British Phycological Journal

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The settlement, attachment and establishment of marine algal spores Robert L. Fletcher & Maureen E. Callow To cite this article: Robert L. Fletcher & Maureen E. Callow (1992) The settlement, attachment and establishment of marine algal spores, British Phycological Journal, 27:3, 303-329, DOI: 10.1080/00071619200650281 To link to this article: http://dx.doi.org/10.1080/00071619200650281

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Date: 18 January 2017, At: 21:57

Br. phycol. J. 27:303-329 1 September 1992

The Settlement, Attachment and Establishment of Marine Algal Spores By ROBERT L. FLETCHER and MAUREEN E. CALLOW

The Marine Laboratory, School of Biological Sciences, University of Portsmouth, Ferry Road, Hayling Island, Hampshire, P O l l ODG, UK and School of Biological Sciences, University of Birmingham, Edgbaston, Birmingham, B15 2TT, UK One of the most fundamental and precarious stages in the life history of a marine benthic alga is the colonization of a new substratum. For the majority of algae this is achieved by the formation and detachment of different types of highly specialized reproductive propagules which are then dispersed via the pelagic zone. This paper reviews the process of "settlement", "attachment" and "establishment" of these propagules. Particular attention is given to the influence of substratum surface properties, both physical and chemical, on these processes, along with aspects of the derivation, chemical composition, mechanisms of release and mode of action of the various adhesives secreted by the attaching spores and germlings.

One of the most fundamental processes in the life history of a benthic marine alga is the colonization of a new substratum. In many algae, particularly those with a heterotrichous mode of construction, this can be achieved by the lateral outgrowth of the basal attachment processes, followed where appropriate by erect shoot development. In some algae, e.g. Taonia, these marginal portions with emergent plantules can become detached to form new plants (Mathieson, 1966), usually as a result of wave action or grazer activity. In other algae, e.g. Ralfsia verrucosa, this peripheral growth can be accompanied by the senescence of the older central tissue (Fletcher, 1978). Such a vegetative means of propagation was considered likely by Davies & Wilce (1987) to be important in unstable, physically disturbed habitats such as cobble stones. Occasionally, some algae can develop specialized, horizontally spreading, stolon-like branches, as in Polysiphonia spp. (Fletcher, 1977a) and Pterosiphonia dendroidea (Neushul et al., 1976). However, for the great majority of algae the colonization of new substrata is commonly achieved by the formation and detachment of "propagules" from the parent 0007-1617/92/030303+ 27 $08.00/0

plant, which are then dispersed via the pelagic zone; very rarely young germlings/ plants have been implicated in the dispersal process (e.g. Laminaria sporophytes: see Moss et al., 1981; Sargassum muticum: see Deysher & Norton, 1982). In many cases, these propagules can take the form of ordinary vegetative fragments which are accidentally released by various environmental agents, such as grazers and wave action (Carlisle et al., 1964; Mshigeni, 1978). Probably small, filamentous algae or portions of algae are commonly dispersed in this way, for example as suggested for Feldmannia simplex (Etherington, 1964), for Codium fragile subspecies tomentosoides (Fletcher et al., 1989) and for Enteromorpha and Ectocarpus fragments released by the mechanical scrubbing of ships' antifouling coatings (Moss & Marsland, 1973). The importance of accidental vegetative dissemination was clearly demonstrated by Clokie & Boney (1980) who entrapped a surprisingly large number of algae using bottle brush collectors. Sometimes, more specialized vegetative propagules are released, e.g. the branched propagules commonly described for species of the brown algal genus Sphacelaria (Prud'homme van Reine, 1982), © 1992 British PhycologicalSociety

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and the red algae Deucalion levrringia and Anisochizus propaguli (Huisman & Kraft, 1982), and the "missiles" described for the red alga Centroceris (Lipkin, 1977). Usually, however, the term propagule refers to reproductive spore bodies of which there are a large number of different types. It is with these spores that the present review is concerned. Particular attention will be given to aspects of their settlement, attachment and establishment. SPORE SETTLEMENT The process of spore settlement can be divided into two sequential stages. These are: locating the substratum and establishing surface contact. Locating the substratum

For the great majority of algae, individual spore bodies are released into the pelagic zone and subsequently distributed, either locally or distally, by water currents. In many cases the release of the spores involves an active discharge mechanism, usually as a result of increased turgor pressure of the mucilage surrounding the spore within each sporangium (e.g. egg release in Tilopteris, Kuhlenkamp & Miiller, 1985; spore release in Laminariales, Toth, 1976b; Maier & Miiller, 1982; spore release in various red algae, Boney, 1975, 1981). In some algae, however, the reproductive spores are distributed whilst still attached to the parental plant body. For example, portions of blade with reproductive sori are reported to be shed from the erect blades of the bull kelp Nereocystis luetkeana which sink to the underlying benthos and then release their spores; the close proximity of the sori to the substratum increase the chances of successful spore settlement and recruitment. Floating portions of fertile algae have also been strongly implicated in the process of spore dispersal, e.g. in Postelsis palmaeformis (Dayton, 1973), Cystoseira osmundica (Schiel, 1985) and Sargassum muticum (Deysher & Norton, 1982) and are described

as ideal vectors for long distance travel (Dayton, 1973; Deysher & Norton, 1982) along with algal propagules (Lipkin, 1977). Spore release is then usually accomplished in close proximity to a substratum, either when the fertile portion becomes caught up or is isolated in an intertidal pool. The considerable geographical spread of Sargassum muticum along the northwestern coast of North America was attributed to the release of floating vegetative fragments which became fertile en route and subsequently released viable zygotes. Certainly there is increasing evidence that "drift dispersal" of algae can play an important role in the colonization of new substrata (Fager, 1971; den Hock, 1987). For example, spore dispersal by drift algae was considered to be responsible for recruitment of a number of species onto test panels placed in Macrocystis beds (Neushul et al., 1976) as well as for the colonization of isolated rocky outcrops (Fager, 1971); it might also play a role in the colonization of offshore oil and gas platforms (Hardy, 1981; Moss et al., 1981). Finally an increasing number of reports are implicating animals in the spore dispersal process. For example, spores can be transported on the legs of some amphipods (Buschmann & Bravo, 1990) and, together with vegetative fragments, are reported to survive digestion by fish and molluscs (Buschmann & Bravo, 1990; Santelices & Paya, 1989). Advantages offered to spores in faecal pellets include a faster sinking rate, an early establishment due to the sticky nature of the faeces and protection from desiccation in intertidal habitats. Following their release from either attached or drifting portions of algae and subsequent dispersal, it is necessary for the spores to re-enter the benthic boundary layer. In view of the small, usually microscopic dimensions of the spores, and the large volume and dilution factor of the surrounding water, this does appear to be a difficult task and in many respects this is suitably reflected in the excessive and apparently wasteful reproductive spore output

Settlement of algal spores

reported in genera such as Laminaria and Macrocystis. In general, it is likely that successful colonization is achieved under conditions of limited dispersal and/or minimal water current activity. Both these factors ensure an early location of the benthic boundary layer and, potentially, an early settlement by the spores. Pertinent to this proposal are reports of spores/ propagules losing their capacity for attachment with time (Deysher & Norton, 1982). It is also important that the settling spores obtain and maintain substratum surface contact: a number of workers, for example, have reported germting colonization to be inhibited by previously established algal communities (Deysher & Norton, 1982; McCourt, 1984), possibly because of their barrier effect (McCourt, 1984), canopy characteristics (Brawley & Johnson, 1991) or by sweeping clear the substratum (Ang, 1985). However, some studies suggest that an algal turf favours algal recruitment (Hruby & Norton, 1979) possibly by offering a refuge from water displacement and by entrapping zygotes. Once the spores are in close contact with the substratum they reveal a number of adaptive features relating to the colonization process including mobility and tactile responses. Spore motility. A particular characteristic of

the large majority of green and brown algal spores is their motility, which is accomplished by the emergence from the spore body of variously numbered, sized, positioned and structured hair-like flagella. Depending on the species and spore type, motility can be either sluggish or active, and maintained for either long or short periods e.g. up to, and for at least, 24 h in Ectocarpus (Baker, 1971) and Laminariales (Henry & Cole, 1982) respectively, 8 days in gametes of Enteromorpha (Jones & Babb, 1968). The period of motility appears to be determined by environmental conditions such as temperature and salinity (Christie & Shaw, 1968; Jones & Babb, 1968; Christie, 1973) which will likewise determine the ability of spores to settle (Christie & Shaw, 1968;

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Christie, 1973). It is unlikely, however, that spore motility plays a major role in the location of the substratum except in very close proximity to the surface and under conditions of very reduced water movement (Chamberlain, 1976). In the majority of benthic macroalgae, however, the spores are non-motile. These include representatives from the brown algae (e.g. the monospores of Acinetospora and Tilopteris, the tetraspores of Dictyota and Padina and the multicellular embryospores of Sargassum) as well as representatives from the green algae (e.g. the aplanospores of Ulothrix and the mitospores of Prasiola). More significantly, however, all the spores of red algae are non flagellate, with motility only sometimes expressed as a very slight amoeboid movement (Lin et al., 1975). For all the above, algal dispersal is a wholly passive process. However, spores do vary in their sinking rate as determined by size and density, with large spores generally sinking faster than small spores (Okuda & Neushul, 1981). These correlations were particularly well demonstrated in several red algae by both Coon etal. (1973) and Okuda & Neushul (1981). It is also likely that the outer halo of residual mucilage observed around red algal spores and whether the spores are released singly or in groups (as for example the release of Fucus eggs in packets) will influence the frictional drag and modify the settlement rate (Coon et al., 1973; Boney, 1975, 198l; Chamberlain, 1976; Hoffman, 1987). Similarly, Schonbeck & Norton (1979) referred to the oogonial sheaths around Pelvetia zygotes providing more buoyancy. Supporting evidence for differential settlement rates of algal spores and their influence on dispersal capability was provided by Amsler & Searles (1980) who found differences in the vertical distribution of seaweed spores in coastal waters; they suggested these differences indicated differences in evolutionary tactics of spore dispersal. Certainly the relatively large and dense embryospores of Sargassum, for example, sink rapidly ( > 0.5mm s 1; Deysher & Norton, 1982) compared to the

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Correa et al. (1987) suggested that spores of endophytes gain entry into Chondrus near apices where the cuticle has been disrupted by growth. In many circumstances this apparent preference for rough surfaces may well be due to the greater protection (and, therefore, survival) given to the algae against adverse environmental conditions (see later). However, there is evidence from laboratory based experimental studies that algae do preferentially settle on roughened surfaces. This has been demonstrated for example, for the motile spores of the brown algae Ectocarpus (Miiller, 1964; Russell & Morris, 1971; Clitheroe & Evans, 1975) and Chorda filum (South & Burrows, 1967) and the green alga Enteromorpha (Christie & Shaw, 1968; Christie, 1973). This ability to detect surface profiles was reported by Christie (1973) to be lost with time in Enteromorpha. Not all algae, however, demonstrate this preference Tactile responses of motile spores. Particularly pertinent to the process of settle- for roughened surfaces. An indifference to ment of algal spores is their ability to detect surface texture was demonstrated for settling and respond to environmental conditions zoospores of Ulva fasciata (Subbaramaiah, 1970) and Ectocarpus (Baker, 1971), whilst which favour their subsequent survival. Probably the best known responses are to Linskens (1966) demonstrated that the surface topography (thigmotactic response) preference of different algae differed widely, and light (phototactic response); lesser with some algae such as Enteromorpha known influences include surface chemistry Porphyra, Nitophyllum and Ectocarpus siliculosus preferring rough surfaces but and surface energy. Ectocarpus fasiculatus and Polysiphonia (1) Thigmotactic response. On the basis of preferring smooth surfaces. Variation in field observations, a number of authors have response to surface texture can also occur in reported that algae generally prefer to different spore types within a single species colonize roughened surfaces compared to (Linskens, 1966). For example, whilst smooth (Ogata, 1953; den Hartog, 1959; gametes of Acetabularia selected smooth Nienhuis, 1969; Harlin, 1974; Foster, 1975; surfaces, quadriflagellate zygotes were indifNeushul et al., 1976; Harlin & Lindbergh, ferent until 12h after fusion and then 1977; Watanuki & Yamamoto, 1990), showed a predilection for rough surfaces. although there are some notable exceptions Differences were similarly shown by Christie e.g. Watanuki & Yamamoto (1990) observed (1973) for different Enteromorpha spore Sargassum to be more abundant on smooth types; whilst zoospores were strongly thigsurfaces whilst Rees (1940) and Tittley motactic, gametes never showed such a (1985a) reported similar findings for response and paired gametes were only mildly thigmotactic. It is also interesting to Porphyra and Btidingia respectively. Similarly, Russell & Veltkamp (1984) note Christie's (1973) observation that zooreported that spores of the brown alga spores released from old fronds, or those Elachista scutulata settle preferentially in the that had been motile for some time, showed cryptostomata of the host alga Himanthalia decreasing thigmotactis. In addition to the above described thigmorather than on the thallus surface whilst

spores of many red algae, thereby increasing their chances of an early and more successful settlement. Indeed, Deysher & Norton (1982) revealed a very restricted embryospore dispersal in S. muticum with the majority arising within 2-3 m of the parent plant. It is doubtful, however, if the size and density of spores play any significant part in the settlement process since very similar and restricted dispersal ranges were described for the much smaller, motile spores of brown algae such as Macroeystis pyrifera (5m: Anderson & North, 1966), Postelsia palmaeformis (1.5-3m: Dayton, 1973), Alaria (10-12m: Sundene, 1962) and Fucus eggs (60m: Burrows & Lodge, 1950). However, Reed et al. ( 1 9 8 8 ) reported that Pterogophora californica spores can be transported at least several kilometres.

Settlement of algal spores

tactic response, the surface profile can exert additional indirect influences on the spore settlement process. It can, for example, influence the water flow over a surface which in turn will determine the degree of sedimentation; layers of sediment are generally detrimental to spore settlement and silt covered top surfaces are often reported to be devoid of algae (Dawson et al., 1960; Clark & Neushul, 1967; Kawashima, 1972; Mshigeni, 1978). By influencing water flow over a surface, the surface profile will also determine the pattern of spore deposition due to the creation of eddies and pockets of reduced water speed (Neushul, 1972; Foster, 1975; Norton & Fetter, 1981; DeNicola & McIntire, 1990)). This is particularly well demonstrated by the so-called "edge effect" of substrata which results in enhanced settlement. For example, Harlin (1973) reported epiphytic cushions of Smithora naiadum growing more abundantly on the margins than on the flat faces of the host sea grasses. A similar preference for the edge of Zostera blades was noted for the colonizing epiphytes Rhodophysema georgii and Audouinella virgatula by Novaczek (1987) and for several other algae on various substrata (Johansen & Austin, 1970; Foster, 1975; Jacobs etal., 1985; Watanuki & Yamamoto, 1990). The influence of "sheltered" and "exposed" regions on algal spore recruitment was particularly well demonstrated by Pearson & Evans (1990) in their experimental studies of Polysiphonia spore settlement on Ascophyllum. These authors attributed the smaller number of spores settling on the vesicles, compared to other regions of the thallus, to the streamlined shape of the former. Certainly there are a number of advantages afforded to spores which have settled on roughened surfaces. These include higher water retention on the surface which will protect the spores from desiccation and provide evaporative cooling in the intertidal region (Gonzalez & Goff, I989b). Such depressions in high intertidal rock appear to attract some species which are usually found lower down on the shore (Saito & Atobe,

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1970). It has been suggested that roughened surfaces will also protect the spores from dislodgement by wave action/water currents/ grazer activity (Norton, 1983; Vadas et al., 1990; Brawley & Johnson, 1991) and, in the case of spores settled on algae, from the skinshedding activities of the hosts e.g. in various brown algae (Filion-Myklebust & Norton, 1981; Moss, 1982; Russell & Veltkamp, 1984), red algae (Gerwick & Lang, 1977; Sieburth & Tootle, 1981; Gonzalez & Goff, 1989b) and green algae (McArthur & Moss, 1977). For example, Pearson & Evans (1990) demonstrated good survival of Polysiphonia spores in lateral pits and wounds of Ascophyllum whilst Watanuki & Yamamoto (1990) refer to surface roughness as being an important contributing factor to the survival of algal communities after initial attachment. The protective role of roughened surfaces was also demonstrated by Russell & Morris (1971) who attached Enteromorpha spores to both roughened and smooth glass slides which they then attached to the hull of a model ship; experimental tows of the model in the Mersey estuary revealed much greater survival for spores attached to the roughened surfaces. Similarly cracks in antifouling paints are reported to protect spores from mechanical brush cleaning procedures (Moss & Marsland, 1973). Finally there are reports of roughened surfaces protecting settled spores/germlings from grazer activity (Lubchenco, 1982). There is also some evidence that the degree of surface roughness can influence the spore settlement process. Neushul et al. (1976), for example, reported that increasing the surface roughness increased the quantity of algae present, this being the result of the increased number of surface planes available for settlement. Similarly a large increase in surface roughness was reported by Foster (1975) to increase Macrocystis pyrifera settlement. However, there is also some evidence that the degree of roughness can determine the type of spore which settles and thus influence the quality of the attached flora. This does suggest that some spores can detect very small differences in surface

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profile and this will determine their settlement pattern. For example, on the basis of field observations, Luther (1976) concluded that Enteromorpha preferred to settle on fine granulated substrata whilst Porphyra purpurea preferred rough granulated substrata. Increasing the irregularity of a surface increased the number of red algae. Although these differences might well relate to differences in survival rather than initial colonization, there does seem ample scope here for further exlzerimental studies. One aspect of the influence of surface roughness on spore settlement which has received attention relates to the differences in spore size shown by different algae. Rees (1940), for example, suggested that the apparent preference shown by the brown algae Pelvetia and Fucus for well roughened surfaces in the field was due to the larger pit sizes being necessary to accommodate the relatively large reproductive oospores. Similarly Pearson & Evans (1990) suggested that the absence of Polysiphonia settlement in the eryptostomata of Fucus was due to the relatively large size of the spores. Conversely it might be expected that algae with relatively small sized spores would find lodgement on surfaces with small pits and in this respect it is interesting to note that Rees (1940) explained the presence of Porphyra on a smooth concrete wall as being due to the relatively small size of the carpospores. Note also that small spores are less likely to be dislodged in the slow moving waters of the more undisturbed laminar sublayer of surfaces (Coon etat., 1973; Okuda & Neushul, 1981), an explanation offered by Houghton et al. (1973) for the apparent ability of Enteromorpha swarmers to settle onto surfaces subjected to water speeds of up to 10.7 knots. Such a relationship between spore size and surface pit size might well explain the ability of some algae to colonize smooth surfaces (for example, Blidingia on concrete: see Tittley 1985a; Lewis, 1964).

(2) Phototactic response. Probably the most widely reported taxis in algae is phototaxis in which the motile stages of algae can appar-

ently detect and respond to variations in light intensity. It has been widely reported for the motile spores of green and brown algae (Smith, 1947; Christie & Shaw, 1968; Moss & Woodhead, 1970; Baker & Evans, 1973a; Christie, 1973) and appears to be related to the settlement process. For example, whilst gametes are generally positively phototactic keeping them suspended in the water column and increasing their chances of gametic union, zoospores and fused gametes are generally negatively phototactic or swim towards areas of low light intensity, increasing their chances of settlement. In the brown algae the phototactic response appears to be associated with the presence of eyespots and swollen basal bodies on the posterior flagellum; algal groups such as the Laminariales in which these organelles are absent do not exhibit phototactic responses (Henry & Cole, 1982).

(3) Chemotactic response. The best known example of a chemotactic response in the macroalgae relates to the production and release of chemical attractants or pheromones by gametes. Although widely described for both green and brown algae they have been particularly well documented and characterized in the brown algae by Miiller and co-workers (Mfiller et al., 1973; Mfiller, 1976; Luning & Mfiller, 1978; M/iller & Luthe, 1981). Attractants can be released by motile gametes whilst in suspension (as in green algae), by motile gametes following settlement (as in many isogamous and anisogamous brown algae) and by non motile, usually oogamous gametes either in situ on the parental alga (e.g. in Laminaria) or whilst freely released into the water column (e.g. Fucus). More recently, however, some interesting work by Amsler & Neushul (1989) revealed other chemotactile responses in macroalgae. They showed that the motile spores of the kelps Macrocystis pyrifera and Pterygophora californica could detect and respond to a variety of inorganic and organic nutrients. This response was time dependent at 2 to 5 hours and 8 to 9 hours after spore

Settlement of algal spores

release. They also suggested that spore chemotaxis and spore settlement stimulation involved different mechanisms. This ability to move along chemical gradients has already been documented in motile bacteria and dinoflagellates (Hauser etaL, 1975; Marshall, 1985). Given that a surface represents a heterogenous matrix of organic and inorganic materials these results suggest that, in the boundary layer at least, spores can actively detect and preferentially settle in microhabitats more nutritionally favourable for growth. Indeed it seems further likely that spores can respond appropriately to a much wider range of surface chemical stimuli, both positive and negative with important and far reaching ecological and applied implications. Chemotaxis might well play a role, for example, in host/epiphyte relationships with host algae preferentially attracting spores of certain epiphytic algae, similar to that reported for brown algae with respect to serpulid larval settlement (KnightJones et al., 1971). It might also play a role in the process of ship fouling, with the toxic boundary layer derived from the slow release of antifouling paint toxins acting as a repellant to potentially settling spores of all but the most resistant algae such as Ectocarpus. Finally it is possible that chemicals influence the spore settlement process via surface contact systems; such chemosensory factors have already been implicated in the recruitment of invertebrate larvae (Morse, 1984, 1985). Dillon et al. (1989) referred to the possible existence of specific biochemical recognition systems operating between Enteromorpha swarmer receptors (at the flagella tips?) and favourable bacteria-filmed surfaces. Similar relationships between bacterial films and the settlement and metamorphosis of a variety of marine invertebrate larvae have already been described (Wilson, 1955; Neumann, 1979; Kirchman et al., 1982; Weiner, 1985) and explain the apparent need for surfaces to be "conditioned" before spore and larval colonization can take place (Raju & Venugopal, 1971; Neushul et al., 1976; Foster, 1980; Ang, 1985, Peterson & Stevenson, 1989).

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(4) Surface free energy. One surface property which has received least attention from workers is the surface free energy, sometimes termed the surface tension or wettability of a surface. Much of the information available relates to the more recent development of low energy, non-stick, antifouling surfaces. Surfaces coated with fluoropolymers (Griffith & Bultman, 1978, 1980; Bultman etal., 1984; Griffith, 1985) and silicone polymers (Miller etal., 1984; Milne & Callow, 1985; Callow etal., 1986, 1988) appear to be especially promising in this respect and are known to support only relatively light fouling. Although the antifouling activity of these coatings is considered to be related to their influence on the adhesive strength of the algae (see later), there is some evidence that they also exert an influence on the spore settlement process. For example, Christie (1973) reported zoospores of Enteromorpha to be reluctant to settle on hydrophobic surfaces and would only do so when pressed into contact with the surface e.g. around the drying out, peripheral regions of the spore droplet or under the weight of a coverslip. As these surfaces are chemically inert it seems likely that a contact phenomenon is operating and it may well be that the unfavourable surface properties are being detected by the algal flagella. Critical surface energy of substrata have also been shown to influence barnacle and bryozoan larval settlement (Eiben, 1976; Rittschof & Costlow, 1989). In view of the wide range of both organic and inorganic materials available in the marine environment, it would be surprising if their expected differences in surface free energy did not play a role in the process of algal spore settlement and colonization. Particularly interesting in this respect were the studies by Linskens (1963) who revealed quite marked differences in the surface tension properties of the thalli of various algae and indeed differences on parts of the same algal thallus (ranging from 24 to 354dynes/cm). He suggested that these differences played a determining role in characterizing the type of epiphytes present. As

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for the influence of surface roughness, whether these differences relate to the initial colonization or subsequent attachment and establishment is not clear (see later). Note that the surface energy properties of gorgonians have already been implicated in primary film inhibition (Davies et al., 1989). SPORE A T T A C H M E N T Observations on the spore attachment process

Two stages can be distinguished in the spore attachment process. These are: initial attachment and permanent attachment. Initial attachment

As suggested above, the flagella of motile spores play an important role in the settlement process, assisting in the passage of the spore to the boundary surface layer and through variously described spinning and vibratory actions (South & Burrows, 1967; Christie & Shaw, 1968; Toth, 1976a; Fletcher & Peters, 1981) undertaking a degree of site selection by the probing activity of their flagella (Amsler & Neushul, 1989; Russell, 1971) and then positioning the spore correctly in relation to the substratum (e.g. anterior end down in Enteromorpha (Evans & Christie, 1970; Christie & Shaw, 1968; Gunn et al., 1984), Chareium (Lee & Bold, 1974) and Chorda filum (South & Burrows, 1967). However there is further evidence that flagella have adhesive properties at their tip and that they provide the first stages in the spore attachment process; Henry & Cole (1982) occasionally saw clumps of mastigonemes on the long whiplash of the anterior flagellum of some Laminariales which indicated it has adhesive properties. Toth (1976a) and Fletcher & Peters (1981) observed the flagella adhere to the surface in Chorda and Urospora respectively whilst Gunn et al. (1984) considered it likely that a

weak initial attachment was accomplished by the flagella of spores of Enteromorpha. If good adhesion between the flagella and substratum is achieved, this will stabilize the spore body and bring it into direct contact with the substratum surface. Spore/ substratum contact would be further increased during the process of flagella adsorption/axoneme retraction with the spores drawn laterally down as in Chorda (Toth, 1976a; Henry & Cole, 1982) or at the anterior poles as in Enteromorpha (Evans & Christie, 1970) and Urospora (Fletcher & Peters, 1981). [It is also possible that extracellular residual mucilage present on the spore surface, as described for Ulva zoospores by Braten (1975), might mediate initial adhesion.] An essential aspect of the above processes is, therefore, the required compatability between the flagella and the substratum surface and this might well account for the above described influential role played, by surface properties such as free energy and topography on the settlement process. Once spore body/surface contact has been achieved by the flagella, it is further likely that their mutual compatibility will determine if permanent attachment is achieved. Whilst considered to play only a minor role in the initial adhesion of motile spores (see above), the presence of residual surface mucilage is likely to be an important factor in the adhesion of the non-motile red algal spores. Certainly it is a common and very tenacious component of red algal spores (Boney, 1975, 1981; Ngan & Price, 1979) and can be clearly seen under the light microscope using indian ink preparations. The trailing character of this mucilage during spore movement and its adhesive sticky nature enhances entrapment and provides an early attachment mechanism. In this respect, the copious production of mucilage around Jania spores compared with the smaller quantities around Corallina spores is con-

FIG. 1. Transmissionelectron micrograph(TEM) of part of a young maturingcarpospore of Polysiphonia urceolata showing a large Golgi body (G) producing vesicles (V) with reticulate contents. The latter contribute to the large vacuole-like vesicle (VV). Note the florideanstarch grains (F). Scale bar = 0-5 ~tm.

Settlement of algal spores

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sidered to be related to the epiphytic mode of the former and the requirement for an earlier more rapid establishment on a short lived host. Maggs & Cheney (1990) also suggested that the sticky mucilaginous plug surrounding Chondrus spores probably promoted sporeling coalescence and contributed to the longevity of the plant. As suggested for flagella, it is likely that the successful adhesion of this mucilage, and therefore the spo;e body to the surface, will be determined by aspects of surface compatibility.

Permanent attachment

Following the above described initial attachment process, all spores actively secrete an adhesive material. This material is discharged through the plasma membrane in the region of substratum-surface contact. In settled Enteromorpha spores it was observed initially around the pointed anterior part (Evans & Christie, 1970; Braten, 1975). It is viscous in nature and spreads out from the spore body to form a distinct mucilaginous pad, particularly copious and prominent around the base of red algal spores (Chamberlain & Evans, 1973; Chamberlain, 1976). The mucilaginous pad is frequently described as hyaline in the proximal region but reticulate and fibrillar in the distal region (Chamberlain, 1976). In Ceramium spores, adhesive liberation was reported to be light independent but took longer at low temperatures due to possible increase in viscosity; once released the glue was independent of the spores metabolism (Chamberlain, 1976). In some fucalean zygotes, attachment is characterized by a copious secretion of mucilage from the whole surface e.g. in Ascophyllum (Moss, 1975); however the derivation of this material is different to that described for spores (see later).

Ultrastructura| studies

A major contribution towards our understanding of the derivation and structure of spore adhesive materials has been obtained from ultrastructural and cytochemicat studies. In this respect particularly notable are the studies of Evans & co-workers on Enteromorpha spore adhesive, this work being initiated in order to provide a better understanding of this alga's role as an important ship fouling organism. Although adhesive production has now been studied in a number of macroalgal species with structurally different spores, the processes of adhesive production appear to essentially follow the same pattern. As described above, two adhesive materials are produced by spores. The first type comprises the residual mucilage which accompanies the spore following its release from the sporangium and which plays a part in the initial attachment process. Ultrastructural studies have revealed this material to be derived from the activity of Golgi bodies during the early stages of spore development within the sporangium (Fig 1). It is fibrillar and electron light in appearance and is transported in small vesicles either directly, or via large vacuoles into the interface between the spore plasmalemma and the sporangial wall (Baker & Evans, 1973a; Chamberlain & Evans, 1973; Chamberlain, 1976: Wetherbee & West, 1977; Scott & Dixon, 1973; Fletcher, 1979; Pueschel & Cole, 1985). This mucilage is also considered to play a role in the release of the spores from their sporangia, usually as a result of hygrostatic swelling upon water contact (Boney, 1981; Toth, 1976b). In many respects this mucilage functions in a similar manner to that reported on the frustules of many diatoms (Daniel et al., '1987) and is similar to the "sticky" yet able to relax cements and mucilaginous secretions (Stefan

FIGS 2-3 TEMs of developingcarpospores in Polysiphoniaurceolata. Fig. 2. Part of a mature carpospore showing a

Golgi body (G) producingelectrondense vesicles(DV). Scalebar = 0.3 gm. Fig. 3. Part of the peripheral regionof a mature carpospore showing two electron dense vesicles(arrows) lyingjust beneath the plasmalemma. These vesicles contain the spore adhesive which is released upon settlement. Scale bar = 0-4 gm.

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adhesion) which are characteristic of animals such as limpets or barnacles (Crisp & Walker, 1985). The Golgi bodies are also responsible for the production of the second, more permanent spore adhesive material during the later stages of spore differentiation (Figs 2, 3). As for residual mucilage production, several Golgi bodies are involved in this activity, these usually anteriorly positioned in the motile green algal spores (Evans & Christie, 1970; Fletcher & Peters, 1981), perinuclear in brown algal spores (Baker & Evans, 1973a, b) but more irregularly positioned in red algal spores (Chamberlain & Evans, 1973; Scott & Dixon, 1973). In structure the vesicles are characteristically electron dense in the centre with a peripheral, electron light, swirled material (Evans & Christie, 1970; Braten, 1975; Chamberlain, 1976; Fletcher, 1979; Oliveira et al., 1980; Henry & Cole, 1982; Clayton, 1984; Pueschel & Cole, 1985). More rarely, they have been described as fibrous (Baker & Evans, 1973a; Toth, 1976a), fibrillar (Loiseaux, 1973; Vesk & Borowitzka, 1984) and plaque-like (Oliveira etal., 1980). Vesk & Borowitzka (1984) suggest these differences reflect differences in chemical composition. Ultrastructural studies of released spores reveal the vesicles are anteriorly positioned in motile spores but more peripherally positioned just beneath the plasma membrane in red algal spores (Vesk & Borowitzka, 1984; Chamberlain, 1976). Upon spore/substratum contact the vesicles rapidly discharge their contents through the plasma membrane, by a reverse pinocytosis mechanism, to give rise to the adhesive pad.

Composition of adhesive and mechanism of adhesion

Studies on the composition of adhesive produced by algal propagules are limited by the availability of material for chemical analysis. Histochemical staining has indicated that the permanent adhesives of

green, brown and red algal spores are glycoproteins viz. polysaccharide-protein complexes, as shown in Enteromorpha (Callow & Evans, 1974), Ulva (Braten, 1975), Ectocarpus (Baker & Evans, 1973a,b; Clitheroe, 1977), Ceramium (Chamberlain & Evans, 1973, 1981) and Palmaria (Pueschel, 1979). This adhesive appears to differ from that involved in the initial attachment of red algal spores which is largely polysaccharide in composition (Chamberlain & Evans, 1973; Scott & Dixon, 1973). Hosing experiments designed to test the strength of adhesion of spores to glass slides also led Christie et al. (1970) to conclude that Enteromorpha zoospore adhesive was a glycoprotein since weakening occurred when attached spores were treated with the proteolytic enzymes trypsin and pronase and the carbohydrase enzyme a-amylase. These studies indicate that the adhesive of macroalgal spores are more ~omplex than the different types of substituted acidic polysaccharides produced by diatoms (Chamberlain, 1976; Daniel et al., 1987) and marine bacteria (Fletcher & Floodgate, 1973). EM autoradiography indicated that the protein component was synthesized in the ER found subtending the forming face of the Golgi bodies whilst the carbohydrate component was added later probably within the vesicles after detachment from the Golgi bodies (Callow & Evans, 1974). Once released from the spore, an essential requirement for the adhesive material is that it spreads and forms a strong bond with the substratum. Compatibility with the substratum surface is, therefore, fundamental to the attachment process and it might be expected that the surface characteristics of the substratum would play an important influential role. Certainly the degree of roughness would be important because this would determine the number of surface planes available to the spore adhesive. Probably the surface free energy is also important and this finds support in the reports of Goldsborough & Hickman (1991) (freshwater studies), Thomas & Allsopp (1983) and Dillon etal. (1989) (marine

Settlement of algal spores

studies). The latter authors recorded much greater numbers of Enteromorpha swarmers attaching to polystyrene surfaces filmed by some bacteria compared to those that were unfilmed. They attributed this to the higher surface energy properties of the filmed surfaces stabilizing the adhesive and increasing the adhesive strength of the spores. Similarly Norton (1983) reported that the presence of a bacterial film on a surface enhanced the attachment tenacity of Sargassum muticum propagules. The report of Thomas & Allsopp that some bacterial films composed of a single species can either increase or decrease Enteromorpha swarmer adhesion to glass surfaces is explained by the preferential effectiveness of the bacteria to change the surface energy of the substratum. A very similar relationship has been demonstrated between the surface energy properties of a substratum and bacterial attachment (Dexter et al., 1975; Dexter, 1976; Fletcher & Loeb, 1979; Hamilton & Duthie, 1984; Fletcher & Pringle, 1985). However, it is possible that some marine bacteria produce specific molecules that enhance spore attachment, as demonstrated for the adhesion of Chlorella cells to glass (Tosteson & Corpe, 1975; Iman etal., 1984; Tosteson etal., 1985). Possibly both systems (attachment enhancing molecules and adhesion stabilizing surface energies) are operating, as suggested for Enteromorpha spores by Dillon et al. (1989). The ecological implications of "stabilizing" the spore adhesive were highlighted by Peterson & Stevenson's (1989) observation that conditioning films enhanced spore attachment in conditions of fast water current flow. One interesting aspect of the adhesive mechanism is that the adhesive seems to undergo a chemical bonding or "curing" which increases the strength of the adhesion. This finds support in reports showing increased attachment strength with time (Christie et al., 1970, 1975; Baker, 1971; Russell & Morris, 1971; Charters etal., 1973; Christie, 1 9 7 3 ; Braten, 1975; Chamberlain, 1976; Gunn etal., 1984). Chamberlain (1976) reported this curing

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process to take 36 h in Ceramium. Also, whilst the Enteromorpha glue is initially susceptible to proteolytic attack, after 2 h the majority of spores cannot be dislodged (Christie et al., 1970). This hardening of the adhesive may be due to a polymerization or cross-linking process (Chamberlain, 1976; Jones et al., 1982). In brown algae this could be the result of the protein constituent being tanned by polyphenol compounds (Baker, 1971); in red algal spores, calcium influenced cross-linkage of the adhesive has been suggested (Jones et al., 1982). Work by Moorjani & Jones (1972) suggests that algae might differ in the speed of their respective curing processes and this might have ecological implications. For example the more rapid and stronger attachment of Jania compared to Corallina was considered to be a function of the epiphytic life mode of the former. Differences in spore attachment speeds for Microcladia coulteri and M. californica were also related to their respective basiphyte range by Gonzales & Goff (1989a). These findings do not preclude the suggestion by Gunn et al. (1984) that the increase in attachment strength recorded with increasing settlement time up to 60 mins. could be related to an increased production and outward spread of the adhesive. Finally it is perhaps pertinent to add that the above adhesives described for motile green and brown algal spores and nonmotile red algal spores do not represent the total range of adhesive mechanisms present in the algae. In the higher fucalean algae e.g. Fucus, no specialized adhesive material is formed. Following sperm entry into the egg a cell wall of alginic acid is immediately secreted. A number of post-fertilization changes then take place including the secretion of other cell wall polymers, particularly sulphated fucans which are thought to be instrumental in anchoring the zygote to the substratum (Evans et al., 1982). Similarly the adhesion of Halidrys zygotes to the substratum is described as being due to the very rapid production of a zygote wall and associated mucilages (Hardy & Moss, 1978).

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SPORE E S T A B L I S H M E N T Once firmly anchored to the substratum the spore undergoes the process of "establishment". Essentially this comprises 4 stages. These are: cell wall formation, establishment of polarity, spore germination, primary rhizoid growth and adhesion. Cell wall formation

Following attachment, the spore commonly secretes an enveloping wall (Figs 4, 5). Although the process of wall formation and the structural components will vary for different species it is usually a fairly rapid process and accomplished in a matter of a few hours. For example, Evans & Christie (1970) recorded a wall 2 0 0 n m thick in Enteromorpha spores after only 4 hours settlement. The wall material appears to be derived from the contents of small, fibrous

vesicles which are released through the plasma membrane. As for the spore adhesive, scattered Golgi bodies are attributed with the formation of this material. However, unlike the polarized release of the spore adhesive, the cell wall material is evenly distributed all round the spore periphery. Once laid down, the wall probably offers increased protection to the attached spore from adverse environmental conditions, including, for example, the toxic activity of antifouling paints (Christie, 1973; Christie et al., 1975).

Establishment of polarity

Prior to germination, a polarity is established within the spore cell in order to allow the differentiation of the two growth axes responsible for the development of the basal and erect shoots. This process has been

FIGS 4-7. Post settlement development in carpospores of Polysiphonia elongata. Fig. 4. Newly settled carpospore. Scale bar = 18 p.m. Fig. 5. Settled carpospore with enclosing cell wall. Scale bar = 16 p~m.Figs. 6-7 Germinating carpospores. Note basal adhesive pad in Fig. 7 (scanning electron micrograph, SEM). Fig. 6, scale bar = 18 ~m. Fig. 7, scale bar = 16 p.m.

Settlement of algal spores

particularly well reviewed in Fucus zygotes by Quatrano (1978) and Evans et al. (1982). Essentially it involves the induction of a polarized state within the spore body by various vectors such as light which results in a redistribution of organelles. Once these organelles have been relocated, the spore cell undergoes the process of cell division/ germination. A similar spatial redistribution of organelles have been described for other algae (Jones & Jones, 1986; Evans & Christie, 1970). Spore germination

In the majority of macroalgae investigated, spore germination proceeds soon after attachment with no obvious resting stages apparent (Figs 6-13). Occasionally, however, the process can be delayed or staggered within a population (Moss, 1973; Charnofsky et al., 1982) whilst after initial establishment, sometimes dormancy can occur, e.g. in Dictyota (Richardson, 1979). From the viewpoint of successful establishment, there would be obvious advantages for algae with a rapid germination process, and it is interesting to note that the rapidly formed early-branched and mucilaginous germ tube of Porphyra carpospores was considered by Rees (1935) to be an adaptation to the alga's early establishment on newly laid smooth concrete surfaces. Although a wide range of germination patterns have been described, in most algae studied there is an initial protrusion and growth of one or more rhizoidal initials from the basal region of the spore cell; soon after, erect shoot/ filament growth occurs from the opposite pole axis. It is the processes of rhizoid formation and attachment which concern us here and these have been particularly well studied in Fueus by Quatrano and coworkers. For example, twelve hours after fertilization the perinuclear region becomes highly polarized with finger-like projections radiating towards the presumptive rhizoidal part of the cell. In the area of rhizoid formation are many mitochondria, ribosomes, densely fibrillar vesicles and hypertrophied

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Golgi bodies. The pole associated with thallus growth, on the other hand, contains chloroplasts and vesicles. Following nuclear division at approximately 20 hours after fertilization the smaller rhizoid daughter cell contains numerous mitochondria and Golgi bodies with associated vesicles. One of the cytoplasmic components which becomes localized in the expression of polarity is a sulphated fucan called F2. Fucan F2 is produced in the Golgi and is directionally transported to the rhizoidal pole in vesicles which require the presence of an actin cytoskeleton. Fucan F2 becomes localized in the rhizoid wall by 16 hours after fertilization (Evans et al., 1982) where it is instrumental in anchoring the rhizoid to the substratum (Quatrano, 1 9 7 8 ) . Recent evidence (Quatrano, 1990a, b) suggests involvement of transmembrane linkages between the cytoskeleton and cell wall forming an axix stabilizing complex (ASC). The tip of the rhizoid is the main attachment site and Quatrano has proposed a similar mechanism for Fucus to the elaborations of the plasma membrane on animal cells at the site of adhesion to the substratum (see Burridge et al., 1988). In animal cells, regions of the plasmamembrane known as focal adhesions or focal contacts represent transmembrane connections between the cytoskeleton and the cell wall and a number of focal adhesions have been characterized. The adhesive glycoproteins fibronectin or vitronectin are components on the external side of the plasma membrane; integrins are internal plasma membrane components while actin and associated proteins are located on the internal side of the plasmamembrane. In Fucus an actin network is necessary for directional transport of vesicles containing fucan F2 to the rhizoid tip (Brawley & Robinson, 1985; Kropf et al., 1989). More recently, Quatrano (pers commun.) has shown that a vitronectin-like protein is present in Fucus zygotes; first localized around the nucleus, then as the rhizoid forms it moves toward the rhizoid end becoming localized in the extracellular matrix of the rhizoid cell wall. Sulphation of fucan F2 is required both for

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Settlement of algal spores its directional transport to the rhizoid tip and for that of vitronectin suggesting that both may be co-localized in Golgi-derived vesicles. Such exciting information opens up new ideas on the complexity of rhizoid attachment in algae and the possibility that focal adhesions are instrumental in the process makes previous discussions of mechanisms of adhesion in the aquatic environment appear too simplistic. Primary rhizoid growth and adhesion The primary function of the rhizoid initial cell is to produce an attachment system capable of securing the developing young erect thallus. Continued growth of the latter requires the production of secondary rhizoids which originate from either basally positioned vegetative cells or from highly specialized attachment organs such as haptera (Figs 14, 15) (Fletcher, 1977a). The role of rhizoids is to increase the area of surface-substratum contact and form a strong adhesive bond; sometimes they are also involved in new erect shoot production. To assist with these functions rhizoids show a number of adaptive features including apical growth, frequent branch formation, negative phototropism, positive geotropism, positive thigmotaxis, morphological plasticity allowing them to adapt to variable pit sizes, physiological hardiness and the secretion of a peripheral mucilaginous adhesive material (Figs 11, 13) (Moss, 1973, 1975; Moss et al., 1973; Braten, 1975; Fletcher, 1976, 1977a, 1980; Tovey & Moss, 1978; Hardy & Moss, 1978, 1979; Fletcher & Peters, 1981; Norton, 1983; Polne-Fuller & Gibor, 1990). Little is known about the derivation and composition o f this mucilage. It appears to originate from Golgi derived

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vesicles which have accumulated at the tip (Braten, 1975; Fletcher, 1976, 1981) and represents the outer amorphous cell wall layer. Histochemical studies on the rhizoid adhesive of Ulva by Braten (1975) demonstrated a polysaccharide/protein complex. Algae vary quite widely in their process of attachment and there is some evidence this may be related to their mode of life style. For example, Moorjani & Jones (1972) observed differences in the development of Jania and Corallina; the limited basal development and early axis initiation in Jania only, reflected its epiphytic mode. Similarly Jones & Duerden (1972) described two attachment forms of Ceramium which they related to either the epilithic or epiphytic modes (see also Gonzalez & Goff, 1989a, b). The latter authors revealed the early germination patterns of algae to determine their success as epiphytes. For example, the immediate penetrating growth of Myriocladia coulterii as distinct from the discoid development in M. californica enhanced success of the former as an epiphyte. Whilst the formation and growth of the rhizoids is dependent on environmental conditions such as temperature, salinity etc, (Nagata, 1973; Fletcher, 1980; Cecere et at., 1991; Seoane-Camba, 1989) they also appear to be strongly influenced by the nature of the substratum. In this respect particularly significant are features such as the topography, surface energy and surface chemistry of the substrata. Topography. In addition to determining patterns of spore settlement, there is much evidence that the surface topography of a substratum can influence the subsequent establishment of the plants. It has been widely reported, for example, that rough-

FIGS 8-15. Developmental stages of marine algal spores. Figs 8-9. Germinating carpospores of Polysiphonia urceotata showing basal emergenceof rhizoidal filament. Scalebars = 20 iam. Fig. 10. Young germlingof Ceramium rubrum with discoid attachment base. Scalebar = 70 iam. Fig. 11. SEM of part of an attachment disc of Polysiphonia urceolata showing firm adhesion to substratum. Scalebar = 10 gm. Fig. 12. Germinating embryosporeof Sargassum muticum showing emergent rhizoidal filaments. Scale bar = 35 gm. Fig. 13. SEM of part of two rhizoidal filaments of Sargassum muticum showing underlyingadhesive. Scale bar = 10/am. Figs 14-15. Secondaryrhizoid production from vegetativecells in Polysiphonia sp. (Fig. 14) and Urosporapenicilliformis (Fig. 15). Scalebar = 48 p.m (Fig. 14), 14 lam (Fig. 15).

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ened surfaces support more dense growths of macroalgae than smooth surfaces, probably by increasing the number of surface planes available for attachment and by allowing greater penetration of the surface layers by the rhizoids (Foster, 1975; Neushul et al., 1976; Harlin & Lindbergh, 1977; DeNicola & McIntire, 1990). Both these factors will enhance the adhesive strength of the plants and reduce the chances of removal by wave and current action, By influencing local water circulation, changes in topography could also determine the renewal rate of nutrients with implications for growth and photosynthesis (Neushul, 1972; Foster, 1975). By entrapping more water in the surface layers, roughened surfaces will also protect the rhizoids of intertidal plants from desiccation during unfavourable periods. Indeed, the capacity for water retention was considered by Nienhuis (1969) to be the determining factor behind the influence of surface topography on plant survival in the intertidal and on the zonation patterns and heights of algae observed by himself and den Hartog (1959). Similarly, Brawley & Johnson (1991) concluded that desiccation was the most important stress to newly settled embryos of Pelvetia. There is also some evidence from experimental studies that surface topography can influence the composition of the attached flora. Harlin & Lindbergh (1977), for example, reported differences in the floristic composition of intertidally placed discs to which were cemented different sized quartz particles. Similar findings were reported by Luther (1976) and Stephenson (1961) who exposed different types of natural stone substrata; the latter author reported the brown crustose alga Ralfsia developed on hard rock whereas the fine, erect bladed Blidingia developed on soft rock. These results find support in numerous field reports of different rock types supporting different algae/algal communities, often when in close proximity to each other (Rees, 1935, 1940; den Hartog, 1959, 1972; Stephenson & Searles, 1960; Stephenson, 1961; Lewis, 1964; Nienhuis, 1969; Wynne, 1969; Fletcher, 1977b, 1978;

Kornmann & Sahling, 1977; Tittley & Price, 1977a, b, 1978; Tittley, 1985a, b, 1986; DeNicola & McIntire, 1990). Such differences are particularly evident in the upper intertidal regions and on sheltered coasts (Nienhuis, 1969); differences in ftoristic composition are less evident on exposed coasts and in lower intertidal regions (Boalch, 1957; Foster, 1975). As suggested earlier, these floristic differences could be based on differences in initial spore settlement patterns, and/or plant survival rates in the different microhabitats provided by the substrata. However, it is possible that they could be related to aspects of the plant attachment process. It is particularly well known that friable rocks offer poor substrata for algal growth. For example, McLachlan et al. (1987) refer to the absence of a stable canopy of laminarians on friable sandstone, Parker & McLachlan (1990) refer to Phymatolithon stabilizing the rock surface and allowing Chondrus populations to recruit whilst Moss et al. (1973) refer to magnesium limestone stones as being too friable for Himanthalia establishment. There is also some evidence that different rock types can influence the development and adhesive properties of the attachment cells/ rhizoids. Seoane-Camba (1989), for example, reported rhizoids to behave differently according to the substratum type, with Gelidium producing cement only in contact with crystalized limestone and not glass or plastic. Similarly, Harlin & Lindbergh (1977) showed that Corallina developed differently on surfaces made up of different sized particles with much larger, spreading crusts lacking upright shoots developing on the fine particle size surfaces. Two different pathways of rhizoid development, i.e. discs or filaments were also reported by Woods and Fletcher (unpub.) for Polysiphonia germlings grown on coarse and finely roughened glass slides; a much greater number of plants developed discs on the roughened surface compared to the smooth. Rhizoids of different morphology were also described for germlings of various algae on surfaces of different texture by Moss et al. (1973), Moss

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FIGS 16-21. Development of attachment systems in some marine algae. Figs 16-17. Zoospore cultures of Ulva lactuca. Fig. 16. Filamentous attachment base of a 12 day o l d germling grown on a low energy surface. Scale bar = 55 p.m. Fig. 17. Disc-like attachment base of a 12 day old germling grown on a high energy surface. Scale bar = 33 p.m, Figs 18-19. Tetraspore cultures of Polysiphonia brodiaei. Fig. 18. Filamentous base of a 6 day old germling grown on a high energy surface. Scale bar = 40 p.m. Fig. 19. Discoid base o f a 6 day old germling grown on a low energy surface. Scale bar = 40 p.m. Figs 20-21. Tetraspore cultures of Grateloupia doryphora. Fig. 20. Knot-filament development in a 14 day old germling grown on a low energy surface. Scale bar = 50 pm. Fig. 21. Discoid development in a 14 day old germling grown on a high energy surface. Scale bar = 26 lam.

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(1975) Tovey & Moss (1978) and Hardy & Moss (1979). Surface energy. Particularly interesting, but

seldom investigated from an algal attachment point of view, is the surface free energy of a surface. Certainly surface energy properties have been reported to modify the morphogenesis of algal attachment systems with important implications for their adhesive strength. For example, Hardy & Moss (1979) reported the primary rhizoid of Fucus germlings to grow long and thin on low energy Teflon surfaces and were unable to form a secure attachment. Fletcher (1976), Fletcher & Baier (1984) and Fletcher et al. (1984, 1985) grew germlings of a range of green, brown and red algae on surfaces varying in surface energy and revealed marked differences in the extent of outward growth, morphogenetic appearance and adhesive strength of the rhizoids in each alga (Figs 1621). For example, the rhizoids of Enteromorpha and Ulva germlings were found to bond more strongly to high energy surface coatings compared to low energy surface coatings. In addition the response obtained differed for different algae e.g. attachment discs were produced on high surface energies in Enteromorpha but on low surface energies in Polysiphonia (Figs 18, 19). The surface energy of a substratum was also shown by Fletcher et al. (1985) to determine the morphogenesis of the discoid and crustose growth forms in some algae, these providing much firmer establishment than the so-called knot filament growth form reported in laboratory cultures of algae such as Petrocelis hennedyii (Fletcher & Irvine, 1987), Petalonia/Scytosiphon (Fletcher, 1976) and Rhodophysema elegans (Fletcher, 1977c) Figs 20, 21). Note that two pathways of development (discoid and semifilamentous) were also described for Chondrus crispus by Chen & Taylor (1976) which appeared to be determined by the formation and firm adhesion of a blanket-like, extracellular mucilaginous sheath during early ontogeny of the sporelings. As for spore attachment, the morphological expression of the rhizoids

on the different surface energies was determined by the degree of surface contact, with slight pressure resulting in the crustose growth form (Fletcher, 1976, 1977c). In view of the wide range of substrata available to algae for colonization and likely range of surface energy properties and how these influence attachment strength of algae, it is possible that this property plays a greater role in colonization than previously thought. Surface chemistry. Very little is also known about the role of surface chemistry in the attachment of algae. Generally the chemistry of a substratum is considered to play only a minor role in determining algae community structure (den Hartog, 1959; Tittley, 1986) although there is some evidence that heteroantagonism between algae can occur (Russell & Fielding, 1974; Fletcher, 1975; Schonbeck & Norton, 1979; Huang & Boney, 1984) possibly involving the release of antibiotic compounds and that this can control basal growth and development of neighbouring algae (Fletcher, 1975). Gonzalez & Goff (1989b) also considered that released chemical compounds from certain basiphytes might limit epiphyte growth whilst Harlin (1973) suggested that differences in the chemistry of seaweeds and grasses influenced the epiphytic flora. Certainly tannin-like substances released from brown algae are known to have anti-fouling properties (Sieburth & Conover, 1965, 1966; Conover & Sieburth, 1966; Sieburth & Tootle, 1981). Most work on this subject, however, relates to the toxic nature of some artificial surfaces. For example, newly laid concrete usually remains uncolonized probably because of the high leaching rate of alkaline ions (Foster, 1980). Similarly, ship antifouling paints, based on the release of toxic ions from copper and organotin compounds, or compounds such as copper and organotins, also restrict algal growth but at the same time influence the floristic composition. Probably the best known example of this is the occurrence of a very restricted flora on toxic surfaces which is usually dominated by algae such as Ectocarpus, Enteromorpha and

Settlement of algal spores

Ulothrix. In addition, these algae often occur in a reduced growth form, characterized by prostrate rather than erect axis development. Particularly interesting is the not uncommon occurrence of small epiphytic and endophytic algae on the toxic surfaces as well as restricted expressions of morphological growth forms (Rautenberg, 1960; Fletcher, 1983, 1988). REFERENCES AMSLER, C. D. & NEUSHUL, M. (1989). Chemostatie effects of nutrients on spores of the kelps Macrocystis pyrifera and Pterygophora californica. Mar. Biol. (Berl.), 102: 557-564. AMSLER, C. C. & SEARLES, R. B. (1980). Vertical distribution of seaweed spores in a water column offshore of North Carolina. J. Phycol., 16: 617 619. ANDERSON, E. K. & NORTH W. J. (1966). In situ studies of spore induction and dispersal in the giant kelp Macrocystis. In Proe. Fifth Int. Seaweed Syrup., 73-86. Pergamon Press. ANG, P. O. (1985). Studies on the recruitment of Sargassum spp. (Fucales, Phaeophyta) in Balibago, Calatagan, Philippines). J. exp. mar. Biol. Ecol., 91: 293-301. BAKER, J. (1971). Studies on the ship fouling alga Eetocarpus. Ph.D. thesis, Dept. of Plant Sciences. University of Leeds. BAKER, J. R. & EVANS, L. V. (1973a). The ship fouling alga Ectocarpus. I. Ultrastructure and cytochemistry of plurilocular reproductive structures. Protoplasma, 77:1 13. BAKER, J. R. & EVANS, L. V. (1973b). The ship fouling alga Ectocarpus. II. Ultrastructure of the unilocular reproductive stages. Protoplasma, 77: 181-189. BOALCH, G. T. (1957). Marine algal zonation and substratum in Beer bay, south-east Devon. J. mar biol. Ass. UK., 36:519 528. BONEY, A. D. (1975). Mucilage sheaths of spores of red algae. J. mar. biol. Ass. UK., 55:511 518. BONEY, A. D. (1981). Mucilage: the ubiquitous algal attribute. Br. phycol. J., 16: 115-132. BRATEN, T. (1975). Observations on mechanisms of attachment in the green alga Ulva mutabilis Foyn. Protoplasma, 84:161 173. BRAWLEY, S. H. & JOHNSON, L. E. (1991). Survival of fucoid embryos in the intertidal zone depends upon developmental stage and microhabitat. J. Phycol., 27:179 186. BRAWLEY, S. H. & ROBINSON, K. R. (1985). Cytochlasin treatment disrupts the endogenous currents associated with cell polarization in fucoid zygotes. Studies on the role of F-actin in embryogenesis. J. Cell Biol., 100: 1173-1184. BULTMAN, J. D., GRIFFITH, J. R. & FIELD, D. E. (1984). Fluoropolymer coatings for the marine environment. In Marine Biodeterioration: an interdisciplinary study (Costlow, J. D. & Tipper, R.C., editors), 237-243. US Naval Institute Press, Annapolis.

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(Accepted 23 April 1992)