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MARINE ECOLOGY PROGRESS SERIES Vol. 97: 193-207.1993 Published July 15 Mar. Ecol. Prog. Ser.

REVIEW

Settlement of benthic marine

Sebastian R. Rodriguezl, F. Patricio Ojedal, Nibaldo C. Inestrosa2

'Departamento de Ecologia, 2Departamento de Biologia Celular y Molecular, Facultad de Ciencias Biologicas, Pont. Universidad Catolica de Chile, Casilla 114-D, Santiago, Chile

ABSTRACT:Settlement and recruitment of benthic marine invertebrates are complex processes, deter- mined by the interaction of biotic and abiotic factors which operate at different temporal and spatial scales. This review analyses the settlement process, attempting to integrate aspects related to different levels of organization (i.e. ecological-physiological-molecular). This is important because many factors that act at any of these levels and at different times can explain by themselves the patterns of settle- ment andlor recruitment of a large number of . From an ecological perspective, progress has been made in the identification of causal factors of vanations in larval availability for settlement. Many physical and ethological factors that act during settlement have, however, not received much attention. Likewise, since the great majority of settlement studies have been carried out at restricted spatial scales, fewer works consider different biological and physical factors acting at different scales simulta- neously. Settlement patterns are frequently inferred from recruitment. In this sense, a density-indepen- dent action of post-settlement mortality has been cons~deredas prerequisite for thls type of inference. This has, however, recently been challenged on the basis that settler-recruit and mortality-settler den- sity relationships change in time. At the physiological-molecular level, different settlement-inducing chemical cues have been identified. Those cues have, however, not yet been characterized to under- stand better the signal transduction mechanisms involved in larval responses. It is likely that the ner- vous system is involved. The use of artificial inducers would be useful in studying settlement induction, until more effective natural inducers are isolated and characterized Although few studies have ana- lysed the acquisition of competence, stages of larval development have been related to changes in pro- tein patterns or enzymatic levels of the . An inopportune exposure of larvae to inducers may delay settlement and may even have a negative impact on growth and subsequent survival of juveniles.

INTRODUCTION using closed models to describe population dynamics of benthic marine invertebrates with a great capacity Most benthic marine invertebrates have pelagic of dispersion. Indeed, population models should con- larvae capable of dispersing over great distances sider the possibility of recruitment of individuals from (Thorson 1950). Traditional models have described the other populations and that local could be dynamics of many of these populations as closed followed by recolonization processes. Population mod- systems, according to which the new individuals re- els should describe the dynamics of open populations cruiting inside a given local population are offspring of (e.g. Caswell 1978, Frogner 1980). females present in the same population (Karlson & Roughgarden, Gaines & Pacala (in Lewin 1986) Levitan 1990). These models have assumed that once argued that 'at some scale most ecological systems are one of these populations is extinguished, the situation open systems'; therefore the distinction between open is irrevocable (May & Oster 1976, Caswell 1978). and closed systems is somewhat irrelevant nowadays. Roughgarden et al. (1985) recognized the problem of In contrast, the importance of the source of recruits as

0 Inter-Research 1993 194 Mar.Ecol. Prog. Ser. 97: 193-207, 1993

a determining factor in important processes of marine tlement is one of the main stages in the cultivation of systems and its influence on population structure and commercially important species) prompted us to carry dynamics have been widely discussed (Underwood & out this analysis. This integration consists in the simul- Fairweather 1989). Specifically, over the last years a taneous or alternate consideration of ecological and new interest has arisen in the local variation of settle- physiological factors and processes. The objectives of ment and/or recruitment, and its consequences upon the present review are: (1) to analyze the settlement the distribution and abundance of marine species process as a whole, considering ecological, physiologi- (Grosberg 1982, Keough & Downes 1982, Keough cal and biotechnological aspects, and (2) to suggest 1983, 1984, Victor 1983, Underwood & Denley 1984, future Lines of research. The analysis will follow Caffey 1985, Connell 1985, Gaines & Roughgarden the chronology of the settlement process. 1985, Butler 1986, Davis 1987, 1988, Bushek 1988, Fairweather 1988, Sutherland 1990, Minchinton & Scheibling 1991). This new emphasis has been called SETTLEMENT AND RECRUITMENT 'supply-side ecology' (see Lewin 1986, Young 1987, Underwood & Fairweather 1989). Therefore, it is indis- It is important to distinguish between settlement and pensable to incorporate settlement and recruitment as recruitment. There are, however, numerous problems variables in demographic models (Caffey 1985, Under- and conflicting views with respect to existing defini- wood & Fairweather 1989). tions of both processes, particularly those referring to Where settlement is dense, the predominant features settlement (see Keough & Downes 1982, Coon et al. of the community structure have been attributed to 1985, 1990a, b, Keough 1986, Davis 1987, 1988, Bonar factors such as competition, predation and disturbance et al. 1990, Harrold et al. 1991). In the case of benthic (Gaines & Roughgarden 1985, Roughgarden et al. marine invertebrates with pelagic larvae, the term set- 1985, Lewin 1986, Sutherland & Ortega 1986, Rough- tlement should be used to ciescribe the passaye iruln a garden et al. 1991), which correspond to the most im- pelagic way of life to a benthic way of life. This pas- portant and extensively documented processes consid- sage implies not only a descent of the from the ered in traditional models (Underwood & Denley 1984, and a permanent residence on the sub- Underwood & Fairweather 1989) and have been the stratum, but also a set of events and morphogenetic basis of a group of models which have attempted to changes which allow the attached larvae to acquire explain the most important ecological interactions and features appropriate to its new life. These changes processes that determine the structure and dynamics occur solely through . of different marine assemblages (e.g. Dayton 1971, Thus, we define settlement as a process beginning Menge 1976, Menge & Sutherland 1976, Paine 1984, with the onset of a behavioral search for a suitable sub- Connell 1985). Settlement and/or recruitment, in addi- stratum and ending with metamorphosis. Two phases tion to the physical, chemical and biological factors may be distinguished in this process: (1) a behavioral and processes of the water column that affect them, phase of searching for the suitable substratum, and (2) would determine many patterns and would play an a phase of permanent residence or attachment to the important role in communities with sparse settlement substratum, which triggers metamorphosis and in (e.g. Paine 1974, Keough 1984, Underwood & Denley which morphogenetic events take place. Although 1984, Gaines & Roughgarden 1985, Roughgarden et al. there are examples in which metamorphosis occurs 1985, 1991, Menge & Sutherland 1987). before the attachment to the substratum (e.g. Para- Population dynamics and community structure may centrotus;Fenaux & Pedrotti 1988), they are rather un- also be affected by variations in the intensity of settle- common. The recognition of these 2 phases in ment of competing species or of species interacting settlement renders this term more operational. This is through a predator-prey relationship (Connell 1985, important, particularly for those searching for chemical Underwood & Fairweather 1989, see also Fairweather cues that may generate settlement responses in the 1988). Thus, changes in the larval source or recruit- larvae. In fact, the behavioral and morphogenetic ment levels of relevant species can define a scenario of responses may be triggered by different inducers ecological interactions (i.e. vary the intensity and/or (Inestrosa et al. 1988). Recruitment, on the other hand, the importance of one type of interaction or the other, implies the lapse of some period of time. The latter is both spa.tially and temporally; see Keough 1984, variable and defined by the researcher (Roegner 1991). Menge & Sutherland 1987),by determining a pnori the Hence, we consider recruits as newly settled individu- participant's population sizes (Caffey 1985, see also als (i.e. settlers) that have survived to a specified size Fairweather 1988). after their settlement (see also Keough & Downes 1982, The importance of settlement at the population and Connell 1985, Butler 1986, Hurlbut 1991). This review community levels and its biotechnological impact (set- is concerned with factors influencing settlement. Rodriguez et al.. Settlemetnt of benthic invertebrates 195

LARVAL AVAILABILITY Table 1. Examples of the main factors acting during the settle- ment response of benthic marine larvae Factors affecting pre-settlement can be as important as subsequent ones in the determination of distribution Factors Examples patterns of sessile and some mobile species (Denley & - Biological Larval behavior Underwood 1979, Grosberg 1982, Watanabe 1984).For example, the availability of competent larvae for settle- Physical Water flow velocity ment influences the number of individuals recruiting Contour and chemistry of the within a population (Cameron & Schroeter 1980, attachment substrate surface Connell 1985, Cameron 1986) and is subject to tempo- Luminous intensity ral as well as spatial variations. In brief, the most im- Chemical portant phenomena that alter the abundance of larvae Natural inducers Associated with conspecific in the water column, and that are responsible for the individuals temporal variability of settlement, can be associated to Associated with microbial films one of the following categories: (1) reproductive cycles Associated with prey species of adult individuals (Davis 1989, Roughgarden et al. Artificial inducers Neurotransmitters 1991), (2) patterns of winds (Barnes 1956, Hawkins & (e.g.GABA, catecholamines) Hartnoll 1982), currents and other hydrographic fac- Neurotransmitter precursors tors (Yoshioka 1982, Gaines et al. 1985), and (3) (e.g.choline) changes in rates of larval mortality (due to predation, Ions (e.g.potassium) or as the outcome of their longer retention in the plank- ton) (Thorson 1950, Hadfield 1963, Paine 1963, Loosanoff 1964, Mileikovsky 1974, Tegner & Dayton 1981, Cowden et al. 1984, Grant & Williamson 1985, SETTLEMENT Gaines & Roughgarden 1987, Hart & Scheibling 1988, Zimmerman & Pechenik 1991). Dividing the early life-history of marine Larval availability is also subject to spatial variations, into a series of functional stages (e.g. dispersal, devel- mainly determined by the distribution of larvae in the opment, competence, settlement, metamorphosis, etc.) water column. This larval distribution is responsible for is an old idea (see Underwood 1979 for a review). The spatial variability in settlement, at large and small planktonic larval state can be divided into a period of scales, and has been attributed to factors similar to pre-competence, in which growth and development those already analysed as the cause of temporal vari- occurs, and one of competence, in which development ability (see Gaines et al. 1985), such as: (1) currents, has been completed (Jablonski & Lutz 1983). wind patterns and topography (e.g. Underwood 1972, Acquisition of the ability to respond to the appropriate Hawkins & Hartnoll 1982); (2) regional differences in stimuli has usually been termed competence (Coon et larval mortality (Lewis et al. 1982); (3) spatial differ- al. 1990a). The physiological mechanisms by which ences in rates of predation (Mileikovsky 1974); and (4) larvae become competent are poorly understood, but larval behavior through the formation of aggregations some studies implicate the larval nervous system in the water column (Keough 1983). In this context, the (Burke 1983, Hirata & Hadfield 1986, Pechenik & importance of local hydrographic processes and larval Heyman 1987). behavior in the distribution of larvae in the water col- Larval adaptations for a planktonic life are retained umn has been recently highlighted (Jackson 1986). until an adequate stimulus is found for settlement Even though temporal and spatial larval availability (Burke 1983). The stimuli necessary for settlement in- are important when dealing with larval production, we volve a combination of factors including the speed of have only mentioned some of the most relevant factors fluids and contours of the substratum surface (e.g. affecting the abundance of larvae for settlement be- Sebens 1983a, Wethey 1986, Pawlik et al. 1991), lumi- cause a more comprehensive analysis of this subject is nosity and chemical cues (e.g. Morse 1991, see also not directly pertinent to the topic of this review. Hadfield & Pennington 1990). Increases in luminosity The settlement process requires not only that a larva trigger the deposition of cyprid larvae and water cur- be present at a site, but also that, once the larva is at rents can induce their active swimming and attach- the site, its spatial pattern at a small scale be deter- ment to the substratum (Crisp 1955, Crisp & Ritz 1973). mined both by the interaction of physical processes A strong light-dependence can prevent settlement of and biological responses and by the presence of chem- larvae in crevices, as in larvae of the Alcyonium ical cues (Table 1). These processes and responses are siderium (Sebens 1983a). In the absence of an appro- discussed below. priate stimulus, many larvae delay their settlement 196 Mar. Ecol. Prog. Ser. 97: 193-207, 1993

(Thorson 1950, Knight-Jones 1953, Jensen & Morse which allow better survival (Crisp & Barnes 1954, see 1984, Highsmith & Emlet 1986, Coon et a1 1990a). also Wethey 1986). An alternative could be that pas- Nonetheless, Highsmith & Emlet (1986) showed that a sive deposition would determine the distribution of lar- delay of metamorphosis has negative consequences for vae at a large scale and that passive or active redistri- growth and subsequent survival of juveniles of 2 spe- bution would determine the localized distribution, as cies of irregular echinoids. The presence or absence of has been proposed for infaunal organisms (Butman an appropriate stimulus for settlement can have a great 1989).In turn, Carleton & Sammarco (1987) found that impact on postmetamorphic events. the success of settlement in can be improved by Larvae of different species have different degrees of increasing the structural complexity of the substratum dependence and specificity with respect to the indu- through irregularities. They highlighted the impor- cers that trigger their settlement (Morse 1990). This tance of the angle of slope of the substratum and its dependence and specificity would be associated with a protection and pointed out that the aggregated distri- recognition of the inducer of the chemosensory type bution pattern observed in these populations can be (Morse 1991). It is precisely this recognition that acti- influenced, at least in part, by the physical characteris- vates the genetically scheduled sequence of behav- tics of the substratum. The importance of the heteroge- ioral, anatomical and physiological processes which neity of macro- and microsites in the process of select- determine settlement (Morse 1990, see also Yool et al. ing a substratum has also been shown by Le Tourneux 1986). & Bourget (1988) and Chabot & Bourget (1988). The Although exogenous chemical cues have been stud- chemistry of the surface during settlement (e.g. wet- ied, few natural inducers of settlement in invertebrates tability) is an important factor in settlement of barna- have been isolated and characterized (Kato et al. 1975, cles and bryozoan (Maki et al. 1989, Roberts et al. Pawlik 1986, see also Morse 1990, Patvlik 1990). The 1991). These studies indicate that many factors other importance given recently to chemical cues must not than chemical cues have to be considered in any anal- make us underestimate the role played by some phys- ysis of settlement. ical factors or processes, or by larval behavior itself. In this sense, hydrodynamic processes and larval behav- ior (e.g. geotaxis or phototaxis) can be of great impor- NATURAL INDUCERS tance by allowing a larva to be close to the bottom at the time of its settlement (Jackson 3.986, see also Coon Many settlement-inducing chemical cues have been et al. 1985).This closeness to the bottom can be discovered from observations of larval settlement on crucial, because, for many species, the chemical cues different natural substrata (see Rodnguez et al. 1992). would be associated with the inducing substratum and These inducers originate from or are associated with direct contact with the larva would be necessary for various sources and have great ecological importance. any effect to be triggered (e.g. Knight-Jones 1953, These sources are of 3 main types: (l) conspecific indl- Morse & Morse 1984, Pawlik 1986, Raimondi 1988). In viduals (Highsmith 1982, Burke 1984, Jensen & Morse addition to chemical, cues, the responses to the condi- 1984, Pawlik 1986), (2) mi.crobia1 films (Cameron & tions of the water flow played an important role in the Hinegardner 1974, Kirchman et al. 1982, Morse et al. recruitment of the Phragmatopoma lapi- 1984, Maki et al. 1989, Bonar et al. 1990, Pearce & dosa californica (Pawlik et al. 1991). The larvae tum- Scheibling 1991), and (3) prey species (Barnes & Gonor bled along the bottom in the presence of fast flow, 1973, Morse et al. 1979, Morse & Morse 1984, Todd whereas in slow flow they were observed swimming in 1985, Barlow 1990, Hadfield & Pennington 1990). the water column. Although a great majority of the known inducers can Physical factors such, as contouring of the substratum be included in one of these categories, they are not ex- (Crisp & Barnes 1954, Crisp 1961) are used by clusive. larvae to select discontinuities. Wethey (1986) ob- served that up to 30"4 of barnacle larvae settled on identical localities on replicate surfaces of the same Inducers associated with conspecifics contour. Wethey pointed out that passive larval deposi- tion (see also Hannan 1984, Banse 1986, Butman 1989, Settlement induced by conspecific adults has been Pawltk & Hadfield 1990) and active selection of mlcro- descnbed in several benthic marine invertebrates, In- sites with low shear associated with discontinuities on cluding (Jensen & Morse 1984, Pawlik the substratum could account for the settlement ob- 1986), sipunculids (Hadfield 1986), echinoids served. It IS posslble that larvae search first for sub- (Highsmith 1982), molluscs (Seki & Kan-no 1981, strata where there is high shear (Crisp 1955) and, once Slattery 1992), (Knight-Jones 1953, in contact with them, select microsites with low shear Raimondi 1988, 1.991) and (Hldu et al. 197 8). Kodl-iguezet dl . Settlement ot benthic invertebrates 197

The existence of larval inducers associated with con- influence on larval settlement through chemical cues. specific adults has great ecological importance, be- Larvae of the barnacle Chthamalus anlposoma settle cause the induction of settlement by conspecifics can within the range of adult distribution (Raimondi 1991). account for the aggregated distributions of many ben- Larval settlement in adult patches transplanted away thic marine invertebrates. This is a mechanism which from the limits of their distribution Indicates that in- not only increases the probability of fertilization of duction of settlement was somehow associated with gametes of individuals which release their gametes the presence of conspecific adults. Raimondi, however, into the (Pearse & Arch 1969, Russo 1979, Pawlik did not rule out the possibility that other unknown fac- 1986) or which have (e.g. barna- tors also limited settlement within the vertical range of cles), but also acts as an effective defense mechanism distribution of adults. (Garnick 1978, Bernstein et al. 1981, Pawlik 1986). For example, settlement of abalone larvae is stimu- lated by the produced and secreted by adult Inducers associated with microbial films and juvenile individuals (Seki & Kan-no 1981, Slattery 1992). A growth-associated factor has recently been Microbial films are important in the settlement of identified in the large muscular foot of the mollusc many marine invertebrate pelagic larvae. Settlement is Concholepas concholepas. Such a factor stimulates induced by films of diatoms and cyanobacteria (e.g. proliferation, binds to heparin-agarose resins, requires Morse et al. 1984) and by bacterial films (e.g. Kirchman sulfation activity in the responding cell for activity and et al. 1982 for polychaetes, Cameron & Hinegardner apparently induces (Cantillana 1974 for sea urchins, Maki et al. 1988 for barnacles, & Inestrosa 1993) Therefore, it is possible that the Maki et al. 1989 for bryozoans and Bonar et al. 1990 for mucus of adult and juvenile abalones contains hep- oysters). In the latter case the response is quite specific arin-binding growth factors which could be respon- and is generated by the presence of extracellular poly- sible for triggering larval settlement. saccharides or glycoproteins attached to the bacterial The best example of settlement induced by conspe- wall (Kirchman et al. 1982, Hadfield 1986) or soluble cifics is that of the sabellid polychaete Phragmatopoma compounds released by these films (Bonar et al. 1990). lapidosa californica. Larvae settle as a response to free Bonar et al. (1990) observed that while the former fatty acids (e.g.palmitoleic and linoleic acids) isolated favors metamorphosis of larvae of the genus from the sand and cement matrix of the tubes of adults Crassostrea, the soluble compound (n~olecularweight (Pawlik 1986). This response is highly species-specific < 300 Da; see Fitt et al. 1990) induces searching behav- and restricted to the genus Pl~ragmatopoma. None- ior on the substratum (see also Coon et al. 1990b). theless, Pawlik did not rule out the possibility of hydro- Although a greater percentage of settlement (or an in- philic molecules belng involved in the induction. It has crease in the inductive potential) has been observed in been postulated, as an alternative hypothesis, that a the presence of older bacterial films (see also Maki et polymeric protein (rich in residues of dihydroxypheny- al. 1989 for bryozoans, Fitt et al. 1990 for oysters, and lalanine) was the actual agent responsible (Jensen & Pearce & Scheibling 1991 for sea urchins), cases have Morse 1990). also been described in which an inhibitory effect has Highsmith (1982) demonstrated that a small peptide been observed (Maki et al. 1988). The inductive or in- of low molecular mass (< 10 000) produced by adults of hibitory effect of a film may be partly determined by its the irregular echinoid Dendraster excentricus and se- specific composition (Maki et al. 1989). Antibiotics that questered by some component of the sand in which inhibit bacterial metabolism do not inhibit the settle- they were buried was the settlement-inducing chemi- ment response, suggesting that a metabolically active cal cue (see Burke 1984 for the same species, and film is not necessary for the response (Kirchman et al. Pearce & Scheibling 1990b for the irregular echinoid 1982). Echinarachnius parrna). In this context, settlement Besides the soluble inducers derived from bacterial would preferentially occur within the areas inhabited films, ammonia, which is secreted by most and by conspecific adults, generating an aggregated pat- marine , is related to the searching behavior of tern of distribution of the population. This phenome- larvae of the genus Crassostrea (Bonar et al. 1990). non is important not only because this larva-adult This implies that in areas of high biological activity, re- interaction generates an ecological pattern, but also gardless of the presence or absence of bacterial films, because it allows the larva to avoid its predators, which NH3 could reach sufficiently high levels to induce the tend to occur in areas where adults of th~sdetntivorous search behavior (Coon et al. 1990b). Another com- species are absent (Highsmith 1982). pound which i.nduces search behavior in oyster larvae Studies of barnacles have also stressed the fact that is L-P-3,4-dihydroxyphenylalanine(L-DOPA) (Coon et the presence of conspecific individuals can have great al. 1990a, b). This compound could originate in bacte- Mar.Ecol. Prog. Ser. 97: 193-207, 1993

rial films or from conspecific individuals (Coon et al. epoxid of r-tocotrienol present in the red alga 1985). The inducing concentrations of this compound Sargassum tortile is the agent inducing settlement would be found only in the vicinity of the source. If the (Kato et al. 1975). substratum is appropriate, the larva would cement by Some carnivorous species, particularly nudibranchs, itself and endogenous molecules similar in their action also settle in response to their prey. For example, to epinephrine and norepinephrine would induce the Onchidoris bilamellata only metamorphoses in the onset of metamorphosis (Coon et al. 1985). NH3 and L- presence of its prey, newly settled barnacles (Todd DOPA differ in the amount of time needed for induc- 1985). The Phestilla sibogae feeds exclu- tion and probably also in the mechanisms by which sively on the coral Pontes compressa, the only known they are transduced (Bonar et al. 1990, Coon et al. source of an inducer (Pennington & Hadfield 1989, 1990b). Hadfield & Pennington 1990). The inducer is a small (< 500 Da), polar, water-soluble molecule, which acts at small concentrations (< 10 nM). The larvae of P sibo- Inducers associated with prey species gae respond to dissolved substances and do not need to establish direct contact with the substratum In some larvae, settlement is induced by potential (Hadfield 1986, Hadfield & Pennington 1990). No com- prey species of juveniles or adults. Many herbivorous pound induces metamorphosis in P sibogae as quickly species are induced to settle by crustose on and efficiently as the inducer associated with its prey which they feed. These include abalone (Morse & species. Morse 1984, Morse 1990), (Barnes & Gonor Potential predators may also produce inducing sig- 1973), limpets (Steneck 1982) and sea urchins nals. Gastropods of the genus Acanthina are an excel- (Cameron & Hinegardner 1974, Rowley 1989, Pearce & lent settlement-inducing cue for larvae of the barnacle Schelbiing 1550a, i99i j. Chthamal~ls anisgpcma, despite heing an important Inducing chemicals would be available on the sur- predator of that species, probably because the is face of the encrusting algae and would possibly be re- a good index of the limits of vertical distribution of leased when epithelia1 cells are grazed (see Morse & adult barnacles (Raimondi 1988). Morse 1984). In cell-free extracts, the inducer appears Inhibitors of settlement occur. Toxic and non-toxic in association with phycobiliproteins (Morse et al. natural products of the ascidian Eudistoma olivaceum 1979, Morse & Morse 1984, see also Morse et al. 1984). inhibit the settlement of larvae of the bryozoan Bugula The inducer is an oligopeptide which mimics the action neritina (Davis & Wright 1990). The settlement of lar- of y-arninobutyric acid (GABA) by binding to its spe- vae of the colonial ascidian Podoclavella molluccensis cific receptors (see Morse 1990). Induction of settle- is inhibited by natural products released by or asso- ment by larvae of the Strongylocentrofus ciated with the surface of (Davis et al. 1991). purpuratus has been observed by the same partially The presence of oysters inhibits the settlement of bar- purified fraction of the peptide extracted from the wall nacles (Bushek 1988). In this sense, settlement and of crustose coralline algae (Rowley 1989). subsequent recruitment could be the outcome of rejec- Crustose coralline algae are also substrata for settle- tion responses to negative signals rather than the re- ment of coral larvae (Sebens 1983a, b). Morse (1991) sult of lack of positive responses to favorable signals reported that larvae of the coral Agancia humilis settle (Woodin 1991). in response to a sulfating polysaccharide in the wall of the alga. The mechanism of transduction would, how- ever, be different from that in abalone. Morse pointed ARTIFICIAL INDUCERS AND MECHANISMS out that recognition in these organisms could be medi- OF SIGNAL TRANSDUCTION ated by known receptors such as lectins, which are im- portant in the control of cellular differentiation. Besides the proteins associated with conspecifics, Foliose algae also have inducing activities. Inducing polysaccharides from bacterial films, and polypeptides molecules for abalone larvae occur in extracts of fol~ose present in prey species, other chemical substances red algae, including species of Laurencia, Gigartina trigger settlement in marine invertebrate larvae. Their and Porphyra, even though they are not present on the study permits a better understanding of the mecha- surface of any of them and the larvae do not respond to nisms involved in the larval response. In many species, intact fronds of these species (Morse & Morse 1984). chemical cues associated with the substratum are sub- Larvae of the Ischnochiton heathiana metamor- stances which mimic the action of neurotransmitters. phose on follose algae of the genus Ulva (Barnes & This implies the operation of neuronal receptors in the Gonor 1973). A similar phenomenon has been de- initial process which triggers settlement (Baloun & scribed for the hydroid Coryne uchidai in which the Morse 1984, Yool et al. 1986). Rodriguez et al.: Settlement of benthic invertebrates 199

The chemical structure of most of these inducers (Coon et al. 1985, Bonar et al. 1990, Pawlik 1990).The suggests possible mechanisms involved in the trans- endogenous levels of noradrenaline change greatly duction of signals triggering metamorphosis, as dis- during larval development, doubling just before the cussed below. acquisition of metamorphic competence (Bonar et al. 1990). Pharmacological analyses have shown that these catecholamines act on adrenergic receptors of Choline derivatives the a-l type, which leads to the hypothesis that the second inositol-phosphate messenger mediated by cal- Choline is the precursor of the neurotransmitter ace- cium operates in the transduction of the adrenergic tylcholine and of phosphatidylcholine, an important signal. This, however, has not been clearly demon- component of biological membranes. Succinylcholine strated (Bonar et al. 1990). and choline induce settlement in the gastropods L-DOPA, adrenaline and noradrenaline have induc- Phestilla sibogae (Hirata & Hadfield 1986) and tive effects in other molluscs. Larvae of the bivalves Ilyanassa obsoleta and incomplete settlement in the Mytilus edulis and Pecten maximus respond, respec- polychaete Phragmatopoma lapidosa californica (see tively, to L-DOPA and to L-DOPA and adrenaline (see Pawlik 1990). In the case of P sibogae, the receptors for Pawlik 1990). Larvae of the gastropod Ilyanassa obso- choline and for the natural inducer would be different, leta respond to dopamine (Levantine & Bonar 1986). because, in experiments in which both substances Larvae of polychaetes and echinoids respond to were present, neither competition for receptors nor ha- molecules derived from tyrosine. The polychaete bituation of the pre-competent larvae to choline deriv- Phragamtopoma lapidosa californica is induced to set- atives has been observed (Hirata & Hadfield 1986). tle with the same intensity by L-DOPA and by its iso- Apparently choline derivatives do not act on external mer D-DOPA (Pawlik 1990). Only dopamine induces receptors, but directly activate the nervous system, as n~etamorphicresponses in the larvae of the irregular has been suggested for l? lapidosa californica (Pawlik echinoid Dendraster excentricus (Burke 1983). 1990).This is because the larvae actively take up large These observations are compatible with the hypoth- amounts of choline from the external medium esis that dopamine, or one of its derivatives, acts as the (Hadfield & Pennington 1990). Choline could be chemical messenger during the induction of metamor- involved in induction of settlement in several ways: phosis. Burke (1983) indicated that this endogenous (1) by acting directly on the cholinergic receptors; chemical cue could act directly upon larval tissues, or (2) by participating as precursors in acetylcholine bio- indirectly by inducing the release of additional sub- synthesis; or (3) by stimulating synthesis and release stances which stimulate the tissues that contain the ef- of catecholamines as neurotransmitters (Hirata & fectors of metamorphosis. This hypothesis is consistent Hadfield 1986, Hadfield & Pennington 1990). with the fact that reserpine (a substance that depletes catecholamines in tissues) interferes with and inhibits metamorphosis (Burke 1983). L-DOPA and catecholamines

L-DOPA and the catecholamines (dopamine, adren- Other aminoacid derivatives aline and noradrenaline) are tyrosine derivatives with different biological functions, such as hormones, neu- GABA is a product of glutamic acid decarboxylation rotransmitters, pigments and adhesive and structural and acts as an inhibitory neurotransmitter. It induces proteins. Tyrosine derivatives induce settlement in hyperpolarization of post-synaptic membranes by species of bivalves such as Crassostrea virginica and means of an increase in the membrane permeability to Mytilus edulis (Pawlik 1990). L-DOPA induces search- chloride ions. In some cases, however, it actives a de- ing behavior in Crassostrea gigas, whereas adrenaline polarizing flux of chloride (Kuffler et al. 1984). GABA and noradrenaline only induce metamorphosis without and analogous molecules (e.g. y-hydroxybutyric acid, previous searching (Bonar et al. 1990, Coon et al. y-amino-n-valeric acid, E-amino-n-caproicacid, musci- 1990a). Bonar et al. (1990) proposed that L-DOPA from mol, gabuline and baclofen) are powerful inducers of the external medium is incorporated into the larva and settlement in the gastropod Haliotis rufescens (Morse transformed into dopamine, which then acts on dop- et al. 1979, Trapido-Rosenthal & Morse 1986a, b, aminergic receptors. This observation, supported by Morse 1991). This reflects the stereochemical specific- the fact that these oyster species have a delayed re- ity of the larval receptors of this mollusc for these com- sponse to catecholamines with respect to dopaminer- pounds (Morse & Morse 1984, Trapido-Rosenthal & gic stimulation, suggests that catecholamines activate Morse 1986a, b). Induction of metamorphosis by GABA an endogenous sequence of metamorphic events would depend on the depolarization of GABA-sensi- 200 Mar. Ecol. Prog. Ser. 97: 193-207, 1993

tive cells exposed to the external medium and would down-regulation), a phenomenon determined by a re- be mediated by a net depolarizing chloride efflux or duction in the number of these receptors as the out- another anion (Baloun & Morse 1984). Induction by come of the early exposure of the larva to the inducer GABA is inhibited by high external concentrations of (i.e.pre-competent larva) (Trapido-Rosenthal & Morse chloride or a blocker of potassium channels (e.g. tetra- 1986a). Trapido-Rosenthal & Morse (1986b) demon- ethylammonium). This suggests that the chloride ef- strated that, during larval desensitization, the post- flux plays an important role in the transduction of the receptor pathways of transduction (e.g. cAMP and GABA signal (Baloun & Morse 1984). excitatory depolarization) would remain intact. An increase in calcium concentration inhibits induc- Induction by GABA.occurs in other molluscan spe- tion by GABA, probably by means of the activation of cies, namely the gastropods Trochus spp., klopalia potassium channels regulated by calcium, producing a muscosa and Tonicella lineata (complete metamorpho- net hyperpolarizing flux (Baloun & Morse 1984). These sis), Conus spp., Aplysia spp., Teredo spp. (incomplete authors have observed that a decrease in external metamorphosis) and the chiton Katharina tunicata (set- potassium concentration inhibits induction by GABA, tlement without metamorphosis) (Morse et al. 1979, which could be due to hyperpolarization and which Morse et al. 1984, Pawlik 1990). Induction has also would antagonize the depolarization mediated by been observed in the sea urchin Strongylocentrotus GABA. The activation of anionic channels would de- droebachiensis (Pearce & Scheibling 1990a). On the pend on enzymes phosphorylated by protein kinases other hand, no effect at all has been observed in the A, which would, In turn, be activated by cAMP (Morse polychaete Phragmatopoma Iapidosa californica (Paw- et al. 1980, Trapido-Rosenthal & Morse 1986b). The lik 1990), the cnidarian Alcyonium siderium (Sebens levels of the latter would be increased by the activation 1983b), the echinoid Dendraster excentricus (Burke of the adenylate cyclase through the binding of the ex- 1983) or the molluscs Phestilla sibogae (Hadfield 1984), oyenoils liya~~cijillductllj iu tile recepior jMorse i93i). Crassosirea gigas (Coon et ai. i985j and Crepiauia ior- The sensibility of the morphogenetic pathway in nicata (Pechenik & Heyman 1987). The variable results Haliotis rufescens would be controlled by 2 regulatory encountered by diverse authors in the response of ab- pathways. One would be related to a facilitation phe- alone larvae to GABA (from narcotic effects up to com- nomenon (i.e. up-regulation) of the settlement re- plete settlement) explain why it has not been generally sponse, determined by compounds which act in a con- used as an inducer of settlement in the cultivation of centration-dependent manner and which would not this commercially important gastropod (see Pawlik have to be present simultaneously with the inducer to 1990). Additional inductive pathways which utilize generate the effect (Trapido-Rosenthal & Morse mucus or some associated component to trigger larval 1986a). settlement are probably present in molluscs. In fact, re- In this context, Haliotis rufescens larvae exhibit an cent evidence indicates that high larval settlement amplification of sensitivity at small concentrations of rates of Haliotis rufescens occur on substrates of con- the inducer, as a response to small concentrations of ly- specific mucus containing some unknown inductive sine and related aminoacids (Morse 1991). The larval cue (Slattery 1992). In this context, it is interesting to receptor activated by lysine (which is different from mention that a heparin-binding growth factor has been the GABA receptor; see Trapido-Rosenthal & Morse identified in foot extracts of the prosobranch mollusc 1986a) would activate a G protein, which would act on Concholepas concholepas (Cantillana & Inestrosa a phospholipase C associated with the membrane. The 1993). latter would hydrolyze a phosphatidylinositol an- chored to the membrane, releasing diacylglycerol and Induction by ions inositol triphosphate (IP3).The former would activate a protein kinase C, which would phosphorylate other The sensory bases of induction suggest that the ner- proteins involved in the amplification process (Morse vous system is involved in the onset of metamorphosis 1991). The outcome of the interaction of both pathways (Burke 1983, Yool et al. 1986). The conduction of would greatly increase the sensitivity of the larva. This electric impulses in nervous tissues depends on the would presumably allow settlement responses in suit- maintenance of an electrical potential through the cell able areas in the presence of small concentrations of membran.e, which is a function of the permeability of the inducer associated with the algal surface (Morse the membrane to potassium, sodium and chloride 1990). It would even enhance settlement in coastal (Kuffler et al. 1984, Barlow 1990). Hence it is of interest areas rich in nutrients (aminoacids are contained in to analyze the effects on settlement of ions and com- dissolved organic materials. pounds that affect ionic transport through membranes. The other regulatory pa.thway would be related to a Larvae of a number of species undergo metamorpho- habituation process of the settlement receptors (i.e. sis in response to large concentrations of potassium Rodriguez et al.: Settlement of benthic invertebrates

ions, e.g. the molluscs Haliotis rufescens, Phestilla sib- mortality after settlement - that is, whether its action ogae, Astraea undosa (Yool et al. 1986), Crepidula for- is density-dependent or density-independent. As sum- nicata (Pechenik & Heyman 1987), Adalaria proxirna marized by Hurlbut (1991), usually when the settle- (Todd et al. 1991). Concholepas concholepas (Inestrosa ment rate is low, juvenile mortality is density-inde- et al. 1992) and the polychaete Phragmatopoma lapi- pendent; when it is high, mortality is density-depen- dosa californica (Yool et al. 1986). Potassium may act dent. by means of the direct depolarization of excitable cells One way of determining whether settlement density involved in the perception of inductive stimuli and, as affects the subsequent mortality of settlers has been with GABA, their action would depend on their con- to study the mortality-settler density relationship centration and exposure time (Baloun & Morse 1984). (Roegner 1991). Between these 2 variables, 3 funda- Baloun & Morse (1984) showed that tetraethylammo- mental relations have been described using linear re- nium (a compound that selectively blocks potassium gression models (see Roegner 1991): (1) a relation with channels dependent on voltage in neuronal and mus- a slope > 0 which describes density-dependent mortal- cular cells) inhibits metamorphosis in the abalone ity; (2) one with a slope = 0 which describes density- Haliotis rufescens in response to potassium, but not in independent mortality; and (3) one with a slope

(2) selection and attachment to the substratum with and requires more meticulous studies on the identity of subsequent metamorphosis, which depends on physi- the inducers of settlement. cal and chemical cues and on the larval behavior and A recurrent subject in the study of settlement is re- response. lated to the inference of settlement patterns from re- Only when settlement is well understood will it be cruitment patterns. Density-independent mortality possible to incorporate settlement into specific popula- after settlement has been considered as a prerequisite tion models and therefore have a better understanding for this kind of estimation, but this has been chal- of temporal and spatial variations. For these reasons, it lenged by Holm (1990). Holm pointed out that recruit- is essential to analyse settlement from the widest pos- ment could reflect settlement in spite of density- sible perspective, attempting to integrate aspects of dependent mortality, especially if settlement densities different disciplines (e.g. ecology and physiology). were small. Roegner (1991) indicated that, with oys- It is important to clarify the concepts used in order to ters, even density-independent mortality did not allow unify criteria. It is indispensable that these concepts be the estimation of settlers from recruits with reasonable operational, so that they may be really useful. In this accuracy. That was the case because mortality rate context, we define settlement as a process of change between censuses (i.e. in time) was not constant. Thus, from a pelagic to a benthic way of life, including 2 simple back estimates of settlers from recrults using phases: (1) one of searching behavior for an appropri- linear regressions are not precise enough to be useful ate site, (2) another of permanent contact with or (Roegner 1991). Roegner's study places the issue at the attachment to the substratum which triggers meta- starting point, and further investigations would be morphosis. needed in the attempt to infer settlement patterns from A number of ecological factors and processes are in- recruitment. Notwithstanding, development of refined volved in the generation of settlement. Physical factors techniques and methodologies allowing direct exam- such as surtace contour, heterogeneity ot substratum lnation ot the settlement process (i.e.metamorphosis) and microsites of low shear and larval behavior can be will be more useful than retrospective estimations from critical for the selection of settlement sites. Larvae, for recruitment. instance, may simply tumble along the bottom (Pawlik From a physiological-molecular perspective, chemi- et al. 1991) or vary their phototaxic response according cal cues have been widely considered in studies of set- to luminous intensity (Young & Chia 1982). Many of tlement. Few natural inducers have, however, been these processes have, however, not received sufficient identified, isolated and characterized (Pawlik 1986, attention, particularly in relation to their interaction 1990). Hadfield (1984) found no artificial inducer more with inductive chemical cues. For example, larvae rapid and efficient in action than that derived from the search for suitable sites for settlement at several differ- prey species of the nudibranch PhesfilJa sibogae.This ent scales, with consequently different biological and suggests that future research should focus on features physical influences (Le Tourneux & Bourget 1988). of the natural habitat. Inducers of settlement are more Chabot & Bourget (1988) found that selection by larvae likely to be found among natural cues. Furthermore, of the barnacle Semibalanus balanojdes at a large these are the best tools for studying mechanisms of scale was related to the heterogeneity of the substra- transduction and larval response. This is especially tum. In contrast, at a smaller scale settlement was in- interesting because transduction is not well under- fluenced by conspecific individuals. Butman (1989) in- stood, although it is known that the generation of ner- dicated that while passive deposition of larvae could vous impulses, and hence the nervous system, would determine their distribution at a large spatial scale, the be involved. Nonetheless, the use of artificial inducers outcome at a small scale could be the consequence of a is and ~1.11remain a useful tool for the study of settle- subsequent redistribution (passive or active). Such ment, particularly in the cultivation of commercially studies are scarce; most analyses of settlement have important species, until more effective natural indu- been at restricted spatial and geographic scales. cers are discovered and isolated (Johnson et al. 1991a). Together with intensifying the study of physical and Similarly, identification of these inducers could, in ethological factors, it will be necessary to analyse more many cases, facilitate the search for signals in nature, accurately the identity of agents responsible for the in- especially through the knowledge of their physico- duction of settlement. Johnson et al. (1991a, b) sug- chemical structure. gested that the compounds inducing settlement of a The specificity of the inducer and a high dependency number of species - which historically have been asso- of the larva to it may also be very important. In some ciated with the surface of crustose coralline algae cases, knowledge of specificity could allow better pre- (Morse & Morse 1984, Morse et al. 1984) -likely would diction of population and/or community patterns. not be produced by the algae, but by bacteria asso- Thus, determining patterns of distribution of settle- ciated with them. This new hypothesis is interesting ment-inducing substrata and/or the differential con- Rodriguez et al.. Settlem ent of benth~c~nvertebrates 203

centrations of inducers in the field would enable settle- secondary messenger CAMP and the appearance of a ment patterns to be predicted. The problem is that to new form of the neurotransmitter-related enzyme ace- determine the specificity of an inducer it is necessary tylcholinesterase (Inestrosa et al. 1993). A further to know and study its specific physico-chemical struc- understanding of the specific molecular mechanisms ture (e.g. aminoacid sequence in the case of peptides, that regulate these processes will undoubtedly estab- or active domains in the case of proteins) and the na- lish an experimental framework to determine the envi- ture of the inducers in related species (Hadfield 1986). ronmental signals that control larval settlement, and This has not yet been done, although there is some consequently population recruitment. Therefore, the evidence of species-specific responses to inducing application of molecular technologies to ecologically substrata, as in the case of different coral species oriented questions is an important new area of re- which respond to different species of coralline algae search to consider. (Morse 1991). Another important point is the possible existence of Finally, the knowledge of settlement-inducing cues inhibitory factors of the settlement process. In this re- at different taxonomic levels could be a useful tool in gard, Woodin (1991)postulated that a rejection of neg- the study of phylogenetic relations between taxa and, ative or inhibitory cues, rather than a positive response in turn, could help to understand the origin and evolu- to inducing signals, could be responsible for many pat- tion of settlement at the receptor-signal level. terns of settlement and recruitment observed in na- Another interesting aspect of settlement that should ture. From an ecological viewpoint, inhibition of settle- be studied in an ecological context is the phenomenon ment would be of vital importance, especially in sessile of habituation of the receptors to inducers (determined species which have no other mechanism for avoiding by a decrease of their number in the corresponding epibionts (Davis et al. 1989). On the other hand, isola- chemosensorial cells) as a consequence of early or re- tion and characterization at the molecular level of in- peated exposure to the cue (Trapido-Rosenthal & hibitory substances from these species could allow Morse 1986a, Morse 1991). For species that have lar- identification of anti-fouling substances, which are in- vae with a short period of pelagic life (e.g. abalone), dispensable on the surface of structures such as docks this phenomenon would be an excellent ecological and boats. mechanism for improving larval dispersal and prevent- Settlement and recruitment are the initial processes ing immediate settlement of larvae near their parents, determining the structure of populations of many spe- thus avoiding subsequent competition for space and cies. Although they have long concerned biologists, food. they have received great attention only in recent years. From a biotechnological perspective, ignoring the Much progress has been made in the study of settle- timing of the acquisition of competence could result in ment processes. As shown here, synthesis of the find- a premature exposure of pre-competent larvae to the ings of these studies reveals new areas for future work. inducer, resulting in a delay in settlement. In the same A complete analysis of larval settlement depends on way, a delay in the exposure of competent larvae to the the future integration of biochemical, physiological, inducer could have a negative impact on growth and morphological and behavioural studies in an ecologi- subsequent survival of juveniles, as in an irregular cal context. echinoid (Highsmith & Emlet 1986). The relationship between stages of larval developnlent and changes in protein patterns, second messengers, or enzymatic lev- Acknowledgements. Th~swork was supported by FONDE- els of the nervous system has not been sufficiently ex- CYT Grants 0753/91 to F.P.O. and 3502/89 to N.C.I. We sin- cerely thank constructive cr~tic~smsby Dr J. M. Lawrence on amined, but one example is the study of Inestrosa et al. an earlier draft, and Dr A. J. Underwood for helpful comments (1990). Further studies in this direction are necessary and suggestions that greatly improved this manuscript. S.R.R. to determine the onset of competence, which is para- is presently Becario Residente en Invest~gac~on(DIUC) at the mount for rearing larvae of commercially important Depto. Biologia Celular & Molecular. species, but would also allow investigation of the in- trinsic larval changes associated with settlement. Recently, an interesting and timely study into the LITERATURE CITED biochemical changes accompanying metanloi-phosis in Baloun, A. J., Morse, D. E. (1984). Ionic control of settlement the nlollusc Concholepas concholepas has been pre- and metamorphos~s In larval Haliotis rufescens sented (Inestrosa et al. 1993). Molluscan metamorpho- () Biol. Bull. 167: 124-138 sis is accompanied by several molecular changes in- Banse, K. (1986) Vertical dlstr~butionand horizontal transport of planktonic larvae of ech~nodermsand benthlc poly- cluding a modification in the pattern of protein chaetes in an open coastal sea. Bull. mar. Sci. 39: 162-175 synthesis, an increase in heparin-binding proteins (i.e. Barlow, L. A (1990). Electrophys~ological and behavioral re- growth factors), a decrease in the larval levels of the sponses of larvae of the red abalone (Haliotis rufescens) to 204 Mar. Ecol. Prog. Se

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This article was submitted to the editor Manuscript first received: July 24, 1992 Revised version accepted: March 23, 1993