Pheromones and the gregarious settlement of ... - IngentaConnect

BULLETIN OF MARINE SCIENCE, 39(2): 323-331, LARVAL INVERTEBRATE WORKSHOP

1986

PHEROMONES AND THE GREGARIOUS SETTLEMENT OF MARINE INVERTEBRA TE LARVAE Robert D. Burke ABSTRACT Information on gregarious settlement and metamorphosis of larvae is reviewed for cirripedes, echiuroids, sabellarid polychaetes, and echinoids to determine if the use of adultderived chemical cues is consistent with the concept of pheromonal communication as applied to other types of animals. Examples of several species of marine invertebrates in which adultderived chemical cues may be utilized in gregarious settlement and metamorphosis are listed. In appears this mechanism of habitat selection is similar in many respects to communication common in insects and vertebrates where chemicals released to the environment elicit behavioral, physiological, or developmental responses from con specifics. Evidence is not available to determine if this form of communication in marine invertebrates has specialized beyond adaptive responses ofIarvae to adult-associated chemicals, to true chemical signalling.

Some marine invertebrate larvae "select" suitable adult habitats by metamorphosing in response to cues associated with certain environments. Although a variety of cues may be involved in inducing larvae to metamorphose, adsorbed and diffusable chemicals appear to be employed by a large number of marine invertebrates (Meadows and Campbell, 1972; Crisp, 1976). For several species it has been shown that larvae settle and metamorphose gregariously and this pattern of recruitment is achieved by larvae being induced to settle and metamorphose by chemical cues produced by individuals of the same species (Meadows and Campbell, 1972; Scheltema, 1974; Burke, 1983). The production and detection of chemicals by animals is well established, indeed some see it as a fundamental attribute of all living things (Wilson, 1970). Chemicals released or perceive,d as signals within species are termed pheromones and have been demonstrated in several major phyla (Wilson, 1970). Pheromones are defined as chemicals released from an organism that evoke behavioral, physiological or developmental responses in conspecifics (Karlson and Luscher, 1959). Although this term is not commonly used by larval biologists, gregarious recruitment mediated by adult-derived chemical cues may be part of this more general phenomenon of chemical communication. The objective of this paper is to review several examples of gregarious recruitment of marine invertebrates to determine if they are consistent with the concept of pheromonal communication and to compare them with pheromonal communication in other animals. Pheromones The definition of a pheromone makes apparent the characteristics that must be demonstrated for a substance to qualify as one. To demonstrate that a chemical initiates a certain response, it must be possible to extract it and initiate the response in vitro. Often this serves to isolate the stimulus from other cues that may also playa role. Most often pheromones are single chemical entities, but medleys of pheromones are common in some animals, particularly social insects (Fletcher and Blum, 1983). Synergisms and modification of the signal can occur with mixtures of pheromones (Wilson, 1970). As well, in mammals chemical recognition of individuals is apparently achieved by complex mixtures, the precise balance 323

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of the components forming the basis of the specificity (Wilson, 1970). Although the chemical nature of most pheromones is unknown, pheromones do come from diverse classes of chemicals. Perhaps the best known are the substituted fatty acids of insects, but alkanes, alkenes, alcohols, ketones, aldehydes, steroids and polypeptides, also act as pheromones (Wilson, 1970; Riehl et aI., 1984; Vandenbergh et aI., 1976). Pheromones are often volatile substances that are released and diffuse to the recipient, but other means of transmission are also employed. In aqueous environments pheromones are often soluble and diffuse or may be carried by currents to the recipient (Liley, 1982). In some situations pheromones are transmitted directly by licking or feeding of one individual by another as with the queen substance of honey bees (Gary, 1974). Often the pheromone is applied to a substrate as in trail marking by insects (Wilson and Bossert, 1963; Wilson, 1970), or territorial marking by mammals (Mykytowyzc, 1974). Pheromones applied to the substrate may be volatile or rely on some form of contact chemoreception (Wilson, 1970). Pheromones are distinguished on the basis of the response they induce (Wilson and Bossert, 1963). Releaser pheromones evoke an immediate behavioral response as the alarm response offish which scatter from the vicinity of an epidermal substance that diffuses from an injured conspecific (Pfeiffer, 1974). Primer pheromones alter the physiology of an organism producing a subtler, longer-lasting response. An example of a primer pheromone is the Bruce effect in which a pheromone from a male mouse induces female mice, recently impregnated by another male, to abort and rapidly return to estrus (Bruce, 1966). Pheromones controlling developmental events usually are considered primer pheromones as in caste determination of social insects where development of various forms of individuals is dictated by the presence or absence of certain pheromones (Moore, 1974). Pheromones are usually most effective in evoking responses from conspecifics (Wilson and Bossert, 1963). Although in several situations pheromones may also have an effect on other closely related species. In most cases these cross-reactions are considered a result of common ancestry and communication within the species is not impaired. Thus, rigid species specificity is not a defining characteristic of a pheromone. Gregarious Recruitment Gregarious settlement and metamorphosis of marine invertebrate larvae is a common phenomenon and several mechanisms may be involved in bringing it about. Larvae that occur in swarms, or are short-lived and do not disperse far from the site of release, may tend to settle and metamorphose simultaneously, resulting in apparent aggregations. Pyefinch and Downing (1949) found more new colonies of Tubularia larynx on a plywood settling panel seeded with an adult colony than on a panel without and concluded that actinulae did not disperse more than a few meters from the parent colony. Larvae that possess the capacity to discriminate between substrates may metamorphose in aggregations due to the patchiness of suitable substrates. This form of clumping may be achieved by larvae using any combination of senses. For example, negative phototaxis in some compound ascidians results in larvae that are released in aquaria metamorphosing in patches on blackened portions of the tank wall (R. A. Cloney, pers. comm.). Gregariousness may also result from larvae responding to cues associated with conspecific adults (Table 1). In many of the situations described in the literature

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Table I. List of marine invertebrates and metamorphosis of larvae

Phylum

Cnidaria Anthozoa Hydrozoa

Mollusca Bivalvia

Gastropoda

Annelida

Arthropoda

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for which the presence of conspecifics influences settlement

Species

Ptilosarcus guerneyi Nemertesia antennina Clava squamata Kirchenpaueria pinnata Tubularia larynx

Evidence for chemical cue

YeS Yes Yes Yes

Reference

Chia and Crawford, 1973 Hughes, 1977 Williams, 1976 Williams, 1976 Pyefinch and Downing, 1949

Crassostrea virginica Ostrea edulis Mercenaria mercenaria Raliotis disces Biuium reticulatum Col/isella strigatel/a Rossoa splendida

Yes Yes Yes Yes

Veitch and Hidu, 1971 Knight-Jones, 1949; Bayne, 1969 Keck et aI., 1971 Seki and Kan-no, 1981 Kiseleva, 1967 Wilson, 1968 Kiseleva, 1967

Sabel/aria alveolata Sabel/aria vulgaris Spirorbis borealis Phragmatopoma californica Pomatoleios kraussi Rydroides dianthus Spirorbis pagenstecheri Sabel/aria spinulosa Polydora ligni

Yes Yes

Wilson, 1968 Eckelbarger, 1975 Knight-Jones, 1951 Jensen and Morse, 1984 Crisp, 1977 Scheltema et aI., 1981 Knight-Jones, 1951 Wilson, 1970 Blake, 1969

Aerceriella enigmata Balanus balanoides Elminius modest us Balanus crenatus Balanus amphitrite Balanus tintinnabulum Chthamalus stellatus

Yes

Yes

Yes Yes

Straughan, 1972 Knight-Jones, 1953 Knight-Jones and Stevenson, 1950 Knight-Jones, 1953 Daniel, 1955 Daniel, 1955 Daniel, 1955

Sipuncula

Golfingia misakiana

Yes

Rice, 1978

Echiura

Urechis caupo

Yes

Suer and Phillips, 1983

Echinodermata Crinoidea Holothuroidea Echinoidea

Florometra serratissima Psolus chitonoides Dendraster excentricus

Yes

Mladinov and Chia, 1983 Young and Chia, 1982 Highsmith, 1982

Chelyosoma product urn Pyura haustor

Yes

Young and Braithwaite, 1980 Young, pers. comm.

Chordata Urochordata

where the presence of adults influences patterns of settlement and metamorphosis, chemical cues have been implicated, although in only a few situations have chemical cues been extracted and the responses described in detail. Barnacles. - Field observations and experiments with settling plates have shown cyprids of the barnacle Balanus balanoides prefer to metamorphose on or near con specifics (Knight-Jones and Stephenson, 1950; Knight-Jones, 1953). Texture, contour and chemical characteristics of the substrate are used as cues by larvae

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in determining where they will metamorphose (Crisp, 1974; 1976). An extract of B. balanoides tissues adsorbed to test panels will make them more attractive for settlement and metamorphosis (Crisp and Meadows, 1962). The chemical factor, arthropodin, is heat stable, non-dializable, and has been characterized by gelfiltration, isoelectric focusing and amino acid composition as a polymorphic system of proteins derived from 5-6,000- and 18,000-dalton subunits (Larman et al., 1982). Similar proteins, which will promote metamorphosis, can be extracted from a variety of animal tissues and bear some resemblance to the contractile protein actin (Larman, 1984). The chemical is water soluble but it appears to induce metamorphosis only when it is adsorbed to a surface. It is thought that the protein is released by tissues and is bound to the epicuticle of the barnacle (Crisp and Meadows, 1962; 1963). Although the chemical in solution is unable to induce larvae to metamorphose, it does influence larval behavior. Larvae pretreated with sea water containing the extract were more prone to explore surfaces than larvae not treated with the cue (Crisp and Meadows, 1963). When larvae are offered a choice between panels treated with tissue extracts, more larvae were found exploring the treated panels than the untreated panels (Crisp and Meadows, 1963). It is not clear ifthe larvae alight preferentially on the panel or tend to spend more time on the treated panels. Crisp and Meadows (1962; 1963) found no evidence for larval chemotaxis. Over a period of time more larvae will metamorphose on treated panels and Crisp (1974; 1976) has suggested the chemical and physical features of the substrate are involved in inducing metamorphosis, though the role of each in the initiation of the developmental events of metamorphosis has not been clearly demonstrated. Echiurans. - Larvae of the echiuran, Urechis caupo metamorphose rapidly when exposed to sediments from adult burrows or artificial substrates previously in contact with adults (Suer and Phillips, 1983). Apparently a heat-labile chemical component with a molecular weight of 3,500-14,000 daltons that is released from the surface of adult worms is responsible. The chemical is water soluble, but only capable of inducing metamorphosis when adsorbed to a surface. Exudates from another echiuran were not effective in inducing metamorphosis. Exposing competent larvae to substrates treated with the chemical cue induced rapid secretion of mucus, loss of external ciliation and an abrupt onset of peristaltic burrowing (Suer and Phillips, 1983). Some of these responses can be classified as developmental changes and some, such as mucus secretion and burrowing, are behavioral. In the echiuran family Bonellidae, the sex of the worm is influenced by the presence of adults when the larva metamorphoses (reviewed by Pilger, 1978). Females have a large proboscis which develops from the pretrochallobe at metamorphosis. In males, the lobe remains small and ventral ciliation is retained. Larvae, which are sexually indifferent, will develop as males if they metamorphose on an adult female, but develop as females if they metamorphose on a clean substrate (Balzer, 1925). A heat stable extract of the proboscis, body wall, and gut will induce larvae to metamorphose into males (Balzer, 1925; Agius, 1979). A secretion of the female body wall, which is produced when the worm is disturbed, also has masculinizing properties (Aguis, 1979). Polychaetes. -Several species oftubiculous polychaetes are reported to settle and metamorphose in response to the presence of conspecifics. Wilson (1968; 1970) has described in detail the development, settling behavior, metamorphosis, and gregariousness of Sabel/aria alveolata and Sabel/aria spinulosa. Larvae metamorphose preferentially on the tubes of juveniles and adults. Wilson (1968) de-

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termined that it was not the sand and rock in the tube, but the cement that the worms secrete in constructing the tubes, that influenced settlement and metamorphosis. Although old tubes retain their attractiveness after the worm has died or been removed, the effect is enhanced by the presence of newly metamorphosed worms. Wilson found the cement could be made ineffective by acid treatment, but did not determine its chemical nature. Working with a related sabellarid, Phragmatopoma californica, Jensen and Morse have found the active component of the cement to be a protein with a DOPA moiety linked to it. Wilson (1970) found that the cement was not species specific in the laboratory, but in the field, larvae appear to settle only with con specifics. Wilson (1968) described the "searching" behavior of settling larvae and found that larvae were quickly induced to change from wide to close searching by the tube cement and that the cement was effective in inducing larvae to undergo the developmental changes of metamorphosis. Echinoids.-Highsmith (1982) showed that larvae of the sand dollar, Dendraster excentricus were induced to metamorphose by sand from a sand dollar bed and suggested a low molecular weight protein component ofthe sand was responsible. Burke (1984) made extracts of the sand and from these purified a 980-dalton peptide that will induce metamorphosis of competent larvae. Sand that otherwise will not induce metamorphosis can be conditioned by adult sand dollars to induce metamorphosis. Extracts of some adult tissues also have the capacity to induce metamorphosis and the 980-dalton peptide can be purified from these extracts. The peptide rapidly induces metamorphosis at concentrations as low as 10-6 M. Lower concentrations induce prolonged reversals of ciliary beat and will initiate metamorphosis, but require several hours to do so. The peptide will induce metamorphosis in larvae without larvae contacting a substrate and samples of water from aquaria containing adult sand dollars will initiate settlement and metamorphosis. Extracts of sand from subtidal and intertidal populations of sand dollars will induce larvae of intertidal populations to metamorphose. However, these extracts do not induce larvae of the regular echinoid, Strongylocentrotus droebachiensis to metamorphose. DISCUSSION

Although a precise identification of the chemicals involved in gregarious recruitment is not available for even the best-studied marine invertebrates, none of the chemicals so far characterized appear similar to the volatile compounds utilized by terrestrial animals. It is probably more relevant for aquatic organisms that the chemicals are water soluble if larvae perceive them in solution, and adsorbable if larvae perceive them on a surface. Wilson and Bossert (1963) point out that volatile pheromones are commonly between 80 and 300 daltons. At lower molecular weights, diversity of chemicals, and secretion and storage become limiting. As molecular weight increases, chemical diversity increases rapidly and the energy involved in synthesis is greater. These factors will probably also hold true for water-borne chemicals, but regardless of molecular weight or solubility, diffusivity in water is much less than in air. This implies that pheromones in aquatic environments will take longer to reach their maximum radius of effectiveness and they will have a long fade-out time (Wilson, 1970). The chemical cues that mediate gregarious settlement and metamorphosis in the four examples presented apparently function either in solution (Dendraster excentricus) or adsorbed to a surface (Balanus balanoides, Urechis caupo, Sabel-

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laria alveolata). None of these forms of conveyance of the chemicals differs substantially from mechanisms of transfer of pheromones described for other animals (Wilson and Bossert, 1963; Wilson, 1970; Birch, 1974). Even the extreme case, where the chemical is bound to the surface of the individual that produced it is considered consistent with the concept of pheromonal communication in its broadest sense (Wilson, 1970). Presumably chemicals on the surface of the tunic, cuticle or epidermis that mediate gregarious recruitment in other forms, could be similarly considered. Behavioral responses, such as burrowing in Urechis caupo, ciliary reversals in Dendraster excentricus and changing from wide to close searching in Sabella ria alveolata and Balanus balanoides appear to be elicited by chemical cues. These cues also induce the developmental responses of metamorphosis, which in the examples discussed are relatively rapid and appear released. With insects and vertebrates that have developmental events controlled by pheromones, the chemicals are usually considered primer pheromones because of the duration of the response. However, as metamorphosis in marine invertebrates appears in most lineages to have evolved as a rapid event, it should be considered as a released developmental response. In the bonellid echiurans, determination of the sex of the metamorphosing individual is more similar to the developmental responses evoked by primer pheromones in other animals. Pheromonal communication is highly specialized in some groups, such as mammals and insects. A diverse array of chemicals produce a wide range of responses that form an integral part of the intraspecific interactions in many species. It is generally accepted that pheromonal communication, like other systems of communication, have evolved from non-signal precursors. Movements, physical features, or chemicals that function in another context have secondarily acquired a signalling function (Tinbergen, 1964; Wilson, 1975; Liley, 1982). Territorial marking with urine by mammals is a fairly clear example of this (Liley, 1982). As defined and used pheromonal communication is a very general term including the highly specialized situations typical of insects, reptiles and mammals, as well as more rudimentary phenomena where individuals respond adaptively to chemicals associated with con specifics (Wilson, 1970; Wilson and Bossert, 1963). Liley (1982) has distinguished the general attribute of most animals from chemical signalling in which the release of the chemical implies an act of volition that in some way also serves to benefit the signaller. This is a useful distinction as situations that are only unilaterally beneficial or where mutual adaptations have not been demonstrated would otherwise be excluded from the concept of pheromonal communication. As an example, alarm substances are only clearly a benefit to the perceiver of the signal, yet they are commonly considered pheromones (Pfeiffer, 1974). The disadvantage to a broad definition for pheromones is that bulk chemicals with primarily structural or metabolic functions that also elicit responses from con specifics and represent little specialization are also included. The question arising from a comparison of marine invertebrate larvae with other animals, is how specialized is pheromonal communication in marine invertebrates? Larvae may simply be responding adaptively to metabolic by-products or excretory products that are leaked into the environment, much as larvae respond adaptively to other physical and chemical cues (Meadows and Campbell, 1972). Alternatively, this may represent true chemical signalling that has evolved and become specialized to the benefit of both the signaller and the perceiver. The un specialized condition, larvae responding to chemicals produced by conspecifics, appears from the examples given to be established for at least some

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gregariously settling marine invertebrates. What remains to be determined is if the mechanism has specialized to the extent that it can be considered similar to the chemical signalling characteristic of insects and some vertebrates. In the same way that larval searching behavior and sensory structures for the perception of chemical cues are taken as evidence that larvae seek certain habitats, specialization of the release of chemicals implies the attraction of conspecifics. Liley (1982) outlines several forms of evidence considered consistent with specialized signalling. These include: 1) elaborated secretory structures, 2) behavior involved in the release of the pheromone or its application to the substrate, 3) specialized chemical products, and 4) seasonally timed release of pheromones. For the most part there is very little information available on these aspects of gregarious recruitment in marine invertebrates. Organs involved in secretion of chemicals have not been clearly identified in any forms and behaviors associated with release, or seasonality of release, have not been documented. The observation that chemical cues are species specific suggest there may be specialization of chemicals, but without complete analysis of chemicals in two closely related forms, it is not possible to distinguish this from specialization of larval receptors. With the small amount of information available it is possible to suggest that gregarious settlement and metamorphosis mediated by adult derived chemical cues may be pheromonal communication in its most rudimentary sense. It appears to represent only a simple form of chemical communication, similar to that described for fish (Liley, 1982). Attempts must be made to identify the chemicals involved and their sites of secretion to determine the extent to which this represents more specialized pheromonal signalling. Although pheromonal communication is not known to be highly evolved in marine invertebrates, phenomena such as epidemic spawning, nuptual dances, trail following, alarm responses, and sexual congregations, which are all thought to be mediated by pheromones, suggest that chemical communication in marine invertebrates may be more elaborate than so far demonstrated. ACKNOWLEDGMENTS This research was supported

by a Natural Sciences and Engineering Research Council of Canada

University Research Fellowship and Operating Grant to the author. I am grateful to B. W. Bisgrove, A. W. Gibson and 1. J. King for their comments on the manuscript. LITERATURE

CITED

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in P. T. Grant and A. M. Mackie, eds. Chemoreception in marine organisms. Academic Press, London. ---. 1976. Settlement responses in marine organisms. Pages 83-124 in R. C. Newell, ed. Adaptations to environment: essays on the physiology of marine animals. Butterworths, London. --and P. S. Meadows. 1962. The chemical basis of gregariousness in cirripedes. Proc. Roy. Soc. London, Ser. B 156: 500-520. --and ---. 1963. Adsorbed layers: the stimulus to settlement in barnacles. Proc. Roy. Soc. London, Ser. B 158: 364-387. Crisp, M. 1977. The development of the serpulid Pomatoleios kraussii (Annelida: Polychaeta). J. Zool. Lond. 183: 147-160. Daniel, A. 1955. Gregarious attraction as a factor influencing the settlement of barnacle cyprids. J. Madras Univ. Sec. B 25: 97-107. Eckelbarger, K. J. 1975. Developmental studies of the post-settling stages of Sabel/aria vulgaris (Polychaeta: Sabellaridae). Mar. BioI. 30: 137-149. Fletcher, D. J. C. and M. S. Blum. 1983. Regulation of queen number by workers in colonies of social insects. Science 219: 312-314. Gary, N. E. 1974. Pheromones that affect ~he behavior and physiology of honey bees. Pages 200201 in M. C. Birch, ed. Pheromones. North Holland Publishing Co., Amsterdam. Highsmith, R. C. 1982. Induced settlement and metamorphosis of sand dollar (Dendraster excentricus) larvae in predator-free sites: adult sand dollar beds. Ecology 63: 329-337. Hughes, R. G. 1977. Aspects ofthe biology and life history of Nemertesia antennina (L.) (Hydrozoa: Plumularidae). J. Mar. BioI. Ass. U.K. 57: 641-657. Jensen, R. A. and D. E. Morse. 1984. Intraspecific facilitation of larval recruitment: gregarious settlement of the polychaete Phragmatopoma californica. J. Exp. Mar. BioI. Ecol. 83: 107-126. Karlson, P. and M. Luscher. 1959. 'Pheromones': a new term for a class of biologically active substances. Nature 183: 55-56. Keck, R., D. Maurer, J. C. Kauer and W. A. Sheppard. 1971. Chemical stimulants affecting larval settlement in the American oyster. Proc. Natl. Shellfish Assoc. 60: 24-28. Kiseleva, G. A. 1967. Influence of substratum on settlement and metamorphosis oflarvae of benthic fauna. Pages 71-84 in Benthic biocenosis and the biology of benthonic organisms from the Black Sea. Ukranian Acad. of Sciences, Kiev. Knight-Jones, E. W. 1949. Aspects of the setting behavior oflarvae of Ostrea edu/is on Essex oyster beds. Rapp. P.-V. Reun. Cons. Perm. Int. Explor. Mer 128: 30-34. ---. 1951. Gregariousness and some other aspects of the setting behavior of Spirorbis. J. Mar. BioI. Ass. U.K. 30: 201-222. ---. 1953. Laboratory experiments on gregariousness during setting in Balanus balanoides and other barnacles. J. Exp. BioI. 30: 584-598. --and J. P. Stevenson. 1950. Gregariousness during settlement in the barnacle Elminius modestus Darwin. J. Mar. BioI. Ass. U.K. 29: 281-297. Larman, V. N. 1984. Protein extracts from some marine animals which promote barnacle settlement: possible relationship between a protein component of arthropod cuticle and actin. Compo Biochem. Physiol. 77B: 73-81. ---, P. A. Gabbott and J. East. 1982. Physico-chemical properties of settlement factor proteins from the barnacles Balanus balanoides. Compo Biochem. Physiol. 72B: 329-338. Liley, N. R. 1982. Chemical communication in fish. Can. J. Fish. Aquat. Sci. 39: 22-35. Meadows, P. S. and J. I. Campbell. 1972. Habitat selection by aquatic invertebrates. Adv. Mar. BioI. 10: 271-382. Mladinov, P. V. and F. S. Chiao 1983. Development, settling behavior, metamorphosis and pentacrinoid feeding and growth ofthe feather star Florometra serratissima. Mar. BioI. 73: 309-323. Moore, B. P. 1974. Pheromones in the termite societies. Pages 250-266 in M. C. Birch, ed. Pheromones. North Holland Publishing Co., Amsterdam. Mykytowyzc, R. 1974. Odor in the spacing behavior of mammals. Pages 327-343 in M. C. Birch, ed. Pheromones. North Holland Publishing Co., Amsterdam. Pfeiffer, W. 1974. Pheromones in fish and amphibia. Pages 269-296 in M. C. Birch, ed. Pheromones. North Holland Publishing Co., Amsterdam. Pilger, J. 1978. Settlement and metamorphosis of Echiura: a review. Pages 103-112 in F. S. Chia and M. E. Rice, eds. Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York. Pyefinch, D. A. and F. S. Downing. 1949. Notes on the general biology of Tubularia larynx Ellis and Solander. J. Mar. BioI. Ass. U.K. 28: 21-43. Rice, M. E. 1978. Morphological and behavioral changes at metamorphosis in the Sipuncula. Pages 83-102 in F. S. Chia and M. E. Rice, eds. Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York.

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Riehl, R. M., T. O. Toft, D. M. Meyer, G. L. Carlson and T. C. McMorris. 1984. Detection of a pheromone-binding protein in the aquatic fungus Achlya ambisexualis. Exp. Cell Res. 153: 544549. Scheltema, R. S. 1974. Biological interactions determining larval settlement of marine invertebrates. Thalassia Jugosl. 10: 263-296. ---, I. P. Williams, M. A. Shaw and C. Loudon. 1981. Gregarious settlement by larvae of Hydroides dianthus (Polychaeta: Serpulidae). Mar. Ecol. Prog. Ser. 5: 69-74. Seki, T. and H. Kan-no. 1981. Induced settlement of the Japanese abalone, Haliotis discus hannai, veliger by the mucous trails of the juvenile and adult abalones. Bull. Tohoku Reg. Fish. Res. Lab. 43: 29-36. Straughan, D. 1972. Ecological studies of Mercierella enigmatica Fauvel (Annelida: Polychaeta) in the Brisbane River. J. Anim. Ecol. 41: 93-136. Suer, A. L. and D. W. Phillips. 1983. Rapid, gregarious settlement of the larvae of the marine echiuran Urechis caupo Fisher and MacGinitie 1928. J. Exp. Mar. BioI. Ecol. 67: 243-259. Tinbergen, N. 1964. The evolution of signaling devices. Pages 206-230 in W. Etkin, ed. Social behavior and organization among vertebrates. University of Chicago Press, Chicago. Vandenbergh, J. G., J. S. Finlayson, W. J. Dobrogosz, S. S. Dills and T. A. Kost. 1976. Chromatographic separation of puberty accelerating pheromone from male mouse urine. BioI. Reprod. 15: 260-265. Veitch, F. P. and H. Hidu. 1971. Gregarious setting in the American oyster, Crassostrea virginica Gmelin: I. Properties of a partially purified "setting factor." Chesapeake Sci. 12: 173-178. Williams, G. B. 1976. Aggregation during settlement as a factor in the establishment of coelenterate colonies. Ophelia 15: 57-64. Wilson, E. O. 1970. Chemical communication within animal species. Pages 133-156 in E. Sondheimer and J. B. S. Simeone, eds. Chemical ecology. Academic Press, New York. ---. 1975. Sociobiology: the new synthesis. Harvard University Press, Cambridge. 697 pp. --and W. H. Bossert. 1963. Chemical communication among animals. Rec. Progr. Hormone Res. 19: 673-716. Wilson, D. P. 1968. The settlement behavior of the larvae of Sabel/aria alveolata (L.). J. Mar. BioI. Ass. U.K. 48: 387-435. ---. 1970. Additional observations on larval growth and settlement of Sabel/aria alveolata. J. Mar. BioI. Ass. U.K. 50: 1-31. Young, C. M. and L. F. Braithewaite. 1980. Larval behavior and post-settling morphology in the ascidian Chelyosoma productum Stimpson. J. Exp. Mar. BioI. Ecol. 42: 157-169. --and F. S. Chiao 1982. Factors controlling spatial distribution of the sea cucumber Pso/us chitonoides: Settling and post-settling behavior. Mar. BioI. 69: 195-205. DATEACCEPTED: February 17, 1986. ADDRESS: Department of Biology, University of Victoria, Victoria, B. C. V8 W 2 Y2, Canada.