Research Article

Mediterranean Marine Science Volume 7/2, 2006, 19-29

Marine fouling community in the Eastern harbour of Alexandria, Egypt compared with four decades of previous studies

SH. E., RAMADAN1, A. M., KHEIRALLAH2 and KH. M., ABDEL-SALAM1

1 National Institute of Oceanography and Fisheries, Kayet-Bey, Alexandria, Egypt 2 Zoology Department, Faculty of Science, Alexandria University, Egypt e-mail: [email protected]

Abstract

The aim of the present study is to compare the fouling communities between the years 1960 and 1999 in the Eastern harbour of Alexandria, Egypt and to study the main factors that may be controlling these communities. This comparison is based on monthly durations of panel immersion. By using roughened white polystyrene test panels (12.5x12.5 cm), monthly samples of marine foul- ing were collected from the harbour from October 1998 through September 1999. It is clear that a remarkable variation in number and diversity of fouling communities throughout the last four decades is evident. The minimum diversities were recorded during the studies of 1960 and 1970 (19 and 20 species respectively), while the maximum diversity (35 species) was achieved during the 1991 study. Moreover, a small shift among the four dominant groups (Polychaeta, Cirripedia, and Amphipoda) was noted during the four decades of the studies. The present comparison indicated that many factors may contribute to this variation, of which nu- trient enrichment is the most important and the nature of the applied test panel is lees so.

Keywords: Ecology; Community; Marine fouling; Eastern harbour of Alexandria; Comparison.

Introduction Pollution creates major differences in benthic community structure (Moran & Fouling results from the growth of ma- Grant, 1991). Nutrient enrichment sig- rine and plants on the surfaces of nificantly affects the composition of ma- submerged structures (Anon, 1952). At- rine fouling communities (Rastetter & taching of marine fouling organisms in a Cooke, 1979). remarkable numbers to submerged objects The Eastern harbour of Alexandria, Egypt has been demonstrated by several authors as is a relatively shallow semicircular bay, situ- a usual phenomenon in different world har- ated from longitudes 29º 53´ to 29º 54´ 40” bours (e.g. Wisely, 1959; Lepore & Gh- E and latitudes 31º 12´ to 31º 13´ N (Fig.1). erardi, 1977; Huang et al., 1982; Nair The harbour is surrounded by the city except & Nair, 1987; Cai & Li, 1990; Gordon on its northern side, where it communicates & Mawarati, 1992; Li et al., 1996) and with the sea through two outlets. The area in the Mediterranean harbours (e.g. Riggio of the harbour is about 2.53X106 m2, with a & Mazzola, 1976; Galluzzo, 1980; maximum depth of 11m (Selim, 1997). The Ramadan, 1986) average water depth of the bay is about 6.0 m

Medit. Mar. Sci, 7/2, 2006, 19-29 19 Fig. 1: Location of the Eastern Harbour (E.H.) of Alexandria and sampling site. and it receives many kinds of vessels, espe- (2002) mentioned that due to water circula- cially fishing boats (Al Sayes & Shak- tion the harbour is subjected to an additional weer, 1997). Since 1977, the diversion amount of municipal wastewater from the of municipal wastewater into the harbour main sewer of Alexandria (Kayet Bey), lo- has rendered its water eutrophic (Halim cated in its western vicinity (Fig.1). et al., 1980). Although it is supposed that Studies of fouling organisms in the Egyp- since 1999 the discharge of domestic sewage tian waters go back to Banoub (1960), into the harbour has totally ceased, Labib who investigated the succession of foul-

20 Medit. Mar. Sci, 7/2, 2006, 19-29 ing organisms settled on glass plates in the ing organisms settled on glass plates for a Eastern harbour of Alexandria, Egypt. He re- period of 7 months from February to Sep- corded 19 fouling species. The Eastern har- tember 1958. He recorded 19 species of foul- bour of Alexandria has also been studied by ing organisms which represent the minimum Megally (1970); Ghobashy (1976); diversity of fouling organisms in the Eastern El-Komi (1991; 1992; 1998). harbour as compared with the other studies The present work aims to compare the foul- that followed. He mentioned that competi- ing communities between the years 1960 and tion was very evident between the encrusted 1999 in the Eastern harbour of Alexandria, bryozoa and any other organisms. The most Egypt and to discuss the factors responsible for dominant species were the Hy- controlling these communities. droides norvegica, the amphitrite and the erect bryozoan Bugula Material and Methods neritina. As well, Megally (1970) inves- tigated the marine fouling organisms settled This work was carried out in the Eastern har- on glass plates for a period of 15 months bour of Alexandria, Egypt. Three replicate test from October 1968 to December 1969 and panels fixed to a wooden rack suspended verti- recorded 20 fouling species. The most domi- cally 0.5 m under water level were used to col- nant species were the polychaete lect monthly fouling samples from the harbour norvegica, the barnacle Balanus amphitrite from October 1998 through September 1999. and the erect bryozoan Bugula neritina. He The surface of the test panels facing seawa- found that all fouling organisms in the har- ter was roughened by using sand paper. These bour showed marked seasonal variations in panels were regularly replaced every month. abundance. A preliminary study was performed to com- Ghobashy (1976) studied the month- pare two substrata (the smooth glass and the ly variation and settlement behaviour of the roughened polystyrene panels). Three smooth principal fouling organisms that settled on glass panels and 3 roughened polystyrene pan- roughened panels made of impact-resistant els (each 12.5x12.5 cm) were immersed in sea- polystyrene for a period of 12 months from water for one month during August (summer) March 1973 to February 1974. He recorded 1998, before the survey was started. The fouling 23 species of fouling organisms and indicat- communities on these panels were weighed and ed that fouling occurred throughout the year identified to species level under (20X) zoom ste- but, the community might have been devel- reo- microscope. oping, flourishing and vanishing in a definite It is worth mentioning that this work and all period of time. The most dominant species the previous studies in the Eastern harbour of were the polychaete Hydroides norvegica, Alexandria were carried out at the same place the barnacle Balanus perforatus and the (panels were suspended vertically under the erect bryozoan Bugula neritina. El-Komi jetty of the National Institute of Oceanography (1991; 1992) studied the fouling organisms and Fisheries, Alexandria, Egypt). The present settled on roughened test panels made of comparison is based on monthly durations of polystyrene for periods of 12 and 14 months panel immersion. from March 1983 to February 1984 and Oc- tober 1990 to November 1991, respectively. Results In 1991 he recorded 35 species of fouling organisms which represent the maximum di- It is clear that there has been a variation versity of fouling organisms recorded at the in the number and diversity of fouling species Eastern harbour, while in 1992 he recorded throughout the last four decades (Table 1). 29 fouling species. In the study of 1991, the Banoub (1960) investigated the foul- most dominant species were the polychaete

Medit. Mar. Sci, 7/2, 2006, 19-29 21

(continued) sp. present study Algae Ulva lactuca Corallina officinalis Hydrozoa Obelia geniculata Bryozoa Erect Bugula neritina Encrusting Bryozoa Cryptosula pallasiana Polychaeta (Sed.) elegans Hydroides Bivalvia Modiolus barbatus Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Balanus Tanaidacea dulongii Tanais bovina Cirolana walkeri Sphaeroma serratum Sphaeroma Paradella dianae Cymodoce truncata Amphipoda acutum Corophium sextonae Corophium Elasmopus pectenicrus aera

. prolifera sp

sp. rubrum

. diversicolor

sp El-Komi (1998) Algae Ulva lactuca linza Enteromorpha Chaetomorpha Cladophora Ectocarpus Ceramium Hydrozoa Obelia geniculata Nematoda Epsilonema Bryozoa Erect Bugula neritina Bugula turbinata Zoobotryon verticillatum Polychaeta (Erra.) Nereis Syllis Polychaeta (Sed.) elegans Hydroides Serpula vermicularis Polydora ciliata Sabella pavonina Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Tanaidacea cavolinii Tanais Amphipoda

sp. sp. sp. . sp sp. trigonus

sp. diversicolor

El-Komi (1992) Algae Ulva lactuca Enteromorpha Cladophora Chaetomorpha Ectocarpus irregularis Hydrozoa Obelia geniculata Platyhelminthes Stylochus Bryozoa Erect Bugula neritina Bugula turbinata Zoobotryon verticillatum Polychaeta (Erra.) Nereis Polychaeta (Sed.) elegans Hydroides Spirorbis Pomatocerus triqueter Polydora ciliata Sabella Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Balanus Tanaidacea cavolinii Tanais Isopoda

. sp. . sp. sp. sp sp sp. . sp. sp. larynx sp . diversicolor

sp El-Komi (1991) Algae Ulva intestinalis Cladophora Chaetomorpha Enteromorpha Ectocarpus Ceramium Hydrozoa Obelia geniculata Tubularia Platyhelminthes unidentified specimen Bryozoa Erect Bugula neritina Bugula turbinata Zoobotryon Bowerbankia Encrusting Bryozoa Watersipora Polychaeta (Erra.) Nereis Syllis Polychaeta (Sed.) elegans Hydroides Spirorbis Serpula vermicularis Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus

Table 1

. sp. sp larynx trigonus

intestinalis plicata

sp. Ghobashy (1976) Algae compressa Enteromorpha linza Enteromorpha Ulva Ectocarpus Hydrozoa Obelia geniculata Tubularia Bryozoa Erect Bugula neritina Bugula avicularia Encrusting Bryozoa unicornis Schizoporella cucullata Watersipora Polychaeta (Sed.) norvegica Hydroides corrugatus Spirorbis Dasychone Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Balanus Amphipoda Jassa falcata Ericthonius brasiliensis Ascidian Solitary Ciona Styela Ascidian Colonial

. sp intestinalis plicata

Megally (1970) Algae Enteromorpha compressa linza Enteromorpha Ulva lactuca Ectocarpus irregularis Bryozoa Erect Bugula neritina Bugula avicularia Zoobotryon pellucidus Encrusting Bryozoa unicornis Schizoporella cucullata Watersipora Polychaeta (Sed.) norvegica Hydroides Spirorbis Sabella pavonina Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Ascidian Solitary Ciona Styela Ascidian Colonial Didemnum gelatinosum Didemnum maculosum Botrylloides leachii

sp. sp. sp. . sp. sp Banoub (1960) sp. Data from Banoub (1960), Megally (1970), Ghobashy (1976), El-Komi (1991; 1992; 1998) and the present study. sp. sp. sp. Fouling communities recorded on test panels between the years 1960 and 1999 at Eastern Harbour of Alexandria. Algae Ectocarpus Enteromorpha Ulva Porifera small unidentified specimen Hydrozoa Sertularia Tubularia Platyhelminthes unidentified specimen Bryozoa Erect Bugula neritina Bugula Encrusting Bryozoa unidentified specimen Polychaeta (Erra.) Nereis Polychaeta (Sed.) norvegica Hydroides Bivalvia a single specimen Cirripedia Balanus amphitrite Balanus eburneus Balanus perforatus Ascidian Solitary Ciona Styela Ascidian Colonial Author Fouling communities

22 Medit. Mar. Sci, 7/2, 2006, 19-29

1999 24 species Roughened polystyrene present study present 12.5 X cm Oct. 1998 to Sep. Ericthonius brasiliensis Decapoda Liocarcinus depurator Podocerus variegatus Stenothoe gallensis . sp 27 species Iron slides 7 X 2.5 cm El-Komi (1998) Feb. 1992 to May 1993 Ericthonius brasiliensis Jassa falcata Halesoma Ascidian Solitary Ciona intestinalis Corophium sextoni Elasmopus pectenicrus sp.

29 species intestinalis

17.5 X cm El-Komi (1992) Oct.1990 to Nov. 1991 Oct.1990 to Nov. Roughened polystyrene Corophium sextoni Corophium Elasmopus pectenicrus Stenothoe gallensis Ericthonius brasiliensis Pycnogonida Pycogonum Ascidian Solitary Ciona Amphipoda Cirolana aegyptiaca Sphaeroma walkeri . sp trigonus 1984

35 species Roughened polystyrene 15 X cm El-Komi (1991) Mar. 1983 to Feb. Mar. Tanais cavolinii Tanais Isopoda Cymodoce truncata Idotea baltica Dynamene bidentata Amphipoda sextoni Corophium Elasmopus pectenicrus Stenothoe Ericthonius brasiliensis Jassa falcata equilibra Caprella Ascidian Colonial Diplosoma listerianum Botryllus schlosseri Balanus Tanaidacea Table 1. (Continued)

23 species 10 X 12.5 cm Ghobashy (1976) Roughened polystyrene March 1973 to Feb. 1974

Diplosoma listerianum Botryllus schlosseri

20 species Smooth glass 12.5 X 20 cm Megally (1970) Oct.1968 to Dec. 1969

19 species 19 X 17 cm Smooth glass Banoub (1960) Feb. to Sept. 1958

unidentified specimen Author Fouling communities No. of fouling species Nature of test panels of Dimensions test panel Date of the experiment

Sed. = Sedentaria, Erra. Errantia

Medit. Mar. Sci, 7/2, 2006, 19-29 23 Table 2 (a). List of fouling species recorded on roughened polystyrene and smooth glass panels experimented at the Eastern Harbour of Alexandria during the same period of immersion during summer 1998. Roughened Smooth Type of panel Polystyrene panels Glass panels Recorded species Cyanophycophyta layer Cyanophycophyta layer Ulva lactuca Ulva lactuca Corallina officinalis Bugula neritina Obelia geniculata Bugula neritina Balanus amphitrite Hydroides elegans Tanais dulongii Balanus amphitrite Corophium acutum Balanus perforatus Stenothoe gallensis Tanais dulongii Ericthonius brasiliensis Corophium acutum Stenothoe gallensis Ericthonius brasiliensis Elasmopus pectenicrus (b). Average number of species and total biomass ± S.E. of fouling assembled on roughened polystyrene and smooth glass panels experimented at the Eastern Harbour of Alexandria during the same period of immersion during summer 1998.

Roughened Smooth Type of panel Polystyrene panel Glass panel Number of species/panel 10.3±0.9 7±0.6 Total biomass (gm)/panel 53±3.4 38±3.2

Hydroides elegans, the amphipods Erictho- September 1999 and records 24 species of nius brasiliensis, Corophium sextoni and fouling organisms. The most dominant spe- the erect bryozoan Bugula neritina, while in cies were the polychaete Hydroides elegans, the study of 1992 the most dominant species the barnacle Balanus amphitrite, the am- were the polychaete Hydroides elegans, the phipods Corophium acutum and Elasmopus barnacle Balanus amphitrite, the polychaete pectenicrus. As well as the experiment for Polydora ciliata and the erect bryozoan Bu- the settlement of fouling on the roughened gula neritina. polystyrene and smooth glass, test panels El-Komi (1998) studied the monthly revealed that the roughened ones collected fouling organisms settled on iron slides from more weight and fouling species than the February 1992 to May 1993. He recorded 27 smooth panels (Table 2). species of fouling organisms in the harbour. Concerning the dominant groups, the The most dominant species were the results indicated that there is a shift from polychaete Hydroides elegans, the amphi- Polychaeta, Cirripedia and Bryozoa during pod Corophium sextoni and the the studies of 1960, 1970and1976 to Poly- Balanus eburneus and B. amphitrite. chaeta, Amphipoda and Bryozoa during the The present work refers to the biota set- study of 1991, and a return to the previous tled on roughened polystyrene test panels for dominant groups in the study of 1992. The a period of 12 months from October 1998 to study of 1998 indicated that there was an-

24 Medit. Mar. Sci, 7/2, 2006, 19-29 other shift from Polychaeta, Cirripedia and groups which appeared in all studies (Algae, Bryozoa to Polychaeta, Amphipoda and Cir- Bryozoa, Polychaeta and Cirripedia). The ripedia. Meanwhile, in the present study, the groups Hydrozoa and appear in dominant groups are Polychaeta, Cirripedia all studies except one. On the other hand, and Amphipoda. there are groups like Porifera, Nema- toda, Decapoda, Pycnogonida which were Discussion recorded only in one study. Bivalvia appear in the studies of Banoub (1960) and the Recruitment of many sessile inverte- present work. Platyhelminthes were record- brates is influenced by a variety of biological, ed during the studies of Banoub (1960) chemical and physical factors (Crisp, 1984; and El-Komi (1991, 1992). Tanaidacea ap- Pawlik, 1992; Walters et al., 1997). pear in the studies of El-Komi (1991, 1992, The present results indicate that the maxi- and 1998) and in the present work. The Is- mum diversity of fouling organisms was re- opoda group appear in the present study and corded during the work of El-Komi (1991), the studies of El-Komi (1991 and 1992). while the minimum diversity was recorded It is clear that, the appearance or disap- during the work of Banoub (1960). pearance of animal groups may be related to Generally speaking, the fouling com- some environmental changes in the Eastern munities in the harbour consisted mainly of harbour. Banoub (1960) mentioned that Algae, Hydrozoa, Bryozoa, Polychaeta, Cir- the Alexandria sewage pumping station dis- ripedia, Amphipoda and Ascidiacea (Gho- charged very near to the harbour, which was bashy, 1976). occasionally slightly affected. Megally Banoub (1960) indicated the ap- (1970) indicated that the harbour was mod- pearance of detrital tubes during the period erately polluted due to both sewage disposal (May-September, 1958) and he thought that and waste material dumped from fishing the builder of these tubes was either an am- boats. phipod or a worm, since neither of these had Pollution creates major differences in been found inside the tubes. Ghobashy community structure (Moran & Grant, (1976) mentioned the occurrence of Am- 1991). It is worth mentioning that the dis- phipoda tubes and he recorded two species charge of domestic sewage into the harbour Jassa falcata and Ericthonius brasilensis. started in 1977 (Halim, 1980). During 1983, Moreover, he added that Megally (1970) did a total of 230,137 m3/day of this waste was not refer to Amphipoda tubes although their discharged in the Eastern harbour. At Kayet attachment constitutes one of the character- Bey pumping station, 200,000 m3 of wastes istics of this harbour fouling. From these, it were discharged daily into the open sea and could be concluded that during the studies of the remainder was discharged into the East- (1960 and 1970), the Amphipoda group was ern harbour of Alexandria. This means that represented but the authors did not mention the daily amount of discharge of domestic the appearance of any species of this group. sewage inside the harbour was 30,137 m3 / The present comparison revealed the ap- day in 1983. This amount varied with time. pearance of 15 fouling groups in the Eastern It gradually increased to reach 63,014 m3 / harbour of Alexandria. These groups are Al- day in 1986 (Said & Maiyza, 1987) and gae, Porifera, Hydrozoa, Nematoda, Platy- 95,134 m3 /day in 1987 (Faragallah, helminthes, Bryozoa, Polychaeta, Bivalvia, 1995). Recently during 1999-2000, after the Cirripedia, Tanaidacea, Isopoda, Amphipo- construction of the western treatment plant da, Decapoda, Pycnogonida and Ascidiacea. (which primarily treats the sewage and in- The distribution of fouling groups var- dustrial wastes from the central and western ies from one study to another, but there are parts of Alexandria), the discharge of domes-

Medit. Mar. Sci, 7/2, 2006, 19-29 25 tic sewage inside the harbour totally ceased during the same period of immersion (Table and the daily discharge into the open sea de- 2). This may be an explanation of the low creased to reach 140,000 m3 /day and 50,000 diversities of fouling organisms during the m3 /day from the main Kayet Bey pipeline studies of (1960 & 1970) which used smooth and El-Silslla outfall respectively (Jammo, glass surfaces. 2001). The waste discharged from the Kayet The present comparison revealed that the Bey pipeline may enrich the environment in- polychaete Hydroides elegans was the most side the harbour with nutrients, depending on dominant species in all the studies. It is worth the direction of both water current and wave noting that the previous studies in the East- action. ern harbour (1960, 1970 and 1976), men- Nutrient enrichment significantly affects tioned Hydroides elegans as H. norvegica. the composition of marine fouling communi- Zibrowius (1971) discriminated between ties (Rastetter & Cooke, 1979). The the two similar species in the shape of byonet discharge of sewage can stimulate autotrophic setae and in the operculum, as well as in the production in planktonic food sources and in habitats. H. elegans is an introduced species the fouling community itself, or depress the commonly found in Mediterranean harbours abundance of species sensitive to toxins in and polluted waters while H. norvegica in- the effluent and low oxygen levels associated habits deeper, unpolluted waters. Schel- with eutrophication. Biotic diversity in terms tema (1975) reported that the calcareous of species number usually increases when tube worm Hydroides is an important foul- pollution is moderate (Mor et al., 1970), but ing organism in warm temperate and tropical drops again in heavily disturbed areas. This seas. Moreover, it has already been shown was the case in 1983 when the daily amount that the development of an epibenthic com- of discharge of domestic sewage inside the munity is influenced by interspecific or in- harbour was moderate, reaching 30,137 m3 / traspecific epigrowth competitions. Despite day. This amount may support the maximum the fact that epigrowth competitions should diversity of fouling organisms (35 species) be far more frequent on smaller panels than in the Eastern harbour during the study of on larger ones, Levin & Paine (1974) ob- El-Komi (1991), meanwhile the increased served that on a larger surface where many or the decreased amounts of domestic sew- species compete for the available space, the age inside the harbour may not support the chances of survival in the presence of spa- settlement of larger numbers of fouling or- tial competition are relatively small. Kara- ganisms. That is to say that the daily amount nde & Swami (1988) indicated that the of about 30,000 m3 /day of sewage may be polychaete Hydroides showed no preference the optimum amount for fouling diversity in for any particular area. This may favor the the Eastern harbour. dominance of this species in any panel area. It is well established that most of the The comparison indicated that there is a sedentary animals settle preferably on rough small shift between the four dominant groups rather than on smooth surfaces (Ramadan, (Polychaeta, Cirripedia, Bryozoa and Am- 1986; McGuinness & Underwood, phipoda) during the four decades of studies. 1986; McGuinness, 1989; Anderson Regarding the results of dominant spe- & Underwood, 1994). Indeed, a prelimi- cies, there are few alien species occurring in nary study in the Eastern harbour of Alexan- the harbour. Alien species are those occur- dria indicated this. The roughened polysty- ring outside their historically known range rene panel hosted more species with higher as a result of direct or indirect introduction biomass (10.3±0.9 species and 53±3.4 gm re- or care by humans (Zenotos et al., 2005). spectively) than the smooth glass panel with In the Mediterranean Sea the polychaete the same area (7±0.6 species and 38±3.2 gm) Hydroides elegans is considered as a cryp-

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Accepted in April 2007

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