NETHERLANDSJOURNALOFAQUATICECOLOGY30(4) 309-325 (1997)

SEASONALSETTLEMENTAND SUCCESSIONOF FOULING COMMUNITIES IN KALPAKKAM,EASTCOASTOF INDIA S. RAJAGOPAL1, K.V.K. NAIR2, G. VAN DER VELDE1 and H.A. JENNER3

KEYWORDS: macrofouling, seasonal settlement, community structure, substratum, competition, fouling biomass.

ABSTRACT Seasonal distribution and community succession of macrofoulants were studied using concrete panels in the coastal waters of Kalpakkam, east coast of India, for a period of two years. The panels were suspended at 1 m, 4 m and 7 m depths and categorised into short-term and long-term exposures. A high total of 105 fouling taxa were recorded. The major fouling organisms observed were hydroids, barnacles, mussels, anthozoans and ascidians. Considerable faunistic and biomass variations were noticed both with respect to season and depth. The month of panel exposure had a significant influence on the succession of fouling communities. On the short-term panels, the maximum fouling biomass was 64 kg m-2 in 30 days at 4 m depth, whereas on the long-term panels, it was 250 kg m-2 after 216 days at 4 m depth. A comparison with the biomass values reported from elsewhere shows that biomass build-up in Kalpakkam coastal waters is one of the highest ever reported. Such a very high biomass accumulation is due to the extremely dense settlement of mussels, especially the green mussel, Pema viridis (L.).

INTRODUCTION A review of the literature on settlement and colonisation of sedentary benthic fauna indicates that most of these studies have been prompted either by an academic interest in the ecological processes underlying the phenomenon, or by operational problems associated with some kind of maritime activity (WROI, 1952; OSMAN, 1978; RAJAGOPAL,1991; NANDAKUMAR,1996). Though the techniques used for a study of this nature are largely similar, being based on the exposure of test panels for known periods of time, the parameters which are studied might vary depending on the objectives of the researcher. Some workers were largely interested in the seasonal variations and ecological succession in the community and factors responsible for it (DAYTON,1971; CONNELLand SLATYER, 1977; SMEDES, 1984). Other workers showed interest in the changes occurring in the quality and the quantity of fouling over short 309

periods of time and correlated it with such factors as environmental parameters, larval availability, settlement preferences and other ecological processes (SUTHERLAND and KARLSON,1977; VENUGOPALAN, 1987; SMEOESand HURD,1981). Quantitative variations in biofouling are generally expressed in terms of biomass, percentage cover, numerical density and/or frequency of occurrence. LEWIS (1981) made a comparative study of these methods, and concluded that biomass and panel coverage were better indices of fouling development than either numerical density or frequency. The assemblage of fouling organisms on an exposed surface depends obviously on the species which are naturally present at a given site as well as their ability to attach and grow on that surface (RILLMAN, 1977). Although over 4000 species have been reported in the process of fouling (CRMSP, 1984), only a few species make up the potential problem-species of interest to power plant operators (RAJAGOPAL, 1997). The species of foulants

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RAJAGOPAL, NAIR, VAN DER VELDE and JENNER

Fig.1. a. Map showing the location of Kalpakkam and other study sites on Indian coasts. Figures in circles indicate the total number of fouling taxa reported in each location, b, Schematic representation of the Madras Atomic Power Station intake tunnel showing sampling location (MSL = Mean sea level).

Settlement and succession of fouling communities

and their settlement periods and biomass vary from power plant to power plant, and an understanding of these aspects is very important in order to develop an economic and safe antifouling measure. Therefore, several studies have been conducted in different sea areas in this context (RELINI, 1984; BRANKEVICRet aL, 1988). The present paper reports results of panel studies on the vertical distribution and biomass of macrofoulants with season and depth vis-a-vis environmental conditions in the Kalpakkam coastal waters, where seawater is used for condenser cooling in a nuclear power plant.

MATERIALS AND METHODS Study area The Madras Atomic Power Station (MAPS), at Kalpakkam, is situated (12~ 33'N and 80~ 11'E) about 65 km south of Madras on the east coast of India (Fig. la). Seawater for condenser cooling in the power plant (35 m3 s-l), is drawn through a sub-seabed tunnel which is located 53 m below mean sea level (MSL). The seawater cooling system consists of an intake structure (located 420 m away from the shore in the sea), tunnel (468 m long and 3.8 m in diameter) and fore-bay (Fig. l b). The tunnel connects the fore-bay and pump house to the intake structure. From the intake shaft, water flows by gravity into the fore-bay. At the fore-bay, 12 pumps draw and circulate the seawater through the condensers and other heat exchangers. The coolant flow, when all the 12 pumps are running, is about 3 m sec-1 (RAJAGOPAL,1991). The sampling station is located near the intake area of MAPS (Fig. lb). Water depth at this site is 8 m. For further details of the cooling circuits, see RAJAGOPALet al .(1991 ). Seasons at Kalpakkam can be conveniently classified into four (RAJAGOPAL,1991): South-West monsoon (July - September), North-East monsoon (October - December), Post monsoon (January March) and Summer (April - June). Hydrographic conditions Surface water samples were collected at fortnightly intervals from April 1988 to March 1990. Water temperature was measured to 0.1~ accuracy. Salinity was estimated by the Mohr Knudsen method and dissolved oxygen content was measured by Winkler's method (STR~CKLANOand PARSONS, 1972). Light penetration was measured with a Secchi disc, and seston by filtering over

311

Millipore filter paper of 0.45 pm porosity (STRICKLANDand PARSONS,1972). Dissolved nutrients (nitrite, nitrate, inorganic phosphate and reactive silicate) and chlorophyll-a were analysed following procedures outlined by PARSONSet aL (1984).

Panel studies Experimental concrete panels (20 x 20 x 20 cm) were suspended with nylon ropes at depths of 1 m, 4 m and 7 m in the Kalpakkam coastal waters. The panels were categorised into shortterm exposures (A-series) and long-term exposures (B and C-series). The short-term panels were suspended (two panels at each depth) and withdrawn at monthly intervals, and foulants collected from 100 cm2 to follow the pattern of their seasonal settlement. The 24 long-term panels (12 panels at each depth) of the B-series were all suspended together, but were withdrawn at the rate of two every 30 days and samples were collected as in the case of short-term panels, in order to study the succession of fouling communities. The Cseries panels (two panels at each depth) were suspended successively at 30 day intervals and retrieved together after one year with a view to study the relationship between the primary settlers and the climax community. Altogether 72 panels were collected in each year (3 series of 24 panels). Each panel was studied with regard to wet biomass, species composition and percentage coverage of the panels (visual estimation) by different foulants. RESULTS AND DISCUSSION Fouling organisms The total number of taxa involved in the process of fouling in Kalpakkam waters was found to be 105 (Table 1). A comparison between the present work and earlier research carried out at other localities along the Indian coast revealed that the fouling community in Bombay waters comprised 85 taxa (VENU6OPALAN,1987). On the west coast, 42 and 65 biofouling taxa have been recorded in the Goa (ANIL and WAGH,1988) and in the Cochin harbour (NAIR and NAIR, 1987), respectively. On the east coast, BALAJI (1988) has reported 121 taxa at Visakhapatnam harbour, whereas at Kakinada only 37 taxa have been recorded (RAO and BALAJI, 1988). Although a direct comparison of species diversity between different locations is not justified owing to the differences in the exposure methodology, substratum and level of

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Table 1. List of fouling organisms collected from test panels in the Kalpakkam coastal waters. Occasional visitors such as seaweeds,

Xanthidae, Portunidae, Grapsidae,Majidae, Alphididae, Hippolytidae, Palinuridaeand fishes are not included in the list. "*Some more species are to be identified. COELENTERATA Campanulariidae Obelia bidontata Clarke Obelia dichotoma (Linnaeus) Obelia geniculata (Linnaeus) Clytia gracilis (M Sars) Pennariidae Pennaria disticha Goldfuss Bougainvilliidae Bimeria vestita Wright Aiptasiidae Aiptasia sp. Sertulariidae Sertularia sp. Sagartiidae*" Sagartia sp. PORIFERA Callyspongiidae Callyspongia diffusa (Ridley) Tedaniidae Tedaniaanhelans (LieberkOhn) Mycalidae Mycale mytilorum Annandale ECTOPROCTA Bicellariidae** Bugula sp. Electridae Electra sp. Acanthodesia sp. Alderina arabianensis Menon & Nair Membraniporidae* ' Membranipora sp. ANNELIDA Nereidae" Perinereis sp. Platynereis sp. Pseudonereis sp. Nereis sp. Spionidae Polydora sp. Sabellidae Dasychone sp. Sabellestarte sp. Serpulidae Ficopomatus sp. Hydroides sp. Hydroides elegans (Haswell) Hydroides dirampha M6rch Hydroides uncinatus complex Hydroides cf. albiceps (Grube) Serpula vermicularis sensu auct. ARTHROPODA Pycnogonidae Pycnogonum indicum Sunder Raj Balanidae Megabalanus tintinnabulum (Linnaeus) Balanus amphitrite Darwin Balanus reticulatus Utonomi Balanus variegatus Darwin var. cirratus Harding

Chirona amaryllis Darwin var. euamaryllis Broch Chthamalus malayensis Pilsbry Talitridae Hyale honoluluensis Schellenberg Corophiidae Corophium madrasensis Nayar Corophium triaenonyx Stebbing Cerapus abditus Templeton Gammaridae** Mefita sp. Ampithoidae Paragrubia vorax Chevreux Ampeliscidae Ampelisca zamboangae Stebbing MOLLUSCA Patellidae Cellana rota rota (Gmelin) Trochidae Euchelus asper Gmelin Muricidae Thais bufo Lamarck Thais blanfordi (Melvill) Thais tissoti (Petit) Drupella rugosa (Born) Ranellidae Lampusia pileare (Linnaeus) Cymatium cingulatum Lamarck Architectonicidae Architectonica perspectiva (Linnaeus) Turritellidae Turritella duplicata (Linnaeus) Nassariidae Bullia melanoides (Deshayesin Belanger) Littorinidae Littoraria ( Littoraria) undulata (Gray) Potamididae Cerithidea ( Cerithideopsilla) cingulata (Gmelin) Cypraeidae Palmadusta gracilis (Gaskoin) Olividae Olivancillaria gibbosa (Born) Dorididae Oiscodoris concinna Alder & Hancock Oendrodorididae Ooriopsilla miniata Alder & Hancock Tergipedidae Caloria militaris Alder & Hancock Arcidae Arca avellana Lamarck 8arbatia fusca (Brogui~re) Cardiidae Acanthocardis caronata (Schroeter) Vepricardium coronatum (Spengler) Veneridae Timoclea arakana (G & H Nevill) Irus exoticus (Hanley) Paphia textile (Gmelin) Tellinidae Tellina angulata (Gmelin)

Settlement and succession of fouling communities

313

Table 1. (Continued)

Carditidae Beguina variegata Brugui~re Pholadidae Pholas orientalis Gmelin Ostreidae Crassostrea madrasensis Preston Saccostrea cucullata (Born) Pteriidae Pinctada anomioides Reeve Pinctada chemnitzi (Philippi) Pinctada margaritifera (Linnaeus) Chamidae Chama reflexa Reeve Chama lazarus Linnaeus Chama fragrum Reeve Pseudochama cristella Lamarck Mytilidae Pema viridis (Linnaeus) Perna indica Kuriakose & Nair Modiolus modiolus sensu auct. Modiolus undulata Dunker Brachidontes striatulus (Hanley) Modiolus metcalfei (Hanley) Modiolus philippinarum (Hanley) Musculus perfragilis (Dunker)

systematic identification, the number of species observed at Kalpakkam might possibly be one of the highest on panels exposed to seawater.

Hydrographical conditions The water temperature in the Kalpakkam coastal waters varied from 25.8~ (December 1989) to 31.7~ (October 1989) (Fig. 2). The temperature data were characterised by two welldefined maxima: one in May-June and the other in October. Similarly, two minima were also observed during July-August and December-January. Such a bimodal type of oscillation in water temperature has been reported to be a common phenomena for several of the warmer areas investigated in the regions around the Indian peninsula (RAJAGOPAL, 1991 ). The salinity values (Fig. 2) ranged from 24.8 (November 1989) to 35.7%o (June 1988). The seasonal distribution of surface salinity was, in general, characterised by a minimum in November following heavy rainfall. In contrast, relatively high salinity values were observed in the summer months (May-June). The dissolved oxygen values ranged from 3.38 to 6.63 mg 1-1 (Fig. 2), but did not indicate any clear seasonal pattern during the study period. The seston values ranged from 9.1 (Septem-

ECHINODERMATA Ophiuridae* * Ophiothrix exigua Lyman Amphioplus graveylii James Holothuriidae * * Ophiactis savignyi M~ller & Hancock Holothuria spinifera Theel UROCHORDATA Didemnidae Oidemnum psammathodes Sluiter Leptoclinum macdonaldi (Herdman) Lissoclinum fragile (Van Name) Polyclinidae Aplidium multiplicatum Sluiter Styelidae Symplegma brakenhielmi (Michaelson) Symplegma viride Herdman Styela bicolor Sluiter Botrylloides magnicoecum Hertmeyer Polycarpa sp. Ascidiidae Ascidia zara Oka Ascidiella aspersa (MLiller)

her 1988) to 59.7 mg 1-1 (April 1988). Relatively higher values were observed during summer and NE monsoon periods (see Fig. 2). The higher values during summer are probably due to higher phytoplankton productivity whereas those during NE monsoon are caused by land drainage (RAJAGOPAL,1991 ). The Secchi-disc values varied from 35 (November 1988) to 310 cm (September 1989). In general, the Secchi-disc values during NE monsoon were lowest when compared to other seasons (Fig. 2). Kalpakkam receives the bulk of the annual rainfall during the NE monsoon period (RAJAGOPAL, 1991), and the heavy inflow of turbid water following rains apparently results in poor light penetration. The nutrient concentrations (nitrite, nitrate, inorganic phosphate and reactive silicate) were generally higher during the NE monsoon and lower during the summer period (Fig. 2). The seasonal distribution of chlorophyll-a was characterised by relatively high values during summer months and ranged from 0.5 to 12.4 mg m-3 (Fig. 2). The high summer values were probably due to increased light intensity that, together with higher salinity and temperature, make the environment suitable for the production of phytoplankton. The lower concentration of chlorophyll-a during the NE monsoon period, inspite of increased availability

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(Fig. 3). However, settlement rates were relatively low at 7 m, where prominent peaks were seen during March-April and November. The settlement pattern of barnacles observed during this study shows similarities to previous studies conducted in the Kalpakkam coastal waters (GODWIN,1980; NArR Seasonal settlement on short-term (A-series) et aL, 1988; SASIKUMARet aL, 1989). It has been panels reported that settlement of some barnacles is inHydroids fluenced by illumination. BRANKEVICHet aL (1988) Hydroid settlement was found almost throughout the year at all depths (Fig. 3). In general, peak and SASIKUMAR et aL (1989) observed that barsettlement of hydroids was observed during NE nacles prefer illuminated areas. However, increased settlement of barnacles on darkened or shaded monsoon. Moreover, hydroids were particularly surfaces has been documented by DAHLEMet aL abundant at 7 m depth. Such preferential depthwise (1984) and VENUGOPALAN(1987). Data obtained in settlement of hydroids has also been reported by the present study showed more abundant settleHUGHES(1977) and BOERO(1984). The influence of ment of barnacles at 1 m and 4 m depths, which light on the settlement of hydroids is not well understood (BOERO,1984), although hydroid larvae receive reasonably good illumination as compared to 7 m (see Fig. 3). are generally known to be negatively phototrophic. Though this is the general behaviour, observations Green mussels Settlement of the green mussel, Perna viridis contrary to this have also been reported. For example, HUGHES(1977) demonstrated that light has was generally observed during April to November with peaks in May-June and October. However, no influence on the behaviour of the hydroid Nemertesia antennina (L.). As other fouling species, the second peak was shorter with lesser spat hydroids have been also found in the deepest settlement. The two peaks coincided with seasonal oceanic waters in absolute darkness (VERVOORT, temperature maxima at Kalpakkam (Fig. 2). Seasonal settlement of mussel spat observed 1966). Generally, they tend to avoid well-illuminated sites. The present observation, wherein greater during the present study showed some similarities settlement was found at 7 m, probably indicates to previous studies carried out on the east coast. In Madras harbour, PAUL (1942) recorded the a preference of some hydroid species for dimly settlement of this species during March to illuminated surfaces. At this point, it is worth November with a distinct peak during August mentioning that hydroids are an integral part of the fouling community residing inside the intake September. However, SELVARAJ(1984) reported tunnel under conditions of absolute darkness that P. viridis from Kovalam and Ennore, a little north of Kalpakkam, bred almost continuously with (RAJAGOPALet al., 1991). peaks in June and October. He also showed that, as Anthozoans in the present study, peak settlement coincided Anthozoans, also a prominent group among with relatively high temperatures at both sites. Hasfouling assemblages, were represented by Aiptasia sp. and Sagartia sp. on the A-series panels (Fig. BRENKO(1973) demonstrated a relationship between 3). Major settlement of anthozoans was observed the larval availability of mussels and their subsequent settlement in the northern Adriatic sea. P~Eduring October 1988, April-May 1989, and OctoberDecember 1989 at all depths. Settlement was less TERS et al. (1980) and NEWELLet aL (1982) opined that the availability of food resources may inor absent during SW monsoon and Post-monsoon periods. No settlement variation of anthozoans fluence spawning, larval abundance and settlement with depth was observed in Kalpakkam coastal of mussels. A correlation between spawning periodicity, availability of food resources and salinity waters. has been demonstrated by MYINTand TYLER(1982). Barnacles In the present study, settlement of mussels was Among the different fouling groups, barnacles represented by Megabalanus tintinnabulum, Ba- observed to be at its maximum during summer /anus reticulatus, B. amphitrite, B. variegatus var. when relatively high temperatures, salinity and cirratus, Chirona amaryllis var. euamaryllis and chlorophyll-a concentration prevailed. From these observations it is reasonable to conclude that Chthamalus malayensis were found to be the most dominant on A-series panels. Barnacle settlement temperature, salinity and food availability are major factors influencing the breeding and spawning was continuous with peaks during March-April, periodicity of mussels, as reported by SEED(1969). July-September and November at 1 m and 4 m

of nutrients, was probably due to low light penetration resulting from the turbidity of suspended silt as reported by earlier workers (see RAJAGOPAL, 1991).

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communities (RYLAND, 1976; JACKSON,1977; OSMAN, 1977). The pattern of fouling in the Kalpakkam coastal waters with respect to depth indicates certain interesting features. The most important constituent of Ascidians the fouling community, Le. green mussels, settled Ascidians are a very important group of fouat 4 m in greater abundance than at other depths ling organisms having a world-wide geographical (Fig. 3). Barnacles were observed in abundance at distribution (WHOI, 1952). It has been reported 1 m and to a lesser extent at 4 m. Hydroids and that in temperate waters only a single generation is bryozoans, on the other hand, were mostly found at established each year, but in tropical areas there 7 m. Ascidians were dominant in the surface waters. are two to four generations per year (GOOOBODY, Anthozoans and Modiolus spp., however, did not 1962; MILLER, 1974). MILLER (1958) reported that show any definite pattern in their distribution with the ascidian breeding season is restricted to a depth. It is reasonable to assume that the fouling short period in Scottish waters. On the other hand, community in Kalpakkam coastal waters, consisting GOODBOOY(1961) stated that ascidians bred contiof a wide variety of organisms (105 taxa), has evolnuously throughout the year in Kingston harbour, ved a strategy for colonisation of a surface by which Jamaica. Also in the present study, ascidians were interspecific competition is reduced to a great found to be continuous breeders, although settleextent by some kind of a vertical zonation. In this ment rates were found to be highest from February way, each of these groups which are mostly susto June (Fig. 3). It is interesting to note that pension feeders, creates an ecological niche for the settlement of ascidians was more frequent itself. at 1 m depth than at 4 m and 7 m. This difference is probably due to the photopositive behaviour of Fouling on long-term (B-series) panels ascidian tadpole larvae (GOOOBOOY,1961, 1962). In the Kalpakkam coastal waters, considerable Other fouling organisms settlement of green mussels, ascidians and barnaSettlement of bryozoans (Ectoprocta) was cles were first observed on the long-term panels generally confined to January - May. However, (B-series) exposed in April at 1 m and 4 m depth they seemed to have their peak settlement from (Fig. 4). During May to January, the mussel February to March, when the recruitment and community remained largely unaffected by the growth of other species were reduced considerably. other fouling organisms. Ascidians were absent in Furthermore, settlement was found to be relatively October and November and were again observed in high at 7 m as compared to the other depths. December. The absence of ascidians coincided with Such a depth preference in bryozoan settlement the onset of the NE monsoon period when low has also been observed earlier (SASIKUMAR et aL, salinities prevailed in the coastal waters (Fig. 2). 1989). It also has been experimentally demonFully developed ascidian colonies, especially of strated that larvae of most bryozoan species Symplegma brakenhielmi and Didemnum psamexhibit a change from photopositive to photomathodes, covered green mussels, barnacles and negative behaviour during the pre-swimming period other fouling organisms by the end of March and (RYLAND,1960). Settlement of sponges, polychaetes, formed a climax community along with green snails, brown mussels (Pema indica) and clams mussels at 1 m (Fig. 4). However, at 4 m, the was also occasionally noticed on the panels. domination by green mussels was total and formed Absence of macroalgae from the fouling coma climax community in March occupying >85% of munity at Kalpakkam may have been due to the panel surface (Fig. 4). At 7 m, mussels and competition for space, predation and grazing ascidians contributed to a coverage of <20% and (CARPENTER, 1990). In general, sessile plants and co-dominance with barnacles and hydroids was animals need to be firmly anchored to the subobserved. stratum for their growth. Studies have shown that An exposure strategy involving short-term certain fouling species (e.g. mussels and bar- panels is ideal for studying seasonal settlement nacles) are more successful spatial competitors, patterns in the fouling community. However, to and frequently overgrow or displace other fouling follow long-term changes or succession occurring species (RICHMOND and SEED, 1991). Therefore, within the community, the cumulative, long-term competition for space is often recognised as an panels (B-series) are more suitable. In an enviimportant organising force in many epifaunal ronment where the substratum is a limiting factor, Settlement of Modiolus spp. showed a maximum during August - September (Fig. 3) and was relatively low during October to March. Moreover, no depth-wise variation of settlement was observed.

Settlement and succession of fouling communities

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Fig. 5. Colonisation curves (number of taxa) on panels submerged in early summer at Kalpakkam (present data) along with reported values on colonisation curves (panels submerged in spring-early summer) of SCHOENERet aL (1978) from Thailand, Hawaii(averagesshown),Washington,Newfoundlandand Alaska(modifiedafterRICHMONDand SEED.1991). organisms colonising it employ a wide range of competitive strategies (SCHEER, 1945; SUTHERLAND and KARLSON, 1977; SMEDESand HURD, 1981; NANDAKUMAR, 1996). However, local factors may play very important roles, modifying the competitive capabilities of an organism so that a particular type of organism which may become dominant in a particular environment may not do so in a different environment. In the present study, data from the Kalpakkam coastal waters indicate that the fast growing and competitively superior green mussels establish a dominance on a panel surface such that most of the other fouling organisms are left with little space to settle. Competitively dominant species, such as mussels, are often successful due to their large body size, fast growth rate, extended longevity and prolonged larval life (RICHMONDand SEED, 1991). Ascidians, however, constitute a notable exception and are able to overgrow the mussels because of their peculiar growth characteristics.

Similar observations have also been made by OSMAN (1977), DEANand HURO (1980) and SMEDES(1984). Ascidians are capable of surviving a high degree of partial damage or mortality by virtue of their mode of growth. Moreover, many clonal organisms (e.g. ascidians) produce secondary substances which have anti-microbial and toxic or noxious properties (DYRYNDA, 1986). Ascidians are well known to employ high concentrations of vanadium or low pH bladder cells in the tunic as antifouling mechanisms (STOECKER,1978). Such an ability to produce secondary substances may result in superior competitive ability and defensive mechanisms against other fouling species (JACKSON,1977; DEAN, 1981). At 7 m depth, where green mussel colonisation is found to be relatively low, opportunistic species such as barnacles and hydroids become the dominant species. Species colonisation curves on panels over a period of 12 months, are given in Fig. 5, along with

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RAJAGOPAL, NAIR, VAN OER VELDE and JENNER

Fig. 6. Seasonal variations in succession pattern (% coverage) on long-term C-series panels at three different depths in Kalpakkam coastal waters from April 1988 to March 1989.

reported literature values from areas at different latitudes (SCROENERet aL, 1978; RICHMONDand SEED, 1991). AS expected, the diversity of fouling assemblades is higher in the tropics (i.e. present study) when compared to temperate waters (i.e. higher latitudes). Frequent short-term changes in the hydrographical conditions of temperate waters have been reported to induce discontinuous settlement (WROI, 1952). However, the tropical marine environment is less cyclical and recruitment occurs at a more or less constant level resulting in the continuous accumulation of fouling organisms. The most obvious difference was in the initial colonisation rates of different species on the experimental panels (Fig. 5). In temperate zones, a slow and continuous increase in the number of species was observed. In contrast, the number of taxa after exposure increased more rapidly in the tropics for three months, but there after, the number of taxa decreased and fluctuated.

Fouling on long-term C-series panels Data on the mode of fouling succession on C-series panels in different periods are given in Fig. 6. The dominant community was found to be different on panels immersed during different months. Green mussels emerged as the dominant species on panels immersed in April whereas panels immersed in July were dominated by barnacles and Modiolus spp. (Fig. 6). Panels immersed in October and January showed a co-

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Settlementand successionof foulingcommunities

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dominance of barnacles, hydroids and to some extent green mussels. Depth-dependent variation was also observed as in the case of A-series and B-series panels. The time of panel initiation and the duration of panel exposure has been reported to be important in determining the composition, succession, and/or development of the fouling community (DAYTON, 1971; BEAN, 1981; NANDAKUMAR, 1996). OSMAN (1977), SUTHERLAND and KARLSON (1977), DEAN and HURD (1980) and SMEDES(1984) demonstrated the importance of initial colonisers on subsequent community development. In the present study, the significance of colonisation by mussels on the subsequent development of the fouling community is well illustrated by the data from the C-series

panels. Since peak settlement of the mussels occurred in April - June, any panel initiated during this period, as well as one or two months immediately proceeding it, showed mussels as the dominant community by the end of the year. On the contrary, panels initiated during July, October and January, ultimately ended up with the co-dominance by barnacles, Modiolus spp. and hydroids. Fouling biomass Seasonal biomass (wet weight) values in Aseries were characterised by relatively high values during summer (May and June) at all depths (Fig. 7). A maximum biomass value of 64.2 kg m-2 was recorded at 4 m depth. A secondary maximum

322

RAJAGOPAL, NAIR, VAN DER VELDE and JENNER

Table 2. Biomass production (maximum biomass recorded) of fouling organisms (wet weight) on different substrates reported from various temperate and tropical waters of the world. Depth (m)

Substratum

Biomass

Unit

Reference

2

Concrete Wood Asbestos Asbestos PVC

13.2 25.0 13.0 64.0 28.0 112.9 76.0 5.1 16.0 38.3

kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2

2

PVC

133.2

kg m-2 yr-1

RAJAGOPALetaL, 1995

2

PVC

8.3

kg m-2 yr-1

RAJAGOPALetal., 1995

2

PVC

11.5

kg m-2 yr -1

RAJAGOPALetaL, 1995

2

PVC

0.3

kg m-2 yr-1

RAJAGOPALetaL, 1995

kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2 kg m-2

HUANGand MAK,1980 HUANGand MAK,1980 HUANGand MAK, 1980 RENGANATHANetaL, 1982 KARANBEetal., 1983 SANTHAKUMARAN, et aL (unpubl.) RAVINBRAN and PILLAI,1984 RAVlNDRAN and PILLAI,1984 RAVINDRAN and PILLAI,1984 DE, 1984 DE, 1984 DE, 1984 OE, 1984 SELVARAJ,1984 SAWANT.1985 SAWANT,1985 VENU(3OPALAN,1987 VENU6OPALAN,1987 VENUGOPALAN,1987 VENUGOPALAN,1987 NAIR etal.. 1988 RAOand BALAJI,1988 RAOand BALAJI,1988 SASIKUMARetaL, 1989 RAJAGOPALetal., 1990 RAO,1990 RAJAGOPAL,1991 RAJAGOPAL,1991 RAJAGOPAL,1991 RAJAGOPAL,1991 RAJAGOPAL,1991 Presentstudy Presentstudy Presentstudy

Temperate waters Norfolk, Virginia, USA San Diego, California, USA Maine coast, USA Lynn, Massachusetts, USA Virginia, USA Palermo harbour, Sicily, Italy Trondheim, Norway Tyrrhenian sea, Italy Liguria, Italy Noordzeekanaal, The Netherlands Velsen power station intake, The Netherlands Velsen power station outfall, The Netherlands Hemweg power station intake, The Netherlands Hemweg power station outfall, The Netherlands

yr-1 yr-1 yr-1 yr -1 yr-1 (2 month) -1 (1 month) -1 yr-1 yr-1 yr-1

WHARTON.1942 WHEDON,1943 WHOI, 1952 WHOI, 1952 WHOI, 1952 RIGGIO,1979 SANTHAKUMARAN etaL (unpubl.) RELINI,1984 RELINI.1984 RAJAGOPALetal., 1995

Tropical waters Sam Mun Jai, Hong Kong 1.1 WU Kwai Sha, Hong Kong 1.5 Ping Chau, Hong Kong 1.5 Tuticorin bay, India 1 Kalpakkam coast, India 1 Madras harbour, India Cochin harbour, India 1 Cochin harbour, India 1 Cochin harbour, India 1 Kalpakkam coast, India Andaman, India Bombay offshore, India Bombay enclosed waters, India Ennore, Bay of Bengal, India 1 Mandovi estuary, Arabian sea, India 3 Zuari estuary, Arabian sea, India 4.5 Bombay high, India 2 Bombay high, India 62 Bombay high, India 2 Bombay high, India 62 Kalpakkam coast, India 1 Kakinada port, Bay of Bengal, India Kakinada port, Bay of Bengal, India 1 Kalpakkam coast, India 1 Edaiyur backwaters, Bay of Bengal, India 1 Visakhapatnam harbour, India MAPS intake gates, Kalpakkam, India 2 MAPS intake gates, Kalpakkam, India 4 MAPS intake gates, Kalpakkam, India 6 MAPS fore-bay, Kalpakkam, India 1 Edaiyur backwaters, India 1 Kalpakkam coastal waters, India 1 Kalpakkam coastal waters, India 4 Kalpakkam coastal waters, India 7

Concrete pier Concrete pier Concrete pier Alominium Wood Aluminium Stainless steel Carbon steel Tiles Mild Steel Mild steel Mild steel Mild steel Aluminium Aluminium Wood Wood Glass Wood Wood Mild steel Mild steel Mild steel Concrete Concrete Concrete Concrete Concrete

51.0 15.9 25.9 5.0 4.5 50.0 21.6 20.7 16.0 8.0 7.5 5.5 0.2 69.3 3.9 5.6 15.1 0.8 8.7 1.4 13.5 23.4 9.2 19.3 10.3 77.6 269.2 259.2 242.8 28.2 32.7 200.6 249.9 83.7

yr-1 (1 month) -1 yr-1 (6 month) -1 (6 month) -1 (6 month) -1 yr -1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr-1 yr -1

Settlement and succession of fouling communities was also recorded at the same depth in October 1988 (37.7 kg m-2). The maximum biomass observed in May - June was largely due to heavy settlement of the green mussels, P. viridis, the barnacle, Megabalanus tintinnabulum, and the ascidians Didemnum psammathodes and Aplidium multiplicatum. The period November to February was characterised by relatively low biomass at all depths. The lowest biomass of 7.4 kg m-2 (November, 1988) was observed at 7 m depth, and coincided with the lowering of salinity as a result of heavy rainfall during NE monsoon (see Fig. 2). Fouling biomass of B-series panels was generally characterised by two maxima at both 1 m and 4 m depths (Fig. 7). At 1 m, the first maximum was observed in July after 122 days (188 kg m-2) and the second in October after 216 days (201 kg m-2). At 4 m depth, the first maximum was recorded in October after 216 days (250 kg m-2) and the second in February after 340 days (237 kg m-2). However, at 7 m biomass did not show any definite seasonal pattern and a maximum value of 84 kg m-2 was observed in June after 92 days. At all depths, the total weight of fouling organisms was often dominated by the green mussel, P. viridis (Fig. 8). The weight of P. viridis over the period of one year was strongly correlated with the total weight of fouling organisms (r = 0.96, P
323

the literature with those obtained during the present study shows that biomass build-up in Kalpakkam coastal waters was the highest. A biomass value of 113 kg m-2 over a period of 2 months has been recorded by aIGGlO (1979) in Palermo harbour, Sicily. The maximum value reported from other Indian coastal waters is 78 kg m-2 at Visakhapatnam harbour (RAO, 1990). In the present study, the high record was 250 kg m-2 after 216 days at a depth of 4 m. The very high values at all depths were due to the extremely dense settlement of the green mussel, P. viridis. ACKNOWLEDGEMENTS We are grateful to the Board of Research in Nuclear Sciences, Department of Atomic Energy, Government of India for the facilities. We are thankful to Dr. P.N. Moorthy, Dr. P.K. Mathur and Prof. J. Azariah for their support. The authors sincerely thank Dr. S. Subba Rao (ZSI, Calcutta) and Dr. K. Satyanarayana Rao (CMFRI, Madras) for identification of various fouling groups. We are also thankful to Prof. Dr. W. Vervoort (hydroids), Dr. H. Ten Hove (polychaetes), Prof. Dr. L.B. Holthuis (crustaceans) and Jeroen Goud (molluscs) for updating the species names. Thanks are due to B. Kelleher for critically reading through the manuscript.

REFERENCES ANIL, A.C. and A.B. WAGH, 1988. Aspects of biofouling community development in the Zuary estuary, Goa, India. In: M.P. Thompson, R. Sarojini and R. Nagabhushanam (Eds.), Marine biodeterioration: advanced technique applicable to the Indian ocean. Oxford & IBH publishing (P) Ltd, New Delhi, p. 529-537. BALAJh M., 1988. Investigations on biofouling at two ports in Andhra Pradesh, India and some aspects of toxicity of copper to the fouling bivalve Mytilopsis sallei (Recluz). Ph.D. thesis, Andhra University, India, 1-209 pp. BOERO, F., 1984. The ecology of marine hydroids and effects of environmental factors: a review. Mar. Ecol., 5: 93-118. BRANKEVICH, G., R BASTIDA and C. LEMMI, 1988. A comparative study of biofouling settlements in different sections of Necochea power plant (Quequen port, Argentina). Biofouling, 1: 113-135. CARPENTER, R.C., 1990. Competition among marine macroalgae: a physiological perspective. J. Phycol., 26: 8-12. CONNELL, J.H. and R.O. SLATYER, 1977. Mechanisms of succession in natural communities and their role in community stability and organization. Am. Nat., 111: 1119-1144, CRISP, D.J., 1984. Overview of research on marine invertebrate larvae, 1940-1980. In: J.D. Costlow and R.C. Tipper (Eds.), Marine biodeterioration: an interdisciplinary study. Naval Institute Press, Annapolis, Maryland, p. 103-126. DAHLEM, C., P.J. MORAN and T.R. BRANT, 1984. Larval settlement of marine sessile invertebrates on surfaces of different colour and position. Ocean Sci. Engi., 9: 225-236. DAYTON, P.K., 1971. Competition, disturbance and community organization: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr., 41: 351-389. DE, K.P., 1984. Present state of technology for control of marine corrosion and fouling in tropical Indian waters. In: Proceedings of International Congress on Marine Corrosion and Fouling, Athens, p. 497-509. DEAN, T.A., 1981. Structural aspects of sessile invertebrates as organising forces in an estuarine fouling community. J. Exp. Mar. Biol. Ecol., 53: 163-180.

324

RAJAGOPAL, NAIR, VAN DER VELDE and JENNER

DEAN, T.A. and L.E. HURD, 1980. Development in an estuarine fouling community: the influence of earlier colonists on later arrivals. Oecologia, 46: 295-301. DYRYNDA, P.E.J., 1986. Defensive strategies of modular organisms. Phil. Trans. R. Soc. Lond., 313: 227-243. GODWIN, W., 1980~ Ecology of the coastal fauna around Madras Atomic Power Plant, Kalpakkam. Ph.D. thesis, University of Madras, India, 186 pp. GOOOBODY, I., 1961. Continuous breeding in three species of tropical ascidian. Proc. Zool. Soc. London, 136: 403-409. GOOOBODY, I., 1962. The biology of Ascidia nigra (Savigny). 1. Survival and mortality in an adult population. Biol. Bull., 122: 40-51. HILLMAN, R.E., 1977. Techniques for monitoring reproduction and growth of fouling organisms at power plant intakes. In: L.D. Jensen (Ed.), 8iofouling control procedures: technology and ecological effects. Marcel Dekker Inc., New York, p. 1-5. HRS-BRENKO, M., 1973. The study of mussel larvae and their settlement in the Vela Draga Bay (Pula: The Northern Adriatic Sea). Aquaculture, 2: 173-182. HUANG, Z.G. and P.M.S. MAK, 1980. Studies on biofouling in Tolo harbour. In: 8.S. Morton and C.K. Tseng (Eds.), The marine flora and fauna of Hong Kong and Southern China. Hong Kong University Press, Hong Kong, p. 767-787. HUGHES, R., 1977. Aspects of the biology and life history of Nemertesia antennina (L.) (Hydrozoa : Plumulariidae). J. Mar. Biol. Assoc. U.K., 57: 641-657. JACKSON, J.B.C., 1977. Competition on marine hard substrata: the adaptive significance of solitary and colonial strategies. Am. Nat., 111: 743-767. KARANDE, A.A., A.K. SRIRAMAN and R. VISWANATHAN, 1983. Marine biofouling in seawater tunnel. Technical Report, NCML/BARC, Bombay, 1-24 pp. LEWIS, J.A., 1981. A comparison of possible methods for marine fouling assessment during raft trials. Technical report, MRL- R-808, Material Research Laboratory, Department of Defence,Australia. MILLER, R.H., t958. The breeding season of some littoral ascidians in Scottish waters. J. Mar. Biol. Assoc. U.K., 37: 649-652. MILLER, R.H., 1974. A note on the breeding season of three ascidians on coral reefs at Galeta in the Caribean sea. Mar. Biol., 28: 127-129. MYINT, UM. and P.A. TYLER, 1982. Effects of temperature, nutritive and metal stressors on the reproductive biology of Mytilus edulis. Mar. Biol., 67: 209-223. NAIR, K.V.K., P. MURUGANand M.S. ESWARAN, 1988. Macrofoulants in Kalpakkam coastal waters, east coast of India. Indian J. Mar. Sci, 17: 341-343. NAIR, N.U. and N.B. NAIR, 1987. Marine biofouling dynamics in and around the Cochin harbour. In: Proceedings of the national seminar on estuarine management, Trivandrum, India. NANDAKUMAR, K., 1996. Importance of timing of panel exposure on the competitive outcome and succession of sessile organisms. Mar. Ecol. Prog. Ser., 131: 191-203. NEWELL, R.I.E., T.J. HILBISH, R.K. KOEHN and C.J. NEWELL, 1982. Temporal variation in the reproduction cycle of Mytilus edulis L. (8ivalvia, Mytilidae) from localities on the east coast of the United States. Biol. Bull., 162: 299-310. OSMAN, R.W., 1977. The settlement and development of a marine epifaunal community. Ecol. Monogr., 47: 37-63. OSMAN, R.W., 1978. The influence of seasonality and stability on the species equilibrium. Ecology, 59: 383-399. PARSONS, T.R., M. YOSHIAKI and C.M. LAW, 1984. A manual of chemical and biological methods for seawater analysis. Pergamon press, Oxford, p. 1-173. PAUL, M.D., 1942. Studies on the growth and breeding of certain sedentary organisms in the Madras harbour. Proc. Indian Acad. Sci., 150: 1-42. PIETERS, H., J.H. KLUYTMANS, D.I. ZANDEE and G.C. CADI~E,1980. Tissue composition and reproduction of Mytilus edulis in relation to food availability. Neth. J. Sea Res., 14: 349-36t. RAJAGOPAL S., 1991. 8iofouling problems in the condenser cooling circuit of a power station with special reference to green mussel, Pema wTidis (L.). Ph.D. Thesis, University of Madras, india, t 13 pp. RAJAGOPAL S., 1997. The ecology of tropical marine mussels and their control in industrial cooling water systems. Ph.D. Thesis, University of Nijmegen, The Netherlands, 184 pp. RAJAGOPAL S., J. AZARIAH and K.V.K. NAIR, 1990. Ecology of fouling organisms in Edaiyur backwaters, Kalpakkam. Mahasagar, 23: 29-41. RAJAGOPAL S., K.VK NAIR, J. AZARIAH, G. VAN DER VELDE and H.A. JENNER, 1996. Chlorination and mussel control in the cooling conduits of a coastal power station. Mar. Environ. Res., 41: 201-221. RAJAGOPAL S., N. SASIKUMAR, J. AZARIAH and K.V.K. NAIR, 1991. Some observations on biofouling in the cooling water conduits of a coastal power plant. Biofouling, 3: 311-324. RAJAGOPAL S., G. VAN DER VELDE and H.A. JENNER, 1995. Biology and control of brackish water mussel, Mytilopsis leucophaeta in the Velsen and Hemweg power stations, The Netherlands. Part I. Biology and behavioural response. Report No. 64211-KES 953109, KEMA Environmental Services, Arnhem, The Netherlands, 55 pp. RAO, K.S., 1990. Macrofouling on the east coast of India - some observations. In: K.V.K. Nair and V.P. Venugopalan (Eds.), Marine biofouling and power plants. Bhabha Atomic ResearchCentre, Bombay, p. 35-66. RAO, K.S. and M.BALAJI, 1988. Biological fouling at port Kakinada, Godavari estuary, India. In: M.F. Thompson, R. Sarojini and R. Nagabhushanam (Eds.), Marine biodeterioration - advanced technique applicable to the Indian ocean. Oxford & IBH publishing (P) Ltd, New Delhi, p. 551-574. RAVINDRAN, K. and A.G.G. PILLAI, 1984. Observations on the interrelation of marine corrosion and fouling in a tropical environment. In: Proceedings of sixth international congress on marine corrosion and fouling, Athens, p. 369-384. RELINI, G., 1984. Three years investigation on macrofouling of a Tyrrhenian power station, Italy. In: Proceedings of sixth international congress on marine corrosion and fouling, Athens, Mar. Biol, p. 159-170.

Settlement and succession of fouling communities

325

RENGANATHAN, T.K., N.B. NAIR and K. DHARMARAJ, 1982. Ecology of marine fouling organisms in Karapad creek, Tuticorin bay, southeast coast of India. Indian J. Mar. Sci., 11:132-137. RICHMOND, M.D. and R. SEED, 1991. A review of marine macrofouling communities with special reference to animal fouling. Biofouling, 3: 151-168. RIGGIO, S., 1979. The fouling settlements on artificial substrata in the harbour of Palermo (Sicily) in the years 1973-1975. Ouad. Lab. Technol. Pasca., 2:207-253 RYLAND, J.S., 1960. Experimentson the influence of light on the behaviour of polyzoan larvae.J. Exp. Biol., 37: 783-800. RYLANO, J.S., 1976. Physio{ogyand ecology of marine bryozoans.Adv. Mar. Bin1.,14: 285-443. SASIKUMAR, N., S. RAJAGOPALand KV.K. NAIR, 1989 Seasona]and vertical distribution of macrotoulants in Kalpakkamcoaslal walers. Indian J. Mar. Sci., 18: 270-275. SAWANT, S.S., 1985. Studies on some aspects of biofouling in the Mandovi and Zuari estuarine systems of Goa, India. M.Sc thesis, University of Bombay, India, 150 pp. SCHEER, B.T., 1945. The developmentof marine fouling communities. Biol. Bull., 89: 103-121. SCHOENER,A., E.R. LONG and J.R. DEPALMA,1978. Geographicvariation in artificial island colonization curves. Ecology,59: 367-382. SEED, R., 1969. The ecology of Mytilus edulis (Lamellibranchiata) on exposed rocky shores. 1. Breeding and settlement. Oecologia, 3: 227-316. SELVARAJ, V., 1984. Community structure in the coastal ecosystem with special reference to the green mussel, Pernaviridis (L) PhO. T~nesis,University of Madras, I~dia, 176 Pg. SMEDES, G.W., 1984. Seasonal changes and fouling community interaction. In: J.D Costlow and B.C. Tipper (Eds.), Marine bindeterioration: an interdisciplinary study. Naval Institute Press, Annapolis, Maryland, p. 155-160. SMEOES, G.W. and L.E. HURD, 1981. A empirical test of community stability resistance of a fouling community to a biological patchforming disturbance. Ecology,62: 1561-1572. STOECKER,D., 1978. Resistanceof a tunicate to fouling. Biol. Bull., 155: 615-626. STRICKLAND, J.D.H. and T.R. PARSONS,1972. A practical handl~ookof seawater analysis. Fisheries Research Board of Canada, Ottawa, 107: 11-26. SUTHERLAND, J.P. and RH. KARLSON, 1977. Development and stability of the fouling community at Beaufort, North Carolina. EcoL Monogr., 47:425-426 VENUGOPALAN,V.P., 1987. Studies on t~iofou~ingin the offs'norewaters of Arabian sea. ~'n.O.thesis, Ur~iv~rsityo~ 9ombay, India, 214 ~p. VERVOORT,W., 1966. Bathyaland abyssal hydroids. GalatheaReport, 8: 97-174. WHARTON, G.W., 1942. Report of the biologist. Norfolk Navy Yard, June 1941 to August 1942. WHEDON, W.F., 1943. Seasonal incidence of fouling at San Diego. Biological laboratory, Navy fuel depot, San Diego, Annual report for 1942-1943. WHOI, 1952. Marine fouling and its prevention. United States Naval Institute, Annapolis, Maryland, 388 pp.

Addresses of the authors:

I) Department o~ Ecology, Laboratory of Aquatic Ecology, Faculty of Science, University of Niimegen, Toernc~oiwld 1~ 6525 EO Niimegefl, The Netherlands. 2) Water and Steam Chemistry Laboratory, Indira Gandhi Centrefor Atomic Research Campus (ApCD, BARC), Kalpakkam603 102. India. 3) KEMA Environmental Research (KES), P.O. Box. 9035, 6800 ET Arnhem, The Netherlands.