Serotonin and dopamine have opposite effects on phototaxis in larvae of the bryozoan Bugula neritina.

Introduction

Regulation of the vertical distributions of pelagic larvae of marine invertebrates is most likely restricted to the vectoral factors of current velocity, light direction, and gravity (Crisp, 1984). Of these, most is known about the influence of light. Studies of the role of phototaxis in larval behavior were pioneered by Thorson (1964), who documented the photic responses exhibited by larvae of 141 species of shallow-water benthic marine invertebrates from 11 phyla. In Thorson's survey, the most frequently observed response to light was for larvae to be initially positively phototactic (82%). Only 6% responded negatively to light throughout larval life, and only 12% were indifferent to light. In 76% of the cases examined, larvae that were initially photopositive became photonegative before the end of the larval period. Apparently, an ontogenetically regulated switch governing the sign of phototaxis is found in larvae of many species. Positive phototaxis early in the larval period may bring larvae up into the water column and facilitate dispersal; later negative phototaxis may bring them down to the substratum where settlement occurs. In addition to changes in phototaxis during development, environmental signals may influence phototactic behavior of larvae (see Crisp, 1984; Young and Chia, 1987, for reviews). Factors such as temperature, salinity, light intensity, ionic shock, pH, exposure to chemical cues from settlement-specific substrates, and pollutants all have been implicated in environmentally induced changes in phototaxis.

Despite the wide phylogenetic distribution and ecological significance of larval phototaxis, very little is known about the internal mechanisms responsible for generating and modulating this behavior. This lack of knowledge stands in contrast to current understanding of the neural bases of stereotyped behaviors in many adult invertebrates. Although that literature is far too extensive to review here, it is important to point out a common theme that has emerged in the last two decades: Many behaviors are initiated, maintained, altered, or terminated by the action of monoamine or peptide modulators on neural networks (see reviews by Harris-Warrick and Marder, 1991; Katz, 1995). Examples involving monoamines include initiation of swimming in an annelid (Willard, 1981; Mangan et al., 1994); modulation of phototaxis, swimming, respiration, and feeding in gastropods (Crow and Forrester, 1986; McClellan et al., 1994; Syed et al., 1990; Wieland and Gelperin, 1983; Kyriakides and McCrohan, 1989); starting and stopping flight in an insect (Claassen and Kammer, 1985); and switching of body postures and modulation of pyloric motor output in decapod crustaceans (Livingstone et al., 1980; Flamm and Harris-Warrick, 1986).

Although evidence has been presented for the existence of neuroactive monoamines in the larvae of many marine invertebrates - including hydrozoans (McCauley, 1995; Walther et al., 1996), a nemertean (Hay-Schmidt, 1990a), a polychaete (Hay-Schmidt, 1995), bivalve and gastropod molluscs (Coon and Bonar, 1986; Goldberg and Kater, 1989; Marois and Carew, 1990; Barlow and Truman, 1992; Pires et al., 1992), several echinoderms (Toneby, 1980; Burke, 1983; Burke et al., 1986; Bisgrove and Burke, 1986, 1987; Nakajima, 1987, 1988; Thorndyke et al., 1992), brachiopods (Hay-Schmidt, 1992), phoronids (Hay-Schmidt, 1990b,c), a hemichordate (Dautov and Nezlin, 1992), and a cephalochordate (Holland and Holland, 1993) - less is known of the roles of these compounds in the mediation or modulation of larval behaviors. Monoamines have been implicated in the control of metamorphosis in a variety of taxa including hydrozoans (McCauley, 1995; Walther et al., 1996), polychaetes (Biggers and Laufer, 1992; Okamoto et al., 1995), gastropods (Couper and Leise, 1996; Pires et al., 1995), bivalves (Coon and Bonar, 1987; Bonar et al., 1990; Chevolot et al., 1991; Kingzett et al., 1990), a barnacle (Yamamoto et al., 1996), and an echinoid (Burke, 1983). Effects of monoamines on ciliary locomotion have also been reported. Bath-applied dopamine (DA) induces ciliary reversal and backward swimming in some echinoid plutei (Lacalli and Gilmour, 1990; Mogami et al., 1992), while serotonin (5HT) increases the speed of forward swimming (Mogami et al., 1992). Serotonin also accelerates ciliary beat frequency in encapsulated embryos of the gastropod Helisoma trivolvis, while DA has no effect (Diefenbach et al., 1991; Goldberg et al., 1994). However, no data have been published on the regulation of larval phototaxis by monoamines or any other neuroactive substances.

Bryozoans are excellent material for experimental studies of larval phototaxis because most species retain their early developmental stages and, on stimulus of light, release larvae that generally settle within a few hours of eclosion. Cohorts of larvae all released within a few minutes of each other can thus be obtained. Ryland (1976, 1977) reviewed in detail the early studies of the phototactic behavior of bryozoan larvae, and several important conclusions come from these studies. First, a range of responses to light are possible, depending on the species. During the course of its larval existence an individual could remain neutral to light throughout; react positively throughout; change from positive to negative or positive to partial negative; and change from positive to alternation between positive and negative (Ryland, 1960). Second, in larvae of Bugula flabellata and B. turrita, it is possible to artificially force a switch in photic response with agents such as elevated pH, hypotonic seawater, or CuCl (Lynch, 1947). Third, in larvae of Cryptosula pallassiana, a rise in temperature decreases the photopositive phase, but the amount of illumination has no effect on the rate of change in sign of the response to light (Ryland, 1962). Furthermore, Ryland observed that pipetting larvae also results in an immediate change from positive to negative phototaxis.

Larvae of many species with phototactic responses possess pigmented epidermal structures that, on the basis of anatomical criteria, are assumed to be photoreceptors (Ryland, 1976, 1977). Not all species with larvae that orient to light have pigmented "eyespots," however (Ryland, 1960); in these species, other specialized epidermal cell types are hypothesized to be photoreceptors (Zimmer and Woollacott, 1989). To date, all pigmented ocelli of bryozoan larvae examined at the ultrastructural level have been based on a sensory cell with an elaboration of multiple cilia that are thought to be the receptoral organelles (Woollacott and Zimmer, 1972; Hughes and Woollacott, 1978, 1980; Reed et al., 1988).

We selected Bugula neritina for detailed investigation of the monoaminergic control of phototaxis in the larvae of marine bryozoans. B. neritina is cosmopolitan in temperate to tropical waters and is often abundant in specific locales at certain times of the year.…