MARINE ECOLOGY PROGRESS SERIES Vol. 123: 301-312, 1995 ' 1 Published July 20 Mar Ecol Prog Ser
REVIEW Biotechnological investigation for the prevention of biofouling. I. Biological and biochemical principles for the prevention of biofouling
Sibylle Abarzua, Sabiene Jakubowski
Universitat Rostock, Fachbereich Biologie, Lehrstuhl Biochemie, Doberaner StraRe 143, D-18051 Rostock, Germany
ABSTRACT The most important b~ologicaland biochemcal methods with potential for the prevention of biofouling are descnbed Among these methods, the isolation of biogenic agents produced by several species of micro- and macroalgae and inanne invertebrates with antibacterial, antialgal, anh- protozoan and antlmacrofouhng properties may be the most promising and effective method for the prevention of biofoul~ng The isolated substances with the most potent ant~oulantactlvlty are fatty ac~ds,terpenes terpenoids, hpoproteins, glycolipids, phenols, lactons, peptides and steroids The advantage of the utilization of micro- and macroalgae for the isolation of biogenic agents is that algae can be cultivated m a short tlme in mass culture, independent of season Furthermore, they can be manipulated to a large extent in the direct~onof the 'production of biogenic agents' However, the cul- tivation of mcro- and macroalgae is very expensive Manne Invertebrates must be collected In certain seasons This collection of manne invertebrates could lead to an uncontrolled explo~tationof marlne organisms and to a change in the balance of marine ecosystems. Therefore, determination of the chem- ical structure and the subsequent synthesis of the deterrmned biogenic agents is necessary if marine invertebrates are to be used as producers of biogenic agents. Ant~foulingsystems must be both envi- ronmentally safe and effective for at least 3 yr when formulated as antifoul~ngpaints. There have been a few attempts at th~s,but no applicable successes have been reported to date
KEYWORDS Antifouling . Biofouling Growth inhibition Marine bioactive agents . Macrofoulers . Microfoulers . Settlement
INTRODUCTION 1978). This process occurs in the first minutes of the biological settlement (Fig. 1). After approximately 1 to What is biofouling? 2 h, the colonization of bacteria involving 2 distinct phases, a reversible approach phase ('adsorption') and Biofouling is one of the most important problems a nonreversible attachment phase ('adhesion'), occurs currently facing marine technology. In the marine (Marshall 1980, Wahl 1989) (Fig 1).The first, reversible environment any solid surface will become fouled. adsorption, is an instantaneous attraction which holds Materials submerged in seawater experience a series bacteria near the surface. The bacterial adsorption is of discrete physical, chemical and biological events essentially governed by physical forces: Brownian which results in the formation of a complex layer of motion, electrostatic interaction, gravity, and van-der- attached organisms known as biofouling. Waal forces (Fletcher & Loeb 1979, Walt et al. 1985). Loeb & Neihof (1975),Baier (1984) and Lewin (1984) The phenomenon is termed reversible because the have shown that the first event is the accumulation organisms can easily be removed before substantial of an organic 'conditioning' film consisting of chemical contact of cell surface has been made. The second, compounds (mostly protein, proteoglycans and poly- irreversible attachment phase can be made by bacteria sacchandes) mahng the surface wettable (Dexter that produce extracellular bridging polymer (e.g. poly-
O Inter-Research 1995 Resale of full article not permitted 302 Mar Ecol Prog Ser 123: 301-312, 1995
macrofouling
microfouling tenlary colonizers ------...------secondary colonlzen tt"ttm*****ttl-*mm*t*t+mN***~mtfm..**
pnmary colonizers 11111/11/111111~11111111~11111111111~////////////l//l/////l///////l///////////////l////////////////////////////////l organlc f~lm ...... subnrate
l min 1-24h l week 2 - 3 weeks
adhesion of bacter~a spores of macroalgae larvae of macrofoulerr organic parti- (e.g Pseudo- (e.g.Enterornorpha mtestinabs, (e.g.Balanus arnphrtrife[Cnrstacea] cles (e g protein) monas pufrefaciens. Ulothnx zonala Electra crustulenta[Bryozoa] ViMo aQinolyticus) [Cnloropnyta]) Laorned~aflexuosa [Coelenterata] Myirlus edulis [Molluscs] diatoms protozoa Spirorbisborealis [Polychaeta] (e g Achnantes brevrpes (e.g. Vaginicolasp.. Sfyela coriacea [Tun~cata]) Amphrprora paludosa. Vort~cellasp.. Amphora coffeaefom~s. Zoothamniu.r!sp., Licmophoraabbfeviata [Cillata]) Fig. 1. Temporal struc- Nirzschra pusilla) ture of settlement saccharide fibrils consisting mostly of glucose and fruc- (Von Oertzen et al. 1989). therefore there is an over- iusej. it is itnown that these polysaccharide fibrils lapping between micro- and macrofouling (Fig. 1).Lar- (slimes) are anchored to their chemical counterparts in vae of macrofoulers (sessile marine organisms such as the macromolecular film by lectins or divalent cations tunicates, coelenterates, bryozoans, barnacles, mus- (Ca++,Mg++) (Costerton et al. 1978). With the establish- sels, polychaetes), which are called tertiary colonizers, ment of covalent bonds between the bacterial glyco- then attach to the microfouling film (Fig. 1) (Takazawa calix and the macromolecular film the adsorption et al. 1992). Larvae of macrofoulers prefer to settle on phase blends into the adhesion phase (Wahl1989). The surfaces coated with microbial and algal films (Col- growing bacterial lawn, composed of dead and living well 1983). cells and their secreted 'slime', together with the macro- According to micro- and macrofouling processes the molecular film, constitutes the so-called primary film following overlapping time sequence is observed: bac- (slime film) (Wahl 1989). teria appear after approximately 1 to 2 h, diatoms after Diatoms, spores of macroalgae and protozoa appear 24 h, spores of macroalgae and protozoa after 1 wk and after the development of the primary film (Fig. 1) with larvae of macrofoulers after 2 to 3 wk (Von Oertzen et a clear quantitative dominance of the diatoms (Mar- al. 1989).It seems that all micro- and macrofoulers pro- shall et al. 1971, Caron & Sieburth 1981, Cuba & Blake duce adhesive substances necessary for their attach- 1983, Zahuranec 1991). Benthic diatoms are attached ment to solid surfaces such as the hull of a ship (Cook- by mucus secretion (Cooksey et al. 1984, Ferreira & sey et al. 1984).In the literature there are contradictory Seeliger 1985) and may densely cover wide substratum opinions on the question whether this sequence of areas. While in the majority of observed events diatom events constitutes a real ecological succession or not colonization was always preceded by bacterial attach- (Little 1984). ment (Little 1984), there may be exceptions (Sieburth The settlement of micro- and macrofoulers on the & Tootle 1981, Maki et al. 1988). Attachment of spores hulls of ships must be prevented for both economic and of macroalgae is realized by species such as Entero- ecological reasons. The bacterial slime films and the morpha intestinalis and Ulothrix zonata; protozoan large numbers of barnacles, mussels and tunicates colonizers belong mostly to the sessile or hemisessile which accumulate on ships increase drag forces and forms [e.g. Ciliata) or are mobile predators of micro- surface corrosion, thereby causing additional fuel, CO, organisms, not being considered to be true epibionts. emissions and maintenance costs (Gitlitz 1981). Bacteria and diatoms represent the primary coloniz- ers and spores of macroalgae and protozoa constitute the secondary colonizers in the process of microfouling Effect of the utilization of antifouling paints (Fig. 1). A clear separation between microfouling and macrofouling is impossible because the spores of In the efforts to avoid marine biofouling, antifoul- macroalgae belong to the macrofouling organisms ing paints are used, mostly with copper and tri-n- Abarzua & Jakubowski Prevention of biofouling 303
butyltin (TBT) as very effective active agents Alternative methods for the prevention of biofouling (Willemsen & Ferrarl 1993). The antifouling paints prevent blofouling by releasing effective biocides at Due to present and expected future restrictive regu- a constant rate. Since the early 1970s, triaryltin and lation on the use of TBT (Dalley 1987) and probably trialkyltin compounds have been increasingly used in other polluting antifouling compounds there is a grow- antifouling paints because of their excellent ability to ing need for other methods of the prevention of biofoul- prevent marine organisms from becoming encrusted ing. Several physical/mechanical, physical/chemical on ship bottoms and culturing nets (Suzuki et al. and biological/biochemical principles for the pre- 1992). vention of biofouling were used in the last 30 yr TBT is used as a biocide in coatings in 3 different (Gerencser et al. 1962, Schulz & Subklev 1964, Kuhl & ways: in free association paints (biocide dispersed in a Neumann 1969, Loeb & Neihof 1975, Characklis 1981, resinous matrix), in ablative paints (biocide is bonded Dhar et al. 1981, Branscomb & Rittschof 1984, Fletcher in a less permeable matrix that gradually flakes off) & Baier 1984, Humphries et al. 1986). and in self-polishing copolymers (SPC) (biocide is It is the aim of the present work to describe and chemically bonded). Self-polishing 01-ganotin copoly- evaluate the most important biological/biochemical mer formulations have the best release rate character- methods used for the prevention of settlement and to istics of currently available antifouling paints and are discuss the possibility of using biogenic agents pro- capable of maintaining vessels free from macroscopic duced by several marine organisms with antibacterial, biofouling for periods of up to 5 vr (Christie & Dalley antialgal, antiprotozoan and antimacrofouling proper- 1987). In use as an antifouling additive the use of ties for the prevention of biofouling. marine paints containing the broad-spectrum poison TBT grew to an estimated 136000 kg yr-' by the late 1980s (Uhler et al. 1993). The worldwide application BIOLOGICAL AND BIOCHEMICAL METHODS FOR of TBT-based paints has caused a growing pollution THE PREVENTION OF BIOFOULING of the environment and foods on a worldwide scale (Suzuki et al. 1992). TBT harms many forms of marine Dissolution of adhesive substances by several life other than fouling organisms, including economi- enzymes cally important species like oysters. Thus, shell defor- mation of the Pacific oyster Crassostrea gigas, and All biofouling organisms achieve their attachment by little or no natural oyster larvae settlement on hard using adhesive substances, the chemical structure of substrates, suggesting toxic effects in early life stages, which is quite similar for bacteria, &atoms, spores of were obseved in Arcachon Bay, France. More macroalgae and macrofoulers (acid polysaccharides extreme deformations occur in the common dogwhelk and glycoproteins) (Fletcher & Floodgate 1973, Haug Nucella lapillus, a species of thick-shelled snail found 1976, Humphrey et al. 1979, Percival 1979, Daniel et around the southwest peninsula of England. The al. 1987, Wigglesworth-Cooksey & Cooksey 1992).It is occurrence of imposex (the development of male assumed that a dissolution of these substances would characteristics, notably a penis and a sperm duct, on reduce the long-term attachment to solid surfaces females) was shown in centres of boating and ship- (Christie et al. 1970, Dempsey 1981, Evans 1981, Cinti ping activities, which is a sign of decline (Oehlmann et al. 1987). Certain enzymes, like trypsin, chymo- et al. 1993). Fewer females occur than would be trypsin, pronase and cc-amylase, are active in the expected, and juveniles and deposited egg capsules weakening action on adhesion in the bacterium Vibros are scarce or absent, indicating a low reproductive proteolytica and in zoospores of the green macroalga capacity. Enteromorpha intestinalis (Christie et al. 1970, Paul & Due to risk in application of organotin antifouling Jeffrey 1985). Short-term exposure to the enzymes coatings they have come under increasing govern- actinidin and pepsin can be used to separate the mental regulation in the United States and many west- stalked epiphytic diatoms Synedra tabulata and ern European countries (Price et al. 1992). This has Licmophora species from their brown or green algal initiated further development of TBT-free antifouling hosts (Booth 1981). A variety of hydrolytic enzymes paints, containing herbicides, antibiotica, copper salts were tested for effects on barnacle settlement on solid and other organic additives like amino-, azine- and surfaces (Rittschof et al. 1991). The majority of en- thio-derivatives (Golchert 1993, Peterson et al. 1993). zymes tested (cellulase, chitinase, collagenase, trypsin, These TBT-free antifouling coatings are capable of chymotrypsin, carboxypeptidase A, B, Y) had little maintaining ships free from biofouling for about 3 yr effect on settlement. But protease XI significantly but none of these additives can compete with organ- inhibited the settlement of barnacles on polystyrene otin containing SPCs (Golchert 1993). and glass surfaces, while papain had an inhibitory 304 Mar Ecol Prog Ser 123: 301-312,1995
effect on polystyrene surfaces only. The biotechnolog- tannic and sialic acids) have a negative effect on the ical production of these enzymes in large quantities is chemotaxis of bacteria, which results in an inhibition of possible, but relatively expensive. Furthermore, the bactenal attachment (Chet et al. 1975, Mitchell et al. enzymes are not permanently stable and different 1975, Chet & Mitchell 1976). Chemotaxis acts as a form enzymes are necessary to split the various adhesive of gravity, holding motile bacteria close to biofouling substances. Therefore, the method of dissolution of surfaces (Mitchell & Kirchman 1984).The strong nega- adhesive substances is applied only partly in practice. tive charged molecules of sialic acid are able to hold bacteria at distance, so that fixed association with the surface is blocked up (Corfield & Schauer 1982, Reuter Intervention in the metabolism of fouling organisms et al. 1982, Sonnichsen 1993). Successful field experi- ments have not yet been carried out. A well-balanced supply of calcium is necessary for a successful adhesion of bacteria, diatoms and spores of macroalgae (Marshal1 et al. 1971, Grant et al. 1973, Biogenic agents Haug 1976, Fletcher 1979, Cooksey & Cooksey 1980, Cooksey 1981, Turakhia & Characklis 1989). The Many marine organisms produce biogenic agents process of synthesis and secretion of adhesive sub- with antibacterial, antialgal, antifungal, antiprotozoan stances leading to motility and adhesion in diatoms can and antimacrofouling properties tc defend themseives 'De prevented by uncouplers of energy metabolism against robbers and settlement in the marine environ- (CCCP, carbonyl cyanide 3-chlorophenyl hydrazone), ment. Therefore, the production and isolation of bio- protein synthesis inhibitors (cycloheximide), and com- genic substances from marine organisms seem to be pounds that interfere with Ca transport (D-600, a-iso- the most promising and effective methods fer the pre- prbp~~-~-i~N-~neihyi-N-nomoveratryl)-y-amino-propyl]-vention of biofouling. 3,4-5-trimethoxy phenylacetonitrile) (Cooksey & Cooksey 1980, Cooksey 1981, Cooksey et al. 1984). The formation of sulfated polysaccharides responsible as gel for the attachment of the spores of green BIOGENIC AGENTS AND THEIR EFFECTS macroalgae can be blocked by the reduction of cal- ON FOULING ORGANISMS cium and borate supply (Haug 1976). All these ex- periments, however, have been carried out only under Definition of biogenic agents laboratory conditions and without regard to antifoul- ing aspects. Numerous living organisms, including microorgan- isms, fungi, plants and anlmals, are able to synthesize Competitive inhibition of receptors by offering biogenic agents. These biogenic agents are synthe- specific lectin-like substances sized in the secondary metabolism of the producer and are not directly essential for its life. They serve It has been shown for many macrofouling organisms animals as protection from enemles (e.g. robbers), that special substances (e.g. insoluble protein-conju- plants as protection against feeding and microorgan- gates) can contact with corresponding receptors of isms in the suppression of growth and reproduction of the larvae and induce an attachment and a metamor- other microbes. Teuscher & Lindequist (1988) defined phosis. By offering specific lectin-like substances, biogenic agents as follows: biogenic agents are chem- which have a stronger affinity to the receptors than the ical compounds which are synthesized by living insoluble protein-conjugates, the attachment is organisms and which, if they exceed certain concen- affected (Morse 1984). It is also possible to inhibit trations, cause temporary or permanent damage or adhesion processes by offering simple sugars to bacte- even the death of other organisms by chemical or rial lectins (reversed process) (Corfield & Schauer physicochemical effects. The concentration which 1982, Reuter et al. 1982, Imam et al. 1984, Sijnnichsen causes damage and the extent of this damage are 1993). These expenments have been performed only determined by the type of substance, the place and under laboratory conditions. type of application, the duration of the effect, the indi- vidual sensitivity of the corresponding organism and other factors Negative chemotaxis Marine organisms (especially micro- and macroalgae and marine invertebrates) were investigated in the last Numerous experimental results prove that special decade with growing intensity regarding chemistry organic nontoxic substances (e.g acrylamide, benzolc, and pharmacology of their active agents. The sub- Abarzua & Jakubowski: Prevention of biofouling 3 05
stances isolated in this connection belong, above all, to algal, antifungal or antiprotozoan effects, are given in the groups of fatty acids, terpenes, terpenoids, lipopro- Table 1. Macrofoulers were not tested. Tables 2 & 3 teins, glycolipids, phenols, lactons, alkaloids and pep- show bioactive substances (e.g. fatty acids, glycolip- tides. Depending on the screening methods used, the ids/lipoproteins, terpenes/carbohydrates, goniodomin, effects of the isolated potential drugs were mainly chlorophyll c and a-linolenic acid) isolated from spe- antibacterial, antiviral and antifungal. According to cial species of Chrysophyceae, Dinophyceae and Ireland et al. (1993), ca 35% of these biogenic com- Chlorophyceae that have inhibitory effects on the pounds are produced by micro- and macroalgae and growth of bacteria, algae, fungi and protozoa. Macro- ca 65 % by marine invertebrates. The ability of marine algae like Phaeophyceae, Chlorophyceae, Conjugato- organisms to produce biogenic substances with phyceae and Charophyceae also produce biogenic antibacterial, antialgal, antiprotozoan and antimacro- substances with antibacterial, antialgal, antifungal, fouler properties could be used in the prevention of antiprotozoan and antimacrofouling effects (Tables 4 & biofouling. 5). The special biogenic substances listed in the tables were isolated from micro- and macroalgae and tested predominantly with regard to antibacterial, antialgal Biogenic agents isolated from micro- and rnacroalgae and antifungal activities and not with regard to anti- fouling aspects. Effects on the growth of macrofoulers An immense number of substances with anti- (e.g. polychaetes, mussels) were investigated only with bacterial, antiviral, antifungal and pharmacological some species of macroalgae (Laminaria digitata, properties have been isolated from micro- and macro- Costaria costatum, Undaria pinnatifida; Tables 4 & 5). algae, analyzed, and tested for medical purposes in the In contrast to micro- and macroalgae, higher plants are last few years. Tables 1 to 5 give an overview of the well documented as antifouling agents (Sawant et al. existence of special biogenic compounds in micro- and 1992, Sawant & Wagh 1994). macroalgae and their effect on the growth of several The cultivation of micro- and macroalgae as well as bacteria, algae, fungi, protozoa and macrofoulers. the extraction of biogenic agents is expensive. How- Several biogenic compounds, such as bromophenols, ever, algae can be used very well as 'extraction organ- malyngolides, aponin, cyanobacterin, hapalindoles, isms' because they can be cultivated in a short time fischerellin, galactosyldiacylglycerols, tjipanazoles in mass culture independent of season and can be and scytophycins, isolated from special species of manipulated to a large extent in the direction of 'pro- Cyanophyceae that have either antibacterial, anti- duction of biogenic agents'.
Table 1. Existence and effects of biogenic agents isolated from Cyanophyceae (microalgae)
Species Biogenic agent Effects Source Anti- Anti- Anti- Anti- bacterial algal fungal protozoan p- Calothliu brevissima Bromophenols Pedersen & Da Silva (1973) Lyngbya majuscula Malyngolide Cardllina et al. (1979) Gomphosphaeria aponina Aponin Eng-Wilmot et al. (1979) Anabaena flos-aquae ? Snell (1980) Scytonema hofmanni Cyanobacterin Mason et al. (1982). Gleason & Paulson (1984), Gleason & Baxa (1986) Fischerella muscjcola Flores & Wolk (1986) Scytonema pseudohofmannj Scytophycins Ishibashi et al. (1986) Hapalosiphon fontinalis Hapalindoles Moore et al. (1987) Synechocystjs leopoliensis Methanolic extracts Cannell et al. (1988) Oscillatoria sp. Ether extracts Baghi et al. (1990) FischereLla muscicola Fischerellin Gross et al. (1991) Nostoc muscorum Methanolic extracts De Mule et al. (1991) Nostoc muscorum Aqueous extracts Bloor & England (1991) Nostoc hncha Cyanobacterin LU-1 Gromov et a1.(1991) Phormldium tenue Galactosyldiacylglycerols Murakami et al. (1991) Tolypothrix tjipanasensis Tjipanazoles Bonjouklian et al. (1991) Scytonema ocellatum Toly toxin (scytophycin) Patterson & Carmeli (1992) Mar Ecol Prog Ser 123: 301-312, 1995
Table 2 Existence and effects of biogen~cagents isolated from Chrysophyceae and Dinophyceae (microalgae)
Species Biogenic agent Effects Source Anti- Anti- Anti- Anti- bacterial algal fungal protozoan
Chrysophyceae Ochromonas dancia Fatty acids ? X Aaronson & Bensky (1967) Prymnesium panrum GlycolipidAipoprotein Paster (1973), Shilo (1979)
Dinophyceae Protogonyaulax tamarensis Terpenes/carbohydrates X Burkholder et al. (1960) Prorocentrum micans Terpenes/carbohydrates X Burkholder et al. (1960) Goniodoma sp. Goniodomin X Sharma et al. (1968) . Peridinium bipes Fatty acids, chlorophyll c X Uchida et al. (1988) Prorocentrum lima Polyether compounds Nagai et al. (1990) Dinoph ysis fortii Polyether compounds X Nagai et al. (1990) Gam bierdiscus toxicus Polyether compounds X Naga~et al. (1990)
Siogenic ayenis isolated trom marine invertebrates phytic organisms. They frequently produce high con- centrations of biogenic agents with potent antifoulant In recent years several comprehensive accounts of activities. Especially octocorals and sponges are a rich antifungal, antibacterial, antialgal, antiviral and phar- source of compounds that act as antifoulants [Willem- maco!ogica! activities of bioyeriic substances isolated sen & Ferrari 1993). from several species of marine invertebrates have been Targett et al. (1983) determined that Leptogorgia published (Targett et aI. 1983, Bakus & Kawaguchi virgulata and L. setacea contain hlgh concentrations of 1984, Wahl 1987, Sears et al. 1990, Ireland et al. 1993). homarine, which inhibited growth of the biofouling From 1977 to 1987, 1595 bioactive compounds were diatom Navicula salinicola. Extracts of L. virgulata and isolated from marine invertebrates worldwide, pre- Neosimnia uniplicata, a snail of L. virgulata, strongly dominantly sponges, coelenterates, bryozoans and inhibited the settlement of the barnacle Balanus ascidians (Ireland et al. 1993). Tests for medical pur- amphitrite. Rioassay-directed purification of L. virgu- poses were performed, for instance, with bryostatines lata extracts led to the identification of 2 diterpenoid from bryozoans with antitumoral properties, with hydrocarbons, pukalide and epoxypukalide, as anti- didemnines from ascidians with antiviral and anti- fouling agents (Gerhart et al. 1988). Many investiga- tumoral activities and palytoxin from corals with neu- tions with new species of octocorals and sponges result rotoxic effects (Ireland et al. 1993). Furthermore, a in the discovery of new compounds, e.g. herbacin, a variety of sessile marine invertebrates contain sec- new furanosequiterpene from the marine sponge ondary metabolites affecting the settlement of fouling Dysidea herbacea (Sarma et al. 1986). organisms. It is known that representatives of Porifera, A series of chemical compounds, like lactons, fatty Cnidaria and Tunicata are rarely overgrown by epi- acids, bromopyrroles, homarine, herbacin, pukalides,
Table 3. Existence and effects of biogenic agents isolated from Chlorophyceae (microalgae)
Species Biogenic agent Effects Source Antibacterial Antialgal
Stichococcus mira bilis Fatty acids? Harder & Oppermann (1953) Protosiphon botryoides Fatty acids? Harder & Oppermann (1953) Chlamydomonas reinhardii Fatty acids Proctor (1956) Hydrodictyum reticulatum Fatty acids Olfers-Weber & Mihm (1978) Dictyosphaerium pulchellum Methanolic extracts Cannell et al. (1988) Klebsorm~dium cren ulatum Methanolic extracts Cannell et al. (1.988) Chlorokybus atmophyticus Acetone extracts Cannell et al. (1988) Pleurastrum terrestre Methanolic extracts Cannell et al. (1988) Sta urastrum gracile Methanolic extracts Cannell et al. (1988) Chlorococcum sp. Aqueous extract Ohta et al. (1993) Chlorococcum HS- 10 1 a-Linolenic acid Ohta et al. (1993) Abarzua & Jakubowski: Prevention of biofouling 307
Table 4. Existence and effects of biogenic agents isolated from Phaeophyceae (macroalgae). S.: Spirorbis; M.: Mytilus
Species Biogenic agent Effects Source Anti- Anti- Anti- Antimacro- bacterial algal fungal fouling on
Laminaria digitata ? X S. inornatus AI-Ogily & Knight-Jones (1977) Fucus vesiculosus Phlorotannins X Glombitza & Lentz (1981) Cytoseira balearica Lipid extract X Caccamese et al. (1981) Zanardinia prototypus Lipid extract X Caccamese et al. (1981) Pelvetia canaliculata Phlorotannins X Glombitza & Klapperich (1985) Laminaria saccharina Unsaturated fatty acids X Rose11 & Srivastava (1987) Desmarestia ligulata Unsaturated fatty acids x Rose11 & Srivastava (1987) Sargassum horneri Mucilage extract Tanaka & Asakawa (1988) Costaria costatum Glycerols Katsuoka et al. (1990) Fucus vesiculosus Methanolic extract X Lustigman & Brown (1991) Fucus endentatus Methanolic extract X Lustigman & Brown (1991) Fucus spiralis Methanolic and X Lustigman & Brown (1991) chloroform extract Lustigmann et al. (1992) Laminaria agardhii Methanolic and Lustigman et al. (1992) chloroform extract Sargassum wightii Chloroform extract Sastry & Rao (1994) Pad~natetrastromatica Chloroform extract X Sastry & Rao (1994) peptides, steroids and saponins, isolated from several (Willemsen & Ferrari 1983) containing compounds of species of Porifera, Cnidaria, Tunicata and Mollusca unknown structure. It can be seen from Table 6 that with antibacterial, antialgal activities and activities antibacterial and antialgal effects (effects against preventing the settlement by macrofouling organisms microfouling) are predominantly observed for homa- are listed in Table 6. In some cases, the structure of the rine, fatty acids, peptides and steroids from Polysyn- active agent has not yet been clarified (Standing et al. craton lacazei (ascidian) and Leptogorgia virgulata 1984, Ware 1984, Rittschof et al. 1985, Sears et al. 1990, (coral) (Targett et al. 1983, Wahl 1987). Mary et al. 1991) (Table 6). Even the results of tests of Potent antimacrofouling activity against the blue 51 sponge extracts under field conditions for their mussel Mytilus edulis and the barnacle Balanus ability to prevent biofouling showed the potential amphitrite and other macrofouling organisms was antifouling activity of most of the tested crude extracts found in extracts of several sponges (Lissodendoryx
Table 5. Existence and effects of biogenic agents isolated from Rhodophyceae, Chlorophyceae, Conjugatophyceae and Charo- phyceae (macroalgae). M.: Mytjlus
Species Biogenic agent Effects Source Anti- Anti- Anti- Anti- Antimacro- bacterial algal fungal protozoan fouling on:
Rhodophyceae Laurencia obtusa Laurencienyne Caccamese et al. (1981) Centroceras clavulatum Lipid extract Caccamese et al. (1981) Sphaerococcus coronopifolius Lipid extract Caccamese et al. (1981)
Grac~lariacort~cata Chloroform extract > Sastry & Rao (1994) Acanthophora delilei Chloroform extract : Sastry & Rao (1994) Chlorophyceae Codium corallo~des Lipid extract Caccamese et al. (1981) Caulerpa ashmead~i Terpenoids Paul et al. (1987) Undaria plnnatifjda Glycerols A4. edulis Katsuoka et al. (1990)
En teromorpha linza Methanolic extract > Lustigman & Brown (1991) Conjugatophyceae Splrogyra sp. Tannin ? Misra & Sinha (1979) Charophyceae Chara globularis Dithiolan, trithian X Wium-Andersen et al. (1982) 308 Mar Ecol Prog Ser 123: 301-312, 1995
Table 6. Existence and effects of antifouling agents isolated from special species of marine invertebrates. Species: Agaricia lamarcki, Balanus amphitnte, Buguia neritina, Hippopodna americana, Hydroides norvegica, Laomedia bistriata, A4ytilus edulis, Serpula ver- micularis
Species Biogenic agent Effects Source Anti- Anti- Antimacro- bacterial algal fouling on:
Porifera Xestospongia halichondnodes ? B. neritina Ware (1984) Placortis Lactons, phenols, A. lamarch Porter & Targett (1988) halichondroides cyclic peroxides Lissodendoryx isodictyalis Terpenoids? B. amphitrite Sears et al. (1990) Agelas conifera Bromopyrroles B. amphitrite Keifer et a1.(1991) Dysidea herbacea Herbicin L bistriata Sarma et al. (1991) (furanosesqul- H. americana terpene) H. norvegica S. vermicularis Phyllospongla papyracea Fatty acids M. edulis Goto et al. (1992) B. amphitrite
Cnidaria [Anthozoa) Leptogorg~asetacea Homarine X Targett et al. (1983) L. virgulata Homarine X Targett et al. (1983) L. virgula fa 2 B. amphitrite Standing et al. (1984) L. virgula ta ? B. amphitrite Rittschof et al. (1985) Ivluricea frutico.ss M-ficin; (saponis) X Bandurraga & Fenical (1985) Renilla reniformis Diterpenes B.amphitrite Keifer et al. (1986) Renilla renlformis ? B. amphitnte Rittschof et al. (1986) L. virgulata Pukalide, epoxypukalide B. amphitrite Gerhart et al. (1988) (diterpenoids) Suberogorgia suberosa ? B. amphitr~te Mary et al. (1991) Spongodes sp. B amphitrite Mary et al. (1991) Solenocaulon tortuosum B. amphitrite Mary et al. (1991) Echinogorgia complexa B. amphitrite Mary et al. (1991) Juncella juncea B amphitrite Mary et al. (1991)
Mollusca (Gastropoda) Neosimnia uniplica ta B. amphitnte Gerhart et a1.(1988)
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a, a2 2 2 2 2 G 8 2 5Ill 2m +l '-4 2i L+ 0m a0 3 G .. 2Ill z!q LOW CO m 6 '?: '?: m m N 3 a b 2'60V 2 67 -0 * 2 L z 5i. - iu 2 3 .- .z h G 2 S >." t"T! 2 0 2 2- m- + Editorial Advisors Marine Ecology Progress Series (MEPS) is edited in cooperation with the Editorial Advisors (EAs) listed below and about 400 Anonymous Referees. EAs are appointed for a 4-year period; re-appointment is possible. They critically evaluate the scientific merits of submitted manuscripts. EAs also recommend authors and topics for reviews to be published in MEPS. Several EAs have been appointed as Senior EAs, marked below by 0; they may act as Sub-editors by processing manuscripts themselves, i.e. see them through a rigorous 3-referee evaluation process and present them to the Editor who reserves the right - - of final acceptance.
Riisgdrd, H. U. e3 Humphrey, G. F. O ENVIRONMENTAL FACTORS Odense L'niv., Biologisk Inst~tut,Campusvej CSlRO hlanne Biochemistr)'. Bu~ldingA12, 55, DK-5230 Odcnse hi., Denmark Sydney llniv.. NSW 2006. .Au.;tral~a Ahmed. S. I. Env~ronmrntaleffects on ~nvenebrates,blo- Photosynthesis; plankton b~ochemlstr). School of Oceanographv, WB-IU, ljnlv of energfJlics suspension geaeis------Washington. Seattle. WA 98145. USA - Leftley. J. W. Phys~ologicalecology of phytoplankton; ther- Southward. A. J. Dunstaffnage Marine Research Laboratory mophiric n;ic?oorgdniin Rheinheimer, G. Cs3 Sccpps Jnst~t~ltionof Oceanugraphy. San Instltut fur Zooloqie drr Leopold-Frdnzcns Inslitut lur Meereskunde, Umv. of K~el,Dus- D~ego,PO Box 1521), Le Julld, CA 92093, USA Univ. Innsbruck. 'TcchnlkerstrdOe 25, i-6020 ternbrooker Weg 20, D-24 105 K~el,Ciermany Comparative, c~lluiar and developmentalp- - Innsbruck. Austrla p.Manne - mrrroh~oloqy.~.- phys~ulogy Phys~oloq~ralecology of . fnvertchrates Zhirmunsky, A. V. Caron. D. A. O Furness. R. W. Institute of Manne B~ology, Academy of B~ology Dept. Woods Hole Oceanographic Dept of Zoology. The Univ. of Glasgow, Sc~ences,Vlad~vostok 690032 Kuss~a lnshtutlon Woods Hole MA 02543. USA Glasgow G12 80Q. Scotland '.lechan~smz of cellular resistdnce and control M~crob~alecology trophlc relations between Ecology of sea blrds pldnktvnic proroloans and-other hetcrotroph~c Furuya, K. CULTIVATION dnd photosvnthetir-orqdnismspclaq1c-detrit2j Faculty of Bioresources, Mle Univ., 1515 Kami- --pagqreqatez hama. Tsu 514, Japan Lawrence, J. M. B Collos. Y. 8 Phvtoplankton ccology; rommun~ty- - structure. , ...... Dept of Biology, Univ. of South Florida, Tampa, Laboratoire d'Flydrobiologie, Universite de dynamics FL 33620, USA Montpellier CC 093, F-34095 Montpellier Cedex Gage, J. D. C9 yutntion of invrrtebrates 5, France Dunstaffnage hlanne Research Laboratory, PO Nltroqen cvcling and primary production Box 3, Oban, 12rqvll PA34 4AD. Scotland Meyers. S. P. O - -- ...... - -- Benthos of deep sca and temperate roasts Dept of Food Science, Louisiana State IJniv.. Conover, R. J. -- . Baton Roug~,LA 70803, USA Manne Ecology Laboratory, Bedford lnstitute of ~ra; J. Cultivation of nucroorr~an~s~nsand crustaceans; Oceanoqraphy, PO Box 1006, Dartmouth, NS. lnst~iuttIor Mnrinb~olog~og L~mnolog~.Umv. ayuaculturF. .- nilcrt~r!nv~ronments Canada B2Y 4.42 Oslo. Postboks 1064. Rlindem, Oslo 3, Nonvay Soft-sedimentA-.. ecology Pandian, T. J. Zooplankton bioloqy School of Biological Sciences, Madurai Kamaraj Cushing, D. H. Haedrich. R. L. O Univ., Madura~625 021, Tdmllnadu, India M~nlstry of Agriculture, Flsher~es and Food, Memorial Cniv. of Newfoundland. St. John's. C:ult~vation,. of decapods and f~shes; bioener- Flsher~esLaboratory, Lowestoft. Suffolk NK33 NF, Canada A1B 3x9 getics- - OHT, England P-Zooqeograghv: .- natural history of fish Rheinheimer, G. O Productivity ofLhe2ea; fish-population-dyna? Hansen, B. Institut fiir Meereskunde, Univ. Kiel, Diistem- ~cs:b~nloq~ral_oceanography Roskilde Univ., lnstltute I, Life Sciences & P Chemistry. PO Box 250. DK-4000 Roskilde. brooker Weg 20, D-24105 Kiel, Gemany Deibel, D. Denmark Culhvation of rmcroorqanisms Ocean Sciences Center, Memonal Univ. of New -- Laboratory and in situ studies on zooplankton; foundland, St. John's, NF, Canada AIC 5S7 seconday production (grazing, growth, ener- Zooplankton ecolo~/nutrit~on,qelatinous ecol- DYNAMICS p. . . . . - getic~.fccdmq behaviour)-. ogy/phvsiology Hardlng, G. C. Ahmed, S. I. de Jonge. V. h4anne Ecology Laboratory, Bedford lnstitute of School of Oceanography, WB-10, Univ of National Institute for Coastal and Marine Oceanography, PO Box 1006, Dartmouth, NS, Washlngton, Seattle, WA 98195, USA Management [RIKZ), PO Box 207, 9750 AE Canada B2Y 4A2 Phytoplankton ecology, greenhouse gases and Haren, The Netherlands Crustacean ecolo~Jincl.deep sea) Tobal ocedm-ilux, sed~mmtary-rm?robloE Esluanne ant1 coactal processes, m~crophvto_ btsnthos and tdqrdcs, pror&<nkton Park%llle.VIC 3052, Australia 1006, Dartmouth. NS, Canadd 4A2 Physiologica~~~!~grr?'andreproductive !low rytomrtry; photosynthet~cphytoplank- Dring, M. J. -of estuanne-and..-mTn"~-n- ton; Flations hr.lwf~'n phytoplankton an8 Biologische Anstalt Helgoiand, D-27498 --~o~a~ hrtEotroph~cFartc?noplankton Helgoland, Germany McLusky, D. S. O Phys~olog~calecology of algae PHYSIOLOGICALMECHANISMS Dept of Biological Sciences. Univ. of St~rling, Fisher, N. S. Stirling FK9 4LA, Scotland hlarine Sciences Research Center. State Osmoregulation in estuarine invertebrates ~nlvof ~ewyork. stony rook* NY 11794- Marine Research Laboratov, Naylor, L. 5000, USA PO BOX 3,Ohan, ~.rgy]! ~AC,Scot;alld School uf Ocean Sciences. Univ of Wales, Physioloplral ~mlogyof phytopl~nkton Behavioural phys~ologyof fish; feedmq; p%- Menai Bridge. G~nedd 5EY. Wales Fowler, S. W. @ daiion offish-larvae Rehaviourdl physiology; invertebrate-- biology International Atomic Energy Agency, Marine Browman, H. I, Pawlik, J. Environment Laboratory. 19, Ave dcs Gas- hlarjne productivity ~ivi~,~~,M~~~,~~- T~VUn~v. of ~orth Carolina at W~lmmgton, tellans, BP 800, MC-98012 Monaco Cedex Lamontagne Institute. Dept of Fisheries and WilmJngton, NC 28403-3297. USA Trace elcmcnt metabolism nre;lns C;.~~+?,c? 130~.:v:ull~-juil, PQ, Cllrl~~icaiaeiense ot invertebytes; ant]- Haedrich, R. L. B Canada C;5H 324 fouling, chemical cues Memorial Univ. of Newfoundland, St. John's, Foraging, behavior and development of (sen- puiseux-D~O,S. NF. Canada A1B 3x9 srqfiydns, aspec~illly~n flshcs Laboratoue de Cytophysiolog~avegetale et de Environmental effects on f~sbes-(incl,deep SPA) B~~,,,,,, B.E, Toxicoloqe ceuula~re,Un~versitP de Paris VJI, 2 ~~ptof ~i~lo~, -rhc University, yewcastle. Place Jussleu. F-75251 Pans Cedex OS, France Kasyanov, V. Ecoph siolo~yand taxicoloq nt algae, crllu- lnst~tute of Marine Biology. Acddcmy of UPO~-TY~~7RU- Engldnd Sc~ences.Vladivoslok 690032, Kussid .-Phys~olop anrl ecology of cordls E-- h;&rly-ile~ivinr-or~~rla(~-~. - Environn~ental clfeclr on invcrtcbrates; re- ~~~hh~]~,F. Rivkin. R. B. protluct~on,d~.vclopmcnt ~~~l~~i~~h~Anstalt ~~l~~l~~d,M~~~~~.Ocean Sciences Centre, Univ. of Newfound- station, D-27498 Helgoland. Gcrmdny land, St. John's, NF, Cdnddd ;\1C 537 Kierboe. T. O !?h~to~lanktnnP~Y~~~~~w "" c.c0109' ~~~~~h ~~~~i~~~~for ~i~h~ri~~and Physiological ecolog)t, rnetdbolic dnd thermal , Charlottenlund Castle, DK-2y20 Char- =amion; zoopldnktorl; moultinr~ Shick, J.M. d lottenlund, Denmark Burton, R. S. Dept of Zooloq, Unlv, of Maine, Murray Phvs~olog~ralPCO~O~V of zooplankton. lnclud- Marine Biology Research Dlrision 0202, Hall, Orono, ME 04469-5751, USA in<'fiiht=s(%P. pp ~~IT~LT - Scnpps Institution of Oceanography, Lnlv, of ph~siologlcal energetics. . -- of-- invertebrates:- - California, 9500 Gilman, La Jolla, CA 92093- '"cl. caTonmet~; s~mEes; Lawrence. J. M. O yperoxld an 0x1 atrv~stress~rrts oi l.'\' De~tof BioloW Unlv Florida. -mermprha- &ht; sea anek~~b~oio~~- Tampa. FL 33620. USA nisms In populat~ons:blorhemlral and m&>- Stickle. W. B. Phys~oloqicalecolov - ofinver?ehrales-. - uldr genet~rTiiXi~K