water column or alternatively, significantly reduce the chances of survival of the the settling larvae prefer discrete light regimes larvae to the settlement stage. In the coastal waters (Figure 5). However, this depth-related feature of Kalpakkam (east coast of India), Rajagopal was not apparent at high flow conditions as was et al. (1998b) reported a maximum mussel larval observed at the intake point of a power station, density of 39,500 larvae m)3 in May (Figure 3), owing probably to turbulent water flow, which which is comparable with densities reported from would disturb any vertical distribution of larvae elsewhere for other mussel species. Schram (1970) or prevent the larvae from exercising their light recorded a similar density (40,000 larvae m)3) for preferences. M. edulis from the Oslo fjord. Hopkins (1977) Apart from flow, settlement pattern in marine observed the lamellibranch larval densities in mussels is influenced by other factors such as Tampa Bay to range from 1200 to 15,500 lar- substratum (Rajagopal 1991; Lasiak and Barnard vae m)3, with an annual mean of 8000 larvae m)3. 1995; Rajagopal et al. 1998a, b). P. viridis selects a Fish and Johnson (1937) reported peak abundance favourable surface prior to the secretion of byssus of more than 25,000 larvae m)3 in Bay of Fundy. (Nishida et al. 2003). According to Widdows (1991), settlement-ready pediveliger larvae of Settlement mussels can delay the process of settlement and metamorphosis for several weeks until a suitable For benthic marine invertebrates like mussels, substratum is found, though such a delay may planktonic larvae represent the rather limited result in a decline in the number of offspring mechanism available for dispersal. Settlement surviving. Alfaro et al. (2005) studied early settle- represents the transient phase between the pelagic ment patterns of P. canaliculus within water tanks life of the larvae and the benthic existence of the exposed to different water flow regimes and oxy- adult. According to Abelson (1997), flow of water gen concentrations. Hatchery-reared larvae and affects settlement in different ways: (a) it can act wild juvenile mussels (0.5 –3.0 mm shell length) by exerting hydrodynamic forces on the settling were used for the experiments. Settlement of larvae larvae, influencing their encounter with the sub- increased with increasing water flow; also higher stratum and their behaviour following encounter; oxygen concentrations appeared to enhance larval (b) it may provide a settlement cue that could settlement but not in juveniles. Interestingly, the induce active behaviour of the larvae and (c) flow experiments suggested that exploratory behaviour may act to mediate various settlement cues (i.e., settlement and re-settlement) takes place (e.g. sediment load and the concentration of within low and medium water flows, but not under attractants). Rajagopal et al. (1998b) reported 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 tripeptide (glycine –glycine –arginine) at concen- ) re-settlement processes in P. canaliculus. It would trations as low as 0.56)3.7810 10 M. That the be interesting to investigate if similar mechanisms chemical cues play any significant role in the operate for P. viridis as well. aggregation of P. viridis needs further investigation. There is not much information on the response of mussel plantigrades to environmental cues. While similar information is being accumulated on Growth rate the larval response of other fouling species (e.g., barnacles, polychaetes and hydroids), progress in P. viridis is capable of high growth rates, especially the case of mussels have been hampered largely under favourable conditions (Vakily 1989). due to the difficulty in consistently and successfully Rajagopal et al. (1998b) reported that on the rearing mussel larvae under laboratory conditions southeast coast of India, the mussel could reach (Bidwell et al. 1999). Interestingly, De Vooys 119 mm shell length in the first year and 152 mm (2003) showed that in blue mussels (M. edulis) in the second year (Figure 6). However, such rates environmental chemical stimuli could cause their were observed at higher than normal flow condi- aggregation. Individual mussels were attracted tions i.e., on the screen walls of a power station and moved actively upstream, in response to a 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 growth rates of P. viridis include Lee (1985, 1986) elsewhere in India: 93 mm year)1 from Kakinada and Cheung (1993). In many studies, the influence on the east coast (Narasimhan 1980) and 96 mm of season was highlighted. Chatterji et al. (1984) year)1 from Goa on the west coast (Rao et al. recorded maximum growth rate at Goa (west coast 1975; Rivonker et al. 1993). Such a high growth of India) during March –May, coinciding with the rate was attributed to increased food flux rate phytoplankton maximum. Mussels in polluted caused by the high flow (Rajagopal et al. 1998b). waters generally show a low growth rate: Lee The overriding importance of food supply in (1986) recorded low growth rates (5 mm month)1 mussel growth rate has been emphasised by Seed in the first year of their existence) in the polluted (1976), Seed and Suchanek (1992) and Wildish and Victoria Harbour, Hong Kong. Similarly, Cheung Kristmanson (1997). Other authors who studied (1993) reported a growth of 49.7 mm in the first 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, behav- ioural and morphological features of P. viridis collected from Tolo Harbour, Hong Kong. They found P. viridis to tolerate a high level of sus- pended particulate matter (up to 1200 mg l)1). Figure 6. Growth of Perna viridis in Kalpakkam after settle- However, there were dose-dependent effects of ment in coastal waters and on the intake screens of cooling suspended particulate matter on the morphology conduits of a power station. Data are presented as mean±SD of gill filaments. The observations that P. viridis (n=27 –30). colonise even muddy sediments, point to the high level of tolerance of the green mussels to high year of their existence from Tolo Harbour, an- suspended particulate matter (Segnini de Bravo other polluted harbour in Hong Kong. Compared pers. comm.). with values reported by Vakily (1989) and Tomalin (1995), the growth rate recorded at Kalpakkam, southeast coast of India (Rajagopal et al. 1998b), Byssus thread production stands apart, being 10 mm month)1 a rate that is the highest ever reported for P. viridis. Mussels are tethered to the substratum by means of a byssus, an extracorporeal collagenous struc- ture 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 artificial 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 Figure 7. Exposure time required for 100% mortality of Perna (Romero and Moreira 1980; Saloma˜ o et al. 1980). viridis (Rajagopal et al. 1995a) and Perna perna (Rajagopal Sivalingam (1977) reported that the normal fluc- et al. 1995b) at several high temperatures. Mortality data are expressed as mean±SD (n=36) of six replicate experiments tuation in salinity (27 –33&) observed in estuarine (n=6 in each experiment). The criterion for mortality of habitats was well within the lower and upper mussels was valve gaping with no response of exposed mantle tolerance limits of P. viridis. However, it can tissues to external stimuli. 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 corre- sponding proteins in P. viridis. Several authors have investigated the environ- mental influence 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 influence byssogenesis (Young 1985; Rajagopal et al. 1996b). In most studies, wave action and mechanical effects proved to be the most impor- tant factors that affected the rate of byssus pro- duction (refer to Rajagopal 1997 for review). Young (1985) showed that M. edulis produced up to 15 threads per mussel within a day when agi- tated every 4.5 s, while P. viridis produced up to 68 threads per mussel within a day, when agitated )1 Figure 8. Exposure time required for 100% mortality of Perna every 3 s (i.e. 20 cycles min ) (Figure 9). Thread viridis subjected to the combined effect of salinity and temper- production, under increasing mechanical agita- ature (modified after Rajagopal et al. 1995a). Mortality data tion, showed an initial increase followed by dras- are expressed as mean ± SD (n=36) of six replicate experi- tic reduction (Figure 9). Cheung et al (2004a, b) ments (n=6 in each experiment). observed that longer and thicker byssal threads were produced by P. viridis, when exposed to three distinct parts, viz., root, stem and thread damaged conspecifics and predators compared (Bayne 1976). Each thread, in turn, consists of a with control. It was surmised that stronger byssal proximal part, a distal part and an attachment attachment would reduce predation as well as non- plaque. The byssal thread functions like a shock predation mortality. In the laboratory, cumulative absorber in its mechanical design: it is strong and byssus threads production by P. viridis, shows a stiff at one end and pliably elastic at the other continuous increase with time and within seven (Waite et al. 1998). Cheung et al. (2004a, b) have days, a mussel (12 mm size group) produces on an shown that byssus production is a plastic response, average about 90 threads (Figure 10), which is influenced by exposure to chemical signals from about twice the figure for P. perna. predators and damaged conspecifics. Nishida et al. (2003) observed that byssus production in P. viridis was significantly influenced by the nat- ure, especially, surface free energy as well as dis- persion 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 Figure 9. Effects of agitation on the byssus thread production protein variants for deposition onto a given sur- of Perna viridis and Perna perna (redrawn from Rajagopal, face might be determined at the level of transla- 1991). Old byssus threads were removed before the experiments tion. Such a flexibility would provide great started. Byssal thread production in post larvae takes gen consumption is also closely linked with the place for the purpose of drifting. These threads pumping of water. Filtration and feeding in mus- differ from the attachment threads: the drifting sels have been extensively dealt with by Bayne threads secreted by young post-larval mussels of (1976). Rajagopal (1991) has estimated the filtra- M. edulis are simple monofilaments, distinct in tion rate in P. viridis as a function of mussel size, structure and function from the attachment byssus temperature, salinity and light –dark cycle. To threads. The attachment threads are relatively estimate the amount of water filtered through the short and have a terminal attachment plaque, gills, he used the dye absorption technique drifting threads are longer and exceed the post- (Coughlan 1969), which is based on absorption of larva in length by more than two orders in mag- neutral red by actively filtering mussels. The data nitude and are without plaques or any other show that filtration rate (expressed as volume of structures (Lane et al. 1985). The drifting threads water filtered per mussel) increases with mussel help in the dispersal of young mussels over wide size. Optimum filtration rates of P. viridis were geographical areas. Calculations by the authors observed at a temperature and salinity of 30 °C showed that the drifting threads would increase and 30 –35&, respectively (Rajagopal 1991). The the fluid drag experienced by the post-larvae of filtration rates were significantly higher in mussels M. edulis in the water column. In fact, the theo- kept in complete darkness, compared with those retical viscous drag force on the threads would be maintained in day light or light/dark conditions sufficient to significantly reduce the sinking rate of (Figure 11). It is generally observed (Rajagopal, drifting post-larvae and effectively enhance their unpublished data) that shadows falling on them dispersal. Very little work has been done on bys- disturb the feeding of P. viridis, probably as a sogenesis in P. viridis and more focussed research defence mechanism against predators. Defence in this area is due. against predation could be the reason for higher filtration in darkness. Figure 12 shows oxygen consumption rates as a function of tem- Filtration perature. Optimum oxygen consumption occurred at 30 °C, while at 40 °C oxygen consumption In mussels gills and ciliary mechanisms associated declined to nil. with them serve to pump water and collect, Rajesh et al. (2001) showed that in P. viridis, transport and sort food particles (Morton 1983). increasing algal concentrations resulted in an in- Food particles are entrapped in mucus strings and crease in the filtration and ingestion rate, until a ) transferred to labial palps, which regulate entry of concentration of 1 105 cells ml 1 was reached, at food into the mouth. The labial palps also help in which pseudofaeces production started. Wong and rejection of excess material as pseudofaeces. Oxy- 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 Figure 11. Effects of light and darkness on the mean filtration mean±SD (n=20). Old byssus threads were removed before rate (n=18; experimental duration=3 h) of Perna viridis and the experiments started. Perna perna. feeding responses of P. viridis for two complete average organic enrichment of filtered relative to tidal cycles, covering both spring and neap tides. available matter and a higher average organic Feeding rates and absorption efficiency were enrichment of ingested relative to filtered matter highest at low tides and lowest at high tides. than have so far been recorded for any species of The clearance rate of the mussels was influenced filter-feeding bivalve. by the tides and was a negative power function of Filter-feeding bivalves can assimilate various total particulate matter and a positive linear kinds of suspended food like plankton, including function of organic content in water. Pseudofaeces dissolved substances (Jo¨ rgensen 1983; Gorham were produced only during spring tide but not 1988; Roditi et al. 2000), bacteria (Crosby et al. during neap tides. Wong and Cheung (2001) 1990; Langdon and Newell 1990; Kreeger and observed that by adjusting feeding rates and Newell 1996), and heterotrophic nanoflagellates enzymatic activities, food absorption in P. viridis (Sherr et al. 1986; Kreeger and Newell 1996). remained constant, irrespective of the changes in Detritus also forms an important part of the diet food availability. Hawkins et al. (1998) compared of P. viridis (Rao 1990). Based on data from the suspension feeding behaviour of different experimental feeding of Mytilus edulis with roti- tropical bivalve molluscs (P. viridis, fers, Wong et al. (2003), argued that dense popu- belcheri, C. iradelei, Saccostrea cucullata and lations of mussels could exert a strong top –down Pinctada margaritifera) under natural seston con- effect on planktonic food webs. Rajagopal et al. centrations. As seston availability increased, a (1991a) have shown that P. viridis are capable of minimum average of 71% of the filtered material forming extremely dense populations in coastal was rejected by each species as pseudofaeces. waters. The effect of such massive Interestingly, all species preferentially rejected as communities on coastal plankton dynamics and pseudofaeces particles with higher average inor- planktonic-benthic energy transfer need to be ganic content, which resulted in a net organic examined in greater detail. For example, Kim- enrichment of the ingested material. P. viridis has merer et al. (1994) showed that naupliar stages of been shown to be capable of selectively capturing copepods could be vulnerable to bivalve grazing. It particles from the water filtered (Ke and Wang may be possible that instead of feeding solely on 2002). Using radiotracers to label diatoms and phytoplankton, which would reduce food for natural sediment, they showed that P. viridis could herbivorous , bivalves may exert a selectively ingest diatom particles from a suspen- top –down effect by preying directly on zoo- sion. However, no significant particle selection was plankton (Wong et al. 2003). observed at concentrations below the level of pseudofaeces production. Hawkins et al. (1998) showed that the fast growth in P. viridis resulted Excretion from a higher average clearance rate, a higher Nitrogenous compounds, end products of protein and amino acid catabolism, are the major excre- tory 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 excre- tion. 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 stop- Figure 12. The oxygen consumption of Perna viridis and Perna ped completely at 15&. Apart from ammonia, perna at different temperatures. Data are expressed as animals excrete nitrite and nitrate as part of a mean±SD (n=12). mechanism for detoxification of ammonia and maintenance of internal ionic stability. Masila- for example, the gastropods opted for mussels moni et al. (2001) reported that nitrite and nitrate previously unexposed to predator cues. Apart excretion in P. viridis showed increase with from predator gastropods, other organisms also decrease in salinity. Phosphate excretion, on the damage mussel shells by boring into them. other hand, decreased significantly with decrease Microbial phototrophic endoliths (mostly cyano- in salinity. bacteria) bore into P. viridis shells and cause Release of nitrogenous (ammonia, nitrite and considerable shell degradation (Kaehler and nitrate) and phosphorus (phosphate) wastes by McQuaid 1999). The authors reported that by large mussel communities may significantly affect attacking the shell such borers reduce the longevity the nutrient dynamics of the receiving water body and reproductive output of the mussels. (Kuenzler 1961; Richard and Dankers 1988). Pea crab (Pinnotheres sp.) is reported to be a There have been reports of mussel activities commensal in P. viridis. Recently, Jose and (especially, selective filtering and nutrient excre- Deepthi (2005) reported the prevalence of Pinnot- tion) promoting algal blooms in bays and lakes heres placunae in green mussels along the Malabar (Vanderploeg et al. 2001). Discharge of condenser Coast of India. Male and female (egg bearing) effluents from cooling water systems of coastal crabs were observed in the mantle cavity of about power plants that harbour massive mussel com- 6% of the mussels sampled over a one year period. munities (e.g., see Venugopalan et al. 1991) into The infected mussels had significantly lower shell inshore areas need to be studied from this point of size and live weight and were characterised by gill view (Masilamoni et al. 2001). In view of the damage (gill erosion and malformation). Koya dramatic population increase of P. viridis in many and Mohandas (1982) reported the presence of coastal localities, bays and harbours, it is sug- adults of a digenetic trematode of the genus gested that nutrient loading by mussels be given Gorgoderina in P. viridis. due attention by researchers.

Cultivation Pest and predators Commercial cultivation of Perna mussels According to Bayne (1976), natural enemies of (P. viridis, P. perna and P. canaliculus) is exten- mussels fall into four categories: predators, com- sively carried out in several countries and the petitors, parasites and shell borers. Algae, hy- subject has been reviewed by Vakily (1989). In droids, free and tubiculous polychaetes, barnacles, mussel farming, harvesting phase commences amphipods and ascidians are important pests when the mussels reach minimum marketable size. which colonise the outer surface of shell valves of This varies significantly according to species, P. viridis and compete for space. The main pre- geographic region and cultivation method. In dators include crabs, fishes, starfish and temperate waters, the mussels (e.g., M. edulis) (Rao 1990). The mud crab Scylla serrata is con- reach marketable size only after a long culture sidered a major predator of P. viridis, while among period viz., 12 –24 months (Hickman 1992). fishes snapper, silver bream and black tail have However, in the tropical/subtropical marine mus- been mentioned (Vakily 1989). However, there are sel P. viridis, marketable size is achieved after a not many studies on the effects of predation on relatively short culture period, i.e., about 6 months P. viridis. Cheung et al. (2004a, b) studied the (Sivalingam 1977; Parulekar et al. 1982; Vakily defensive responses of P. viridis on being 1989; Rivonker et al. 1993; Rajagopal et al. challenged with two predators, the muricid gas- 1998a). This confers a potential advantage to tropod, Thais clavigera, and the portunid crab, farmers of P. viridis over their counterparts in Thalamita danae. They observed that responses of other parts of the world. the mussels were predator-specific. Mussels raised A few values are available for the increases in in the presence of crabs developed thicker shell at meat and shell mass of cultivated P. viridis from the umbo and lip margin, while those raised in the the different parts of world. An increase of presence of gastropods had a thicker shell lip. 1.13 g month)1 for first 6 months and thereafter a Predators also were shown to choose their prey; rate 0.11 g month)1 were reported from the east coast of India (Rajagopal et al. 1998a). A general jagopal et al. 1991a, b). Among them green mus- increase in meat and shell mass coincided with the sels were the most dominant species, in terms of latter half of the post monsoon and early summer biomass. The green mussels have proven to be a period, when plentiful food material and optimum successful fouling species in a variety of maritime hydrographic conditions prevailed. Spawning and industrial environments. Their widespread during April –May and September –October distribution and their ability to attach to different resulted in a sharp decline in the meat weight surfaces even at high flow rates and to make use of (Figure 13). The rates of seasonal increase in shell water flow to achieve fast growth rates and high and meat growth were uncoupled during the population densities, make them highly suited to period from May to November, exhibiting little colonise cooling water systems (Rajagopal 1997). correlation between them, partly due to loss in soft Their characteristic ability to survive extremes of tissue weight resulting from spawning (Figure 13). environmental conditions (salinity 0 –64& and Similar results were also reported from eastern temperature 6 –37.5 °C), thrive well in turbid Long Island Sound, USA (Hilbish 1986) and coastal waters (Morton 1987) and survive under Beggars Island, southwest England (Salkeld 1995) prolonged biocide dosing that gets rid of most of for populations of M. edulis. For P. viridis,an their competitors (Rajagopal et al. 2003a), has inverse relationship between density and produc- contributed to their extraordinary success as foul- tion was found: mussel production increased with ing species. In fact, P. viridis can withstand harsh decreasing density (Figure 13). Rajagopal et al. environmental conditions better than its temperate (1998b) reported that the increase in the weight of counterpart Mytilus edulis (Morton 1987) or its co- individual mussels compensated for the decrease in existing species P. perna (Rajagopal 1997). the density of population, thereby resulting in a Uncontrolled growth of the green mussels can progressive increase in production and biomass create problems for power plants using seawater as (Loo and Rosenberg 1983; Rivonker et al. 1993). the condenser coolant. With continuous flow of However, higher production and biomass rates water that brings in sufficient quantity of food were observed for the first six months (P=5.23 and oxygen, apart from fresh stock of larvae, the kg m)1 month)1; B=2.48kgm)1 month)1), and exposed surfaces like intake tunnel, screens, pipes they were significantly lower for the later and culverts are quickly colonised by young mus- 6 months (P=2.73 kg m)1 month)1; B=1.18 sels (Rajagopal et al. 1996a). Economic aspects of kg m)1 month)1). In general, older mussels have a fouling-induced effects on electric power plants poor growth rate due to reduced metabolic activity can be very significant, such as reduced flow of (Cheung 1993), filtration rate (Bayne et al. 1976), cooling water for steam condensation, causing feeding rate (Seed and Suchanek 1992) and increased condenser backpressure and below- increased gamete production (Hilbish 1986). optimum performance (Rajagopal 1997). Live Although commercial cultivation of P. viridis mussels or empty shells can cause mechanical has a bright future, the recent reports regarding damage to pumps and block the flow of water in shell fish poisoning in P. viridis are disconcerting. condenser tubes and reduce the heat transfer effi- Paralytic and diarrhetic poison (PSP and ciency (Neitzel et al. 1984; Rajagopal et al. 1994). DSP), caused by harmful algal blooms (HAB) Mussel shells can also cause accelerated corrosion were detected in P. viridis from Singapore and of the condenser tubes (Fischer et al. 1984). There Trinidad (Holmes et al. 1999; Yen et al. 2004). are reports of extensive growth of green mussels in the condenser cooling systems of power stations in India (Rajagopal et al. 1991a, b). Green mussels and biofouling Over the years, P. viridis has been able to expand its geographical territory into new areas. Bivalves are a key component of the fouling Today, it is recognised as a potential fouling community that develops inside the cooling cir- organisms in countries such as Malaysia, Hong cuits of coastal power plants. Previous studies Kong, Japan, China, USA (Florida), Trinidad and showed that out of 94 species collected from within Venezuela, making it a truly global player (Morton the seawater intake system of a tropical power 1987; Agard et al. 1992; Kazuhiro and Sekiguchi station, more than 17 were bivalve species (Ra- 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-upratesashighas211kgm)2 year)1 have Mussel control been reported (Rajagopal et al. 1997). With more and more power stations being built in tropical, third The type of fouling control measures adopted by world countries, where seawater will be used as an industry depends on the system being fouled. condenser coolant owing to shortage of fresh water, Antifouling paints have been the method of choice it is anticipated that problems due to green mussel for combating biofouling on ship hulls. However, fouling will aggravate and need to be tackled. paints have only limited service life and require re-application at regular intervals. Hence they are Consequently, the larvae do not settle inside the of not much use in the case of power plant cooling system, but return to the sea along with the out- systems. Biocides used for biofouling control are going water (Rajagopal et al. 1991b). Lower con- of two major categories: oxidizing biocides and centrations of chlorine ( \0.5 mg l)1) are known non-oxidizing biocides (Rajagopal 1997). The to produce changes in swimming and crawling former include chlorine (gas or sodium/calcium behaviour of mussel larvae (Jenner et al. 1998). hypochlorite), bromine, active halogen com- Moreover, growth rate of adult mussels under pounds, ozone, hydrogen peroxide and chlorine continuous low-dose chlorination is substantially dioxide, while the latter include aldehydes, amines lower than that of an untreated population and quaternary ammonium compounds, organo- (Rajagopal 1991, 1997). Several power stations bromines and organo-metals (Jenner et al. 1998). have successfully employed low-dose continuous The mechanisms by which the various biocides chlorination to control mussel fouling, including bring about mortality of the organisms are not that by P. viridis (Rajagopal et al. 1996a). How- fully understood. However, the major causes are: ever, the main disadvantage of this method is that (1) damage of the cellular organization, particu- interruptions in chlorination will allow mussels to larly damage of the semipermeable cell membrane settle, which on resumption of chlorination are not or nucleic acids, (2) interference with the energy easily dislodged (Rajagopal et al. 2003c). production mechanism by inactivation of enzymes Mussels by nature are relatively quite tolerant or the oxidative phosphorylation process that to chlorination. The resistance of adult mussels to generates cellular energy and (3) interference with chlorination partly comes from their ability to the biosynthesis of proteins and nucleic acids tightly close their bivalve shells and isolate (Jenner et al. 1998). themselves from the ambient water conditions for Power plant biofouling control has traditionally long periods of time, and switching from aerobic been achieved by either continuous or intermittent to anaerobic metabolism. This allows the mussels chlorination (Rajagopal et al. 2003b, c). Chlori- to withstand extreme high chlorination concen- nation still remains the most preferred mode of trations of [5mgl)1 (Rajagopal 1997). At a biofouling control in cooling water circuits, owing power station in India, it was necessary to employ to economy, easy availability and wide-spectrum shock-dose chlorination (2 –3 mg l)1) for several efficacy. Although effective control of all types of weeks at a stretch to get rid of the a mussel fouling can be achieved by chlorination, there are population that had established in spite of inter- inherent problems involved in the use of chlorine: mittent chlorination at a level of 1 –2 mg l)1 hazards of handling chlorine gas cylinders, diffi- residuals (Rajagopal et al. 1996a). Data by Mas- culty in maintaining chlorination plants and ilamoni et al. (2002) show that the green mussels non-uniform distribution of chlorine residual at can sense residual chlorine levels \0.15 mg l)1 required sites. Often, it is prudent to adopt suitable and complete valve closure occurs only at preventive measures to avoid or reduce the inten- 0.55 mg l)1. Recent research has shown that sity of mussel fouling, rather than to get rid of it, operational costs associated with chlorine dosing after the mussels established themselves within the can be brought down by judicious dose reduction. cooling circuits. This is because prevention of Research carried out at KEMA, The Netherlands, settlement by young green mussels can be achieved has shown that efficient mussel control could be at much lower biocide levels than that required for achieved by rapidly pulsed chlorination called killing attached adult populations (Rajagopal Pulse-ChlorinationÒ. This technique leads to 40 – et al. 1991b). Accordingly, the developed methods 70% reduction in chlorine use. The method are based on continuous dosing of chlorine, which makes use of the lag time (recuperation time) creates an environment inside the cooling cir- between stoppage of chlorination and full opening cuit that is unattractive to the incoming larvae of the shells by mussels and, in effect, fools the (Rajagopal et al. 1991a). A term – exomotive mussels into ,thinking’ that the dosing is contin- chlorination – has been coined to describe this uous (Polman and Jenner 2002; Rajagopal et al. method of chlorination, which exploits the fact 2003c). However, such a technique will only be that incoming mussel larvae are selective about the feasible if the dosing system is reliable and if the environment in which they settle (Lewis 1985). Total Residual Oxidant or Free Oxidant concen- tration is monitored accurately and continuously. copper, chromium, nickel and cadmium in the Moreover, simultaneous spat settlement moni- Gulf of Thailand (see also Sudaryanto et al. 2002; toring (e.g., using spat monitors) is also required Blackmore and Wang 2003; Bayen et al. 2004). to determine the efficacy of the treatment. This However, byssus threads of mussels accumulate can be done by simple biofouling monitors. Pulse- heavy metal better than meat (Van der Velde et al. Chlorination is adapted as BAT (Best Available 1992, and literature therein). Recently, Yap et al. Technique) in Europe (Polman and Jenner 2002). (2003) used byssus threads of P. viridis as reliable Increasing awareness of the carcinogenic effects indicators of heavy metal pollution in the envi- of chlorination by-products has led to stricter ronment. They observed that concentrations of limitations being placed on effluent limits of Cu, Cd, Pb and Zn in the attachment plaques of residual chlorine (Jenner et al. 1998). Conse- P. viridis were higher, compared with the other quently, there has been a search for alternate parts of byssus, foot and total soft tissue. They methods of fouling control, which are cheap, inferred that different protein composition could effective and safe. In this context, heat treatment, a be the reason for the different heavy metal levels potential alternative, is being practised by several observed in the different parts of the byssus. utilities (Rajagopal et al. 1994, 2005a, b). Steam However, more work is needed to to find out how electric power plants generate waste heat and, accurately byssal levels of heavy metals could therefore, heat treatment can be a viable fouling reflect environmental concentrations. control measure in cooling water circuits of Biomarkers are increasingly being employed to power plants. This method entails a power penalty ascertain the health of marine mussels exposed to due to increased condenser vacuum loss during polluted environments. They provide meaningful the treatment period. Nevertheless, it has been information on the potential impact of a variety of reported to be economical under tropical condi- pollutants on the health of mussels, before the tions, owing to the rather narrow difference effects are manifested externally. Depending on between ambient and lethal temperatures in the the effect of different kinds of contaminants, case of tropical fouling organisms, as compared different categories of biomarkers have been with their temperate counterparts (Rajagopal identified (Narbonne et al. 1999; Lau and Wong 1997). Several plants in Europe and North 2003; Damiens et al. 2004). Biomarkers generally America are presently using heat treatment to have higher sensitivity and specificity at molecular control mussel fouling in their cooling water levels. Often, it is necessary to use a number of systems (Jenner et al. 1998). biomarkers (multimarker approach) to get a real- istic picture of the overall response of mussels to degradation in water quality. The suitability of Mussels as biomonitors antioxidant enzymes, e.g. glutathione S-transfer- ase, super oxide dismutase, catalase, glutathione The use of bivalves, especially mussels, as sentinel peroxidase and glutathione reductase, have been organisms (the ‘Mussel Watch’ concept) for mar- examined in P. viridis (Cheung et al. 2001; Lau ine pollutants has been proposed by Goldberg and Wong 2003). Recently, Nicholson and Lam (1986) and Bayne (1989). This method served to (2005) have reviewed the status regarding the use monitor the pollution in the world oceans in the of biomarkers in P. viridis from the view point of 1980s and 90s (Goldberg and Bertine 2000). Using pollution monitoring. We now know that mantle this method, mussels have been used as bioindi- and gills are relatively more biomarker-responsive cators to study contamination of coastal waters by than the rest of the body (Prakash and Rao 1995). a variety of organic and inorganic pollutants, Since gills are directly involved in filter-feeding including heavy metals, organochlorines and and respiration, they form the frontline organs PCBs. Biomonitoring of persistent organochlo- exposed to water-borne contaminants (Lau and rines in the coastal marine environments of the Wong 2003). Asia pacific region, carried out using P. viridis,can Lawrence and Nicholson (1998) have shown be found in recent work by Monirith et al. (2003). that stress proteins are sensitive biomarkers of Sukasem and Tabucanon (1993) used P. viridis to environmental stress in mussels. They observed monitor heavy metals such as zinc, manganese, induction of stress proteins in mussels at chlorine residuals as low as 0.01 –0.07 mg l)1. Nicholson the presence of natural hard substrata does not (1999) discussed the utility of physiological bio- seem to be necessary for large scale colonization of markers (e.g., cardiac activity) for pollution mon- P. viridis. As a result, the population densities of itoring using P. viridis. Studies by Siu et al. (2004) P. viridis in the Gulf of Mexico have exceeded demonstrated that induction of micronuclei (MN) those of native mussel species (Ingrao et al. 2001). in the gill cells of P. viridis could be used as a It is imperative that further spread of the mussel be sensitive and stable biomarker of exposure to rel- monitored on a regular basis. atively low levels of genotoxicants. They observed Warming of world’s oceans can be expected to an increase in MN frequency with continued increase the geographical distribution of tropical addition of genotoxicants, which did not decrease and subtropical species, especially of the eury- significantly when the external exposure was thermal type. According to data available from the decreased or completely stopped for one to two U.S. National Climatic Data Centre, the average weeks. Their studies also showed that chronic global surface temperature is expected to rise by exposure could lead to a greater genotoxic impact 0.6 –2.5 °C in the next 50 years and by 1.4 –5.8 °C than acute exposure. in the next century, with significant regional vari- ations. Such expected increases in seawater tem- perature would definitely have a significant Perna viridis – the great invader influence on the distribution of species such as P. viridis. More studies on these lines are urgently P. viridis is credited with considerable success as an warranted. invading species, conquering new geographical locations in the east and the west. In general, the life history traits that make a successful invader Perna viridis vs. Perna perna are: a short life span, rapid growth rate, rapid sexual maturity, high fecundity, greater ability to From the foregoing account, it is clear that P. viridis colonise a wide range of habitats, wide physio- has not only ecological and economic impacts but logical tolerance, gregarious behaviour, suspen- also significant human health impacts. P. viridis can sion feeding and ability to repopulate following a out-compete many other benthic species, causing population crash (Morton 1997). In the opinion of changes in community structure and food web Bayne (1976), the competitive superiority of mus- relationships. For example, since the appearance of sels basically stems from their rapid recruitment P. viridis, in the Golfo de Paria in 1993, the habitat and growth, their ability to detach and re-attach of the brown mussel, Perna perna, has been altered with byssus and their ability to quickly migrate to (Segnini de Bravo et al. 1998). Subsequently, vacant spaces thrown open by natural forces. It is P. viridis has driven out P. perna from its natural obvious that P. viridis is endowed with several beds in La Esmeralda, Guatapanare and El Morro characteristics that qualify it for a successful de Chacopata, Sucre State, Venezuela. Hicks et al. invader (Figures 3 –6). (2001) have reported that the green mussel has It is generally perceived that transport of the greater thermohaline tolerance limits than the mussels far and wide has been aided by modern brown mussel and this is why P. viridis could shipping operations. Adult mussels could be car- displace P. perna in such a short time. The latter ried to newer geographical locations as part of the species is characterised by relatively narrow incipi- hull fouling community. Alternatively, larvae or ent thermal limits and limited capacity for temper- young ones could be transported via ship ballast ature acclimation, and as a result, its near extinction water. P. viridis was discovered in the Tampa Bay, was observed in the summer of 1997 in the Texas Florida, in 1999. Prior to that, it was reported at Gulf of Mexico, when mean surface temperature Point Lisas, Trinidad (in 1990), Gulf of Paria, reached 30 °C (Hicks et al. 2000). Thermal as well Venezuela (in 1992) and Kingston Harbor, Ja- as combined temperature-salinity tolerances of maica (in 1998). Mussel beds along the Indian P. perna are significantly lower than those of coasts are known to occur only in those coastal P. viridis (Figures 7 and 8). belts where natural rock formations are present. 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