Aquatic Ecology 32: 313–322, 1998. 313 © 1998 Kluwer Academic Publishers. Printed in the Netherlands.

Settlement and growth of the green viridis (L.) in coastal waters: influence of water velocity

S. Rajagopal1, V. P. Venugopalan2,K.V.K.Nair2, G. Van der Velde1 andH.A.Jenner3 1Department of Ecology, Laboratory of Aquatic Ecology, University of Nijmegen, Toernooiveld, 6525 ED Nijmegen, The Netherlands (E-mail [email protected]); 2Marine Biology Programme, Water and Steam Chem- istry Laboratory, BARC Facilities, Kalpakkam 603 102, India; 3KEMA Power Generation, P.O. Box 9035, 6800 ET Arnhem, The Netherlands

Accepted 20 November 1998

Key words: Perna viridis, flow velocity, growth rate, larval occurrence, spat settlement, spawning periods

Abstract Green Perna viridis were observed to be a major foulant in the seawater intake tunnel of a coastal power station. Field experiments were carried out to ascertain what factors were responsible for the successful colonisation by mussels. Two adjacent stations (25 m apart) were selected, one representing the coastal waters and the other representing the intake screens (with higher water velocity). Gonadal activity, larval abundance, spat settlement and growth rate of the mussels were monitored at monthly intervals for a total period of two years. The results showed that the breeding activity of the mussels at the study area is influenced largely by temporal distribution of seawater temperature. However, ensuing larval availability in the coastal waters is more dependent on food availability. On the other hand, spat settlement and growth rate are predominantly influenced by water flow, probably as a result of increased propagule and food flux rate at higher water velocities. Higher water velocity at the intake screens also contributed to mussel dominance by preventing settlement of many potential competitors.

Introduction ing seawater (Rajagopal et al., 1997). On an earlier appraisal (Rajagopal et al., 1991), it was found that Green mussels, Perna viridis are widely distributed out of 570 tons of fouling debris lodged inside the in the Indo-Pacific region; their distribution extends concrete intake tunnel of a power station, P. viridis from Japan to New Guinea and from the Persian Gulf alone constituted 411 tons. Since this was the first time to South Pacific Islands (Siddall, 1980). They are such massive colonisation of marine mussels has been a characteristic species of midlittoral and sublittoral observed in the cooling circuits of an Indian power zones where they often constitute dense populations station, we were interested to know what aspects of on rocky substrata. In spite of their wide distribu- the ecology of the mussels make them such successful tion and their importance in the ecology of rocky colonisers. This was important as earlier workers who shore ecosystems, detailed works on their biology are studied fouling phenomena on the east coast had not only a few (Lee, 1985). These mussels are also im- indicated the dominance of P. viridis among the nat- portant from the point of view of protein for ural sessile communities (Paul, 1942; Daniel, 1954; human consumption and some aspects of their biol- Renganathan et al., 1982; Rao, 1990). Moreover, in- ogy relevant to fishery and culture have, therefore, formation regarding the breeding activity of P. viridis been studied by other workers (Qasim et al., 1977; from different localities of the Indian peninsula was Sivalingam, 1977; Parulekar et al., 1982; Rivonkar inconsistent. Larval availability and growth rate are et al., 1993; Rajagopal et al., 1998). However, these important parameters influencing successful colonisa- mussels also deserve serious attention on account of tion by sessile species. Earlier workers had indicated their potential to foul industrial cooling systems us- the importance of water flow on the population ecol- 314

Figure 1. (a) Map showing the Kalpakkam. (b) Schematic represen- tation of the Madras Atomic Power Station seawater intake tunnel showing 2 sampling stations (not drawn to scale). ogy of mussels (Nixon et al., 1971; Perkins, 1974; Venugopalan et al., 1991; Wildish & Kristmanson, Figure 2. Seasonal variations in the hydrographic parameters ((a) 1997). It was possible that greater water flow ex- temperature, (b) salinity, (c) dissolved oxygen and (d) chloro- perienced within the cooling water circuit could be phyll-a) in Kalpakkam coastal waters from April 1988 to March responsible for the successful colonisation of mus- 1990. Data are presented as mean  SD. sels. Bearing this in mind, the population ecology of P. viridis was monitored at two locations which repre- Materials and methods sented (a) their natural habitat (coastal waters) and (b) cooling intake point of the power station experienc- Site description ing high water velocity. The present study investigates whether flow regimes are significant in influencing the Kalpakkam is situated (12◦320 N and 80◦110 E) about population ecology viz., growth rate, breeding activity 65 km south of Madras (Figure 1a). Madras Atomic and spat settlement of P. viridis in coastal waters of Power Station (MAPS), Kalpakkam is a seawater Kalpakkam, east coast of India. cooled station, and uses a 468 m long sub-seabed tun- nel to draw cooling water (35 m3 s−1) for its twin (2 × 235 MWe) reactors (for details refer Rajagopal, 315

1997). The seawater flows by gravity from the intake Larval abundance (Figure 1b) via the tunnel to the forebay pump house, from where it is pumped (12 pumps) to the condensers. Mussel larvae were concentrated from 500 l of sea- The coolant seawater flow in the tunnel when all the water using a 22 µm mesh net (De Wolf, 1973), 12 pumps are running, works out to be about 3 m s−1 every month from May 1988 to May 1990. The larvae (Madras Atomic Power Station Design Manual, 1975). were subsequently fixed in 5% buffered formalin and The intake point is guarded by steel weld mesh screens counted in a Sedgwick rafter counter. to prevent the entry of large objects into the cooling circuit. Spat settlement × × Sampling stations Concrete blocks (20 20 20 cm) were used to sam- ple spat fall in coastal waters (Sta 1), as described by Two stations were selected for the study (Figure 1b). Nair et al. (1988) and Rajagopal et al. (1997). Three Station 1 represents the coastal waters which is 8 m test blocks were suspended at 1 m, 4 m and 7 m using deep and experiences coastal currents of velocity in nylon ropes and retrieved after 30 d to estimate spat the order of 0.2–0.3 m s−1. Station 2 is the seawater fall. At Sta 2, spat samples were collected from the intake point which is characterised by high water ve- steel intake screens at 2 m, 4 m and 6 m. Earlier tri- locity (as high as 3 m s−1, depending on the flow). als had shown that mussel settlement on steel surfaces The distance between Sta 1 and Sta 2 is about 25 m. were comparable to those on concrete. The samples The physicochemical characteristics of the water are, (in triplicate) were collected at each depth, and the −2 therefore, identical at both stations, except for water data were averaged and presented as numbers dm 2 2 velocity. (dm = 100 cm ).

Hydrographical features Growth rate

Hydrographical features of the study site were studied Growth rate measurements were initiated by suspend- by collecting surface water samples at fortnightly in- ing test blocks at 1 m (Sta 1) at the beginning of spat tervals during the period April 1988 to March 1990. settlement (April 1988). Every month about 30 mus- Parameters like temperature, salinity, dissolved oxy- sels were randomly collected from the concrete blocks gen (DO) and chlorophyll-a were monitored (Strick- (1 m depth at Sta 1) and from the intake screens (2 m land & Parsons, 1972) to understand their variation depth at Sta 2). Collection of mussels from test blocks and possible influence on the breeding pattern and involved sampling of a different subset of the mus- growth rate of the mussels. sel population every month. In order to monitor the growth increment of the same population over a period Gonad observations of time, mussels (11  0.6 mm shell length, n = ca. 100) were confined in cages (75 × 75 × 75 cm, 0.5 cm Mussels were collected every month (April 1988 to mesh size) and left suspended at 1 m depth at Sta 1 March 1990) from the two stations and were used for 375 d (Page & Hubbard, 1987). Their shell growth for gonadal studies. About 60–65 mussels (approx. increment was monitored at monthly intervals during 30–40 mm shell length) were collected from each the period October 1988 to September 1989. station. In the laboratory, the gonadal tissues were removed from the mantle lobes and fixed in Bouin’s Statistical analysis fluid for 24 h and later transferred to 40% alcohol. Sections (10–15 µm) were made from wax-embedded A 2-factor analysis of variance (ANOVA) was used to tissues and stained with haematoxylin and eosin. The examine variability in gonad index and spat settlement method of Seed (1969) was adopted to categorise of P. viridis taking account of season (sampling time) the gonads into four groups viz., spent/resting, de- and station as two independent variables (Sokal & veloping/redeveloping, ripe and spawning. Gonad in- Rohlf, 1981). Spat settlement of P. viridis at different dex (GI) was also determined based on the method depths was tested by 1-factor ANOVA. For post-hoc described by King et al. (1989). comparison of monthly means, we used student t-tests for comparison of two means and Student-Neuman- Keuls (SNK) tests for comparison of multiple means 316

(Zar, 1984). Prior to the analysis the data were tested with spawning and GI data, with two peaks in a year, for normality and homogeneity of variance. viz., April–June and October–November. The second peak was much lower and occurred during a shorter period when compared to the first. Results The spat fall also showed close correspondence with larval availability, with two peaks per annum Hydrographical features (Figure 6). The October peak, as in the case of lar- val abundance, was much smaller when compared to Surface water temperature ranged from 25.9 ◦C(De- the May-June peak. Settlement of P. viridis varied sig- cember 1989) to 31.3 ◦C (October 1989) during the nificantly with respect to season (ANOVA, df = 23, study period (Figure 2a). It was characterised by two F = 99.813, P < 0.001) and station (ANOVA, df = well defined maxima, one occurring during May/June 1, F = 128.886, P < 0.001, Table 1). P. viridis settle- (30.9 ◦C) and the other in October (31.3 ◦C). Salin- ment was considerably higher in 1988 when compared ity ranged from 27.0% to 35.5%, with a maximum to 1989. The data also showed markedly higher spat in May/June and a minimum in November (Fig- settlement at Sta 2, as compared to Sta 1. The max- ure 2b). Dissolved oxygen of surface water varied imum spat fall recorded was 5224 numbers dm−2 at from 4.19 mg l−1 (June 1989) to 6.24 mg l−1 (Septem- Sta 2, in May 1988. Depth-wise differences in settle- ber 1988) (Figure 2c). A definite pattern of seasonal ment were negligible (ANOVA, df = 2, F = 0.332, P change in dissolved oxygen concentrations was not = 0.72) at the intake point (Table 2), whereas at Sta 1, discernible. Chlorophyll-a ranged from 1.06 mg m−3 settlement was maximum at 4 m, followed by 1 m and to 9.99 mg m−3 (Figure 2d). Maxima were found least at 7 m (ANOVA, df = 2, F = 8.966, P < 0.001). in May and minima in November. The chlorophyll values peaked during May–June months, indicating Growth rate greater availability of in the coastal wa- ters. However, November–December months saw a Significant differences in growth rate were found be- general decrease in chlorophyll values; there was no tween Sta 1 and Sta 2 (ANOVA, df = 1, F = 5.271, chlorophyll increase corresponding with the second P < 0.05, Figure 7). At Sta 1 mussels grew at the rate temperature peak observed in October. of 13  0.5mmin30dupto98 0.7 mm in 370 d. At the same time, mussels growing at Sta 2 exhibited Spawning, larval abundance and spat settlement maximum growth of 27  1.1mmin49dupto119 Histological data showed that spawning of P. viridis 2.1 mm in 375 d. The difference in size of the mussels at Kalpakkam started by March and peaked in May at the end of the period at the two stations was signif- (Figure 3). Extensive spawning during this period was icant (t-tests, P < 0.001). A statistical comparison of indicated by a large proportion of spawning mussels the cage data (11 mm size group) with test block data, in May and presence of spent gonads in June and July indicated that at the end of one year the size of caged samples. The latter also corresponds with a decrease mussels was not significantly different from that of test in GI in July (Figure 3). The GI values increased in block mussels (t-tests, P > 0.05). August and September, due to the large proportion of redeveloping gonads. The second spawning sea- son peaked around October and was followed by a Discussion short cessation of spawning activity in the population. Gonad index was positively correlated with the tem- Prior to our studies on the massive colonisation of the perature (Sta 1: y =−839.1 + 34.4x, r2 = 0.82, P seawater intake system of MAPS (Rajagopal et al., < 0.001; Sta 2: y =−1100.2 + 43.4x, r2 = 0.90, 1991), there are no published reports of large-scale P < 0.001, Figure 4). A comparison of GI did not fouling by P. viridis in cooling water circuits of the show any significant difference between Sta 1 and Sta tropical Indo-Pacific. Huang et al. (1983) have re- 2 (ANOVA, df = 1, F = 2.787, P = 0.10, Table 1). ported P. viridis to be an important fouler of ship hulls, Larval abundance in the coastal water fluctuated piers, buoys and rafts in Hong Kong waters (see also widely during the study period (Figure 5). The max- Lee, 1985; Cheung, 1993). Most of the earlier stud- imum (39532 larvae m−3) was recorded in May 1988. ies on P. viridis from Indian waters (Rao et al., 1975; The data, in general, showed good correspondence Qasim et al., 1977; Narasimhan, 1980; Parulekar et al., 317

Table 1. Results of ANOVA testing whether gonad index and spat settlement of the green mussel, Perna viridis were different at Sta 1 (coastal waters) and Sta 2 (intake screens) during April 1988 to March 1990

Source of variation df SS MS F P

Gonad index Station 1 173.34 173.34 2.78 0.102 Time 23 467003.99 20304.52 326.45 0.001 Station × Time 23 16551.91 719.65 1.57 0.001 Error 48 2985.50 62.20

Spat settlement Station 1 5134000.69 5134000.69 128.89 0.001 Time 23 91446540.64 3975936.55 99.81 0.001 Station × Time 23 23705459.97 1030672.17 25.87 0.001 Error 96 3824044.67 39833.80

Figure 3. Seasonal variations of gonadal maturity stages (%) and gonadal index of Perna viridis in coastal waters and intake screens of power station in Kalpakkam.

1982; Rajagopal et al., 1998) have been related to the are relevant to its potential to colonise cooling water fishery aspects. This necessitated a study on important circuits. aspects of the population ecology of P. viridis,which 318

Cheung (1993), working on the population dynam- ics of P. viridis in the Tolo Harbour, Hong Kong, reported two recruitment periods per year: one from July to September and another from November to March. Lee (1985), who worked in the Victoria Har- bour (Hong Kong) population, reported a single re- cruitment period for P. viridis which extended from June to September. Our data, which includes gonadal observations (Figure 3), larval abundance (Figure 5) and spat settlement (Figure 6), clearly indicate two recruitment periods for P. viridis at Kalpakkam. The first one extends from April to June and the second Figure 4. The relationship between the gonad index of Perna viridis from September to October, the latter being less in- and water temperature in Kalpakkam coastal waters. tensite. A comparison of the present data with the Table 2. Data on spat settlement of Perna viridis at different depths data from other parts of the Indian coast (Figure 8) at Sta 1 and Sta 2 during April 1988 to March 1990. One-way indicate that breeding activity of this species could ANOVA followed by multiple comparison tests (SNK tests) were used vary substantially within narrow geographical regions, to determine whether depthwise spat settlement of mussels differed as observed in Hong Kong waters by Lee (1985 and significantly at Sta 1 and Sta 2 1988) and Cheung (1993). Many of the published lit- Coastal waters Intake screens erature regarding P. viridis reproductive behaviour on Depth Depth the east coast of India (refer Figure 8), are based on 1m 4m 7m 2m 4m 6m spat settlement data (Godwin, 1980; Karande et al., 1983; Nair et al., 1988), which may not give a correct Mean 314 517 68 641 601 687 picture regarding gonadal activity. Some of the nearby Maximum 1734 2486 529 5225 4512 4779 Minimum000000 areas (Edaiyur backwaters and Kovalam, Figure 1a) Median 37 95 14 138 120 150 experience hydrographic conditions (especially salin- SD 524 783 129 1172 1191 1258 ity) significantly different from those at Kalpakkam, SE 112 167 28 234 238 252 which is an open coast experiencing typical marine Lower 95% Cl 82 170 13 158 109 168 conditions for most part of the year. This could have Upper 95% Cl 546 865 127 1125 1092 1207 been a probable cause of the differences in reproduc- = = tive behaviour of P. viridis at these sites. In the case ANOVA F 8.966, P < 0.001 F 0.332, P > 0.05 of the Mytilus edulis (L.) Bayne and Wor- rall (1980) have also reported two spawning periods at Lynher and a single one at Cattewater in the UK. Obviously, local hydrographical conditions (includ- as an indicator of phytoplanktonic food availability, ing pollution levels) and food availability may act key shows only a single summer peak in April–June. A factors for a reproductive strategy (Lee, 1985). rise in water temperature in October is not associated Though the spawning activity of the mussels grow- with a phytoplankton bloom. We hypothesise that food ing at Sta 1 and Sta 2 exhibit two clear peaks per acts as a limiting factor for the growing larvae, result- annum, which are roughly comparable to each other in ing in low numbers of mussel larvae in the coastal terms of intensity, the ensuing larval concentration in waters following the second spawning in October. the water shows only one prominent peak, correspond- However, this would need confirmation by additional ing to the first spawning activity. A possible explana- experimentation. tion for this is as follows. The gonadal development The larval densities observed during the April– and spawning activity of P. viridis at Kalpakkam is June peak were comparable with data reported from linked with the water temperature which shows two elsewhere. The highest density recorded in the present clear peaks, one in April-June and another in Octo- study was 39 532 larvae m−3. Schram (1970) recorded − ber. Gonadal index matches with seasonal fluctuations a similar (40 000 larvae m 3) figure for M. edulis from of temperature (Figure 4). However, larval abundance the Oslofjord. Hopkins (1977) showed that lamelli- in the coastal waters is probably decided largely by branch larvae in Tampa Bay ranged from 1200 to − food availability. Chlorophyll-a, which is used here 15 500 larvae m 3, with an annual mean of 8000 319

Figure 5. Seasonal occurrence of mussel larvae in Kalpakkam coastal waters.

Figure 7. Growth rate of Perna viridis in coastal waters, intake screens of power station and experimental cages (initial shell length 11  0.6 mm, n = 100, suspended in coastal waters at 1 m depth) in Kalpakkam. Data are presented as mean  SD.

(Table 2). Maximum settlement was observed at Sta 2. The high settlement intensity on the intake screens (Sta 2) is explicable on account of the high flow rate, which would enhance the propagule flux rate to the substratum. Though the water velocity is high at this Figure 6. Monthly variations of mussel spat settlement at differ- station, mussel larvae are capable of settling at such ent depths in coastal waters and intake screens of power station in Kalpakkam. high water velocities (Neitzel et al., 1984; Rajagopal, 1997). Neitzel et al. (1984) reported that at veloci- tiesashighas3.5ms−1, mussels could settle and −3 larvae m . Fish and Johnson (1937) reported peak colonise new surfaces. Depth-related variation in in- − abundance of more than 25 000 larvae m 3 in the Bay tensity, which is obvious at Sta 1 is lacking at Sta 2. of Fundy. At Sta 1, the settling plantigrades clearly prefer the The present data indicate significant variations in intermediate depth (4 m), when compared to the near- the settlement intensity of P. viridis at the two stations 320

Figure 8. Breeding periodicity of green mussel, Perna viridis (L.) reported from Indian waters. Thick lines represent intense reproductive ∗ ∗∗ activity ( gonadal observations; spat settlement data). surface (1 m) (SNK tests, P < 0.05) or near-bottom (Narasimhan, 1980) and 96 mm from Goa on the west (SNK tests, P < 0.001). This behaviour is probably coast (Rao et al., 1975; Rivonker et al., 1993). We also due to the subtidal habitat of these mussels. Depth- observed that mussels kept confined in cages in the wise differences in spat fall are likely if the larvae coastal waters reached the same size as those on test are non-uniformly distributed in the water column or blocks after a period of one year growth (Figure 7). alternatively, the settling larvae prefer discrete light The increase in growth rate at Sta 2 is, probably due regimes. However, this depth-related feature was not to increased food flux rate caused by the high flow apparent at Sta 2, owing probably to the turbulent wa- rate. The overriding importance of food supply in mus- ter flow which would disturb any vertical distribution sel growth rate has been emphasised by Seed (1976), of larvae. Seed and Suchanek (1992) and Wildish and Kristman- An analysis of the data presented in Figure 9 shows son (1997). Other authors who studied growth rates that, apart from P. viridis, not many species were able of P. viridis include Lee (1985, 1986) and Cheung to colonise the intake screens, apparently due to the (1993). Lee (1986) recorded low (5 mm month−1) high velocity regime. The high velocity would permit growth rates in the polluted Victoria Harbour, Hong settlement of only those larval forms, such as mus- Kong. Similarly, Cheung (1993) reported a growth sels, which have the ability to withstand a high shear of 49.7 mm in one year from Tolo Harbour, another force (Neitzel et al., 1984). This would have increased polluted harbour in Hong Kong. When compared to mussel dominance at Sta 2 not only directly, but also values reported earlier (Vakily, 1989), the growth rate indirectly, by reducing competition. recorded at Sta 2, in comparison, stands apart as the In our study, a maximum growth size of 119  figure (10 mm month−1) is the highest ever reported 2.1 mm shell length was recorded in the first year for for P. viridis. P. viridis growing on the intake screens. This value is much higher than the values reported from elsewhere in India: 93 mm from Kakinada on the east coast 321

recorded at Sta 2 (high water velocity) is the highest ever reported for P. viridis.

Acknowledgements

We express our sincere thanks to S. V. Narasimhan and S. B. Kuppuraju for the facilities and support. Thanks are due to J. M. van Groenendael and B. Kelleher for suggestions. Thanks are also due to C. van der Rijt for his assistance with the statistics. This work was supported by a grant from the Board of Research in Nuclear Sciences, Department of Atomic Energy, Government of India.

References

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