Lunar Control of Epitokal Swarming in the Polychaete <I>Platynereis

BULLETIN OF MARINE SOENCE, 52(3): 911-924, 1993

LUNAR CONTROL OF EPITOKAL SWARMING IN THE POLYCHAETE PLATYNEREIS BICANALICULATA (BAIRD) FROM CENTRAL CALIFORNIA

Peter P. Fong

ABSTRACT Lunar control of epitokal swarming in the polychaete P/atynereis bicana/icu/ata (Baird) was tested in laboratory experiments employing artificial moonlight. Worms were exposed to the following daylength and lunar conditions: A) in-phase daylengths with: i) artificial moonlight for 6-7 nights/month centered near ambient full moon, ii) centered near am bient new moon, and iii) constant "moonlight", and B) in-phase daylengths with: i) artificial moonlight for 14 nights/month during the period of ambient full moon, ii) centered near ambient new moon, and iii) constant "moonlight." Worms exposed to artificial moonlight for 6-7 nights in phase with full moon swarmed only on "moonless" nights. Those exposed to "moonlight" out of phase with full moon showed field entrainment (swarming during the period of ambient new moon) for the first month, then swarming mainly on "moonless" nights. The pattern of swarming of worms held under continuous "moonlight" suggests a possible circa-semi-lunar rhythm. Exposure to 14 nights (during ambient full moon and new moon) of "moonIight" resulted in entrainment for the first 2 months, followed by a I-month period of "adjustment" or "clock re-setting" to the imposed pattern of artificial moonlight, thereafter, a pattern of swarming mainly on "moonless" nights. These results suggest that individuals of P. bicanaliculata have an endogenous rhythm entrained by moonlight which is manifested in a circa-lunar swarming rhythm, and the gradual decline in illumination from full moon to last quarter moon is probably the cue that synchronizes swarming at the population level. This is the first experimental evidence of lunar-synchronized reproductive rhythm in a marine invertebrate from the west coast of North America.

Lunar control of reproductive events such as spawning or release oflarvae has been documented in a number of marine animals including corals (Jokiel et al., 1985; Babcock et al., 1986), chitons (Yoshioka, 1989), crabs (Saigusa, 1988), sea urchins (Pearse, 1972, 1975; Kennedy and Pearse, 1975; Iliffe and Pearse, 1982), and reef fishes (Robertson et al., 1990); see reviews by Korringa (1947) and Pearse (1990). Polychaete worms have provided especially good examples (Lillie and Just, 1913; Just, 1914; Hauenschild, 1960; Foster, 1978; Caspers, 1984; Franke, 1985; Hardege et al., 1990); see review by Olive and Clark (1978). Hauenschild (1955, 1956, 1960) demonstrated experimentally that moonlight could synchronize the timing of epitokal metamorphosis and swarming in a Med- iterranean population of the polychaete Platynereis dumerilii. Using artificial moonlight in the laboratory, he showed that worms swarmed mainly during the period of new moon, and were synchronized to swarm at this time by the cessation of nocturnal illumination about 14 nights earlier. Moreover, a fixed phase rela- tionship exists between the end of the "moonlight" period and the spawning maxima even when the duration of "moonlight" was extended. Roe (1975) observed highly synchronous summer spawning of Platynereis bicanaliculata in Washington State. In central California, P. bicanaliculata occurs commonly amongst algae, surfgrasses, and in holdfasts in low intertidal zones (Abbott and Reish, 1980). Worms have been observed swarming in Monterey Bay during the spring and summer on moonless nights when extreme high tides occur at midnight (Ricketts et al., 1985). Blake (1975) contends that the environmental cue for epitokal metamorphosis in this species is the light of the full moon, since heteronereids, eggs, and larvae were found in plankton samples from

911 912 BULLETINOFMARINESCIENCE,VOL.52, NO.3, 1993

Tomales Bay, California during the following new moon period when moonlight is minimal. At Soquel Point, along the northern coast of Monterey Bay, California, mats of mucus-bound surfgrasses and algae containing Platynereis bicanaliculata are found from September through to early June. Benthic heteronereids are found during the spring, and nocturnal swarming (2-10 worms/m3) has been observed during the May 1991 new moon at the Santa Cruz Wharf, about 4 km away (M. Silver, pers. comm.). By mid-June, very few mats are left, most worms having spawned out and died. Larval recruitment probably occurs throughout the late spring and summer. Growth is mainly during fall and winter. In the present study, laboratory experiments employing artificial moonlight were performed to test the effect of lunar cues in the control of the timing of epitokal swarming in a Monterey Bay population of P. bicanaliculata.

MATERIALS AND METHODS

Collection Site and Experimental Design. -Specimens of Platynereis bicanaliculata were collected in 1989, from surfgrass-algal mats on an intertidal mudstone reef at Soquel Point, (36°57'N; I 22"O'W). Worms in mats were transported to the laboratory, removed from their tubes, counted (except in experiment 2), and placed in tubs (50 cm wide x 50 cm long x 35 cm deep; 25 cm-tall stand pipe) covered by light-tight wooden boxes and supplied with running sea water. Worms were given algae and surfgrasses on which to rebuild tubes and were fed blades of the kelp Macrocystis pyrifera once a week. To simulate daylight, each tub was illuminated by a fluorescent light (GE F40 Daylight), and the duration of illumination depended on the particular experiment. Daylengths were controlled by time switches (Astronomic Time Switch, R.W. Cramer & Co., Type SY Model SOL). To simulate moonlight, a dim (0.4 /lEm-2 sec-I) incandescent night light was affixed into each wooden box. "Moonlight" was on (I2h/night) for either 6-7 nights (experiment I), 14 nights (experiment 2) or constantly to act as a control (both experiments). During some experiments, night-length was less than 12h, and in these cases the "moonlight" came on before the end of the daylight period. In each tub, the stand pipe was covered with a plastic mesh which caught sexually-mature worms as they emerged from their tubes and swam in the water column. Worms adhering to the mesh were counted each day. Experiments were run until all worms had swarmed, and none remained in any of the tubs. Laboratory Experiments. - EXPERIMENTI. THEEFFECTOFARTIACIALMOONLIGHTFOR6-7 CONSECUTIVE NIGHTS PER MONTH. To investigate the effect of artificial moonlight on the timing of swarming, approximately 450 worms were collected on 9 April 1989, and placed in three tubs (150 worms/tub). Three treatments were established: "moonlight" for 6-7 nights (12h/night) centered around the period of ambient full moon, "moonlight" for 6-7 nights (12h/night) centered around the period of ambient new moon, and constant "moonlight" (control). All three treatments were maintained under in-phase daylength regimes. EXPERIMENT2. ARTIACIALMOONLIGHTFOR14 CONSECUTIVENIGHTSPERMONTH.To ascertain what part of the lunar cycle Platynereis bicanaliculata uses as timing cues for swarming, young worms were exposed to "moonlight" for 14 consecutive nights. If worms cue on the beginning of the moonlight cycle then one would expect a swarming pattern similar to that of experiment I. If, however, the end of the moonlight cycle is the cue, swarming should occur only after the 14 nights of "moonlight" have ended. Worms were collected from algal clumps on 12 November 1989. Clumps containing worms were weighed, equal amounts placed in each of three tubs, and subjected to the following artificial lunar regimes: "moonlight" for 14 nights during the period of ambient full moon, "moonlight" for 14 nights during the period of ambient new moon, and constant "moonlight" as a control. Initially, the first night "moonlight" was turned either on or off was within 1-2 nights of the ambient moon (either full or new). However, from November 1989 through March 1990, there were either 15 or 16 nights between ambient full and new moon, but laboratory moonlight changed only every 14 nights, More- over, in late January 1990, the "moonlight-on" and "moonlight-oW was accidentally delayed by a few days. Thus, by April 1990, the timing of the "moonlight-on" or "-oW' was near the center of each ambient moonlight period. All three treatments were maintained under in phase daylength regimes.

RESULTS Experiment 1. The Effect of Artificial Moonlight for 6-7 Consecutive Nights per Month. -Artificial moonlight had a strong effect on the timing and frequency of epitokal swarming. A total of98 worms exposed to "moonlight" during the period o o A 8 • •

o 11 21 11 21 31 11 Apr 1989 May June

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o 11 21 11 21 11 Apr 1989 May 31 June Figure 1. Running averages of swarmers exposed to the following conditions of artificial moonlight, A) "moonlight" for 6-7 consecutive nights centered around the period of ambient full moon, B) "moonlight" for 6-7 consecutive nights centered around the period of ambient new moon, and C) continuous "moonlight." Worms were collected on 9 April 1989. Trends were smoothed using 3-interval running averages (values were calculated by averaging the number of swarmers on each day with the number on the previous day and the following day. Thus some days (25 May in A) show an average value of swarming but actually had no swarming events. Open circles: ambient full moon; closed circles: ambient new moon. Open bars indicate times of artificial moonlight: closed bars indicate no nocturnal illumination. 914 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.3, 1993

14 A

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Figure 2. Percent ofswarmers exposed to A) "moonlight" for 6-7 nights centered around the period of ambient full moon, B) "moonlight" for 6-7 nights centered around the period of ambient new moon; both during lunar cycles (days after the first night of artificial moonlight) from April-June 1989, and C) constant "moonlight." FONG: LUNAR CONTROL OF SWARMING IN PLATYNERE1S 915

Table I. Platynereis bicanaliculata. Mean swarming date for each lunar month in all experiments. A lunar month begins with the first day after artificial moonlight was turned on until the last day before they were again turned on. Ambient lunar months were used for all constant "moonlight" treatments. Dates of new moons are those on which artificial moonlight was turned off, except where the dates of ambient new moons are used (indicated by *). IP: artificial moonlight (12 h'night-') during the period of ambient full moon (in phase); OP: artificial moonlight (12 h·night-') during the period of ambient new moon (out of phase); constant: continuous artificial moonlight

Mean Dates of lunar month swarming date Date of new moon Lunar period Experiment I 19 Apr.-I 8 May 1989 6 May 24 Apr. (5 May·) IP 20 May-I 8 June 2 June 24 May (3 June·) IP 4 May-31 May 17 May 10 May OP 23 Apr.-20 May 6 May 5 May· constant 21 May-I 9 June 3 June 3 June constant Experiment 2 14 Nov.-12 Dec. 1989 1 Dec. 28 Nov.· IP 13 Dec. 1989-11 Jan. 1990 26 Dec. 28 Dec.· IP 12 Jan.-9 Feb. 27 Jan. 26 Jan.· IP 12 Feb.-9 Mar. 1990 4 Mar. 22 Feb. IP 10 Mar.-4 Apr. 28 Mar. 21 Mar. IP 5 Apr.-2 May 23 Apr. 15 Apr. IP 3 May-29 May 20 May 15 May IP 30 May-26 June 14 June 12 June IP 14 Nov.-12 Dec. 1989 I Dec. 28 Nov.· OP 13 Dec. 1989-11 Jan. 1990 23 Dec. 28 Dec.· OP 29 Jao.-22 Feb. 13 Feb. II Feb. OP 23 Feb.-21 Mar. IS Mar. 8 Mar. OP 22 Mar.-18 Apr. 8 Apr. 4 Apr. OP 19 Apr.-I 5 May 4 May 2 May OP 16 May-I 2 June 3 June 29 May OP 13 June-IO July 29 June 26 June OP 14 Nov.-I 2 Dec. 1989 23 Nov. 28 Nov. constant 13 Dec. 1989-11 Jan. 1990 25 Dec. 28 Dec. constant 12 Jan.-9 Feb. 31 Jan. 26 Jan. constant 10 Feb.-II Mar. 26 Feb. 25 Feb. constant 12 Mar.-10 Apr. 24 Mar. 26 Mar. constant 11 Apr.-9 May 26 Apr. 25 Apr. constant 10 May-8 June 27 May 24 May constant

of ambient full moon (hereafter "in phase" with full moon) swarmed only on "moonless" nights (Fig. 1A). Swarmings began immediately after the "moonlight" was turned off, but peak swarming occurred between the 16th and 19th lunar days· (Fig. 2A). Mean swarming dates for both lunar months were within 1 d of the ambient new moon (Table 1). The pattern of swarming by a total of95 worms exposed to "moonlight" during the period of ambient new moon (hereafter "out of phase" with full moon) was not as clear (Fig. lB). Similar to in-phase worms, out-of-phase worms began swarming 12 nights before the ambient April full moon. Thereafter, swarming ceased for 10 nights, then resumed again for 6 of7 additional nights. Subsequently, "moonlight" was applied, and additional worms swarmed, but more did so after the "moonlight" was turned off 7 nights later. During the next "moonlight" period, no worms swarmed, but they resumed swarming im-

• A "lunar day" was defined as a certain day afler the fIrSt night artificial moonlight was turned on (e.g., in experiments 2 and 3). 916 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.3, 1993 mediately after the "moonlight" was again turned off, Worms swarmed contin- uously during the "moonless-night" periods, but peak swarming occurred between the 6th and 8th lunar days (Fig. 2B). The mean swarming date for the only complete lunar month (4-31 May) was 17 May, 7d after the "moonlight" was turned off (Table 1). A total of 72 worms exposed to constant "moonlight" swarmed on most nights for over 2 months, and showed definite swarming peaks around the period of ambient new moon (Fig. 1C), with the highest percentage of swarmings occurring between the 13th and 17th lunar days (Fig. 2C). The mean swarming dates for both lunar cycles fall within 1 d of ambient new moon (Table 1). Small peaks occur around the period of ambient full moon, and the frequency of swarming was significantly non-random (Mean square successive difference test, Zar, 1974, C = 0.327, P < 0.005). The mean time interval between successive peaks was 12.75 days. Particularly notable was a group of swarmings that peaked from 25- 26 April, mirroring similar peaks in the other two treatments (Fig. lA, B, C). Experiment 2. Artificial Moonlight for 14 Consecutive Nights. -A total of 304 worms swarmed under conditions of "moonlight" in phase with full moon. Worms showed effects of being entrained (i.e., an external zeitgeber (moonlight) was synchronizing an endogenous rhythm) by field lunar conditions in November and December 1989 (Fig. 3). During these months, swarmings occurred repeatedly under both "moonlight" and "moonless" conditions, but most swarmings took place after the time of the ambient full moon. The highest percentage ofswarmings occurred between the 8th and 10th lunar days (Fig. 4A) and the mean swarming dates for these first 2 lunar months were within 3 d of ambient new moon (Table 1). January to early February 1990 was a period during which few swarmings occurred, with no clear relation to laboratory moonlight (Fig. 3). Yet, the mean swarming date for this lunar month was within 1 d of ambient new moon (Table 1). This may be a treatment effect in that worms were "re-setting" an internal clock to a different lunar cycle. Treatment effects changed from February through June. During these months, swarmings occurred mainly on "moonless" nights (Fig. 3). The highest percentage of swarmings during this time became skewed to the right, and occurred between the 15th and 22nd lunar days (Fig. 4A). A total of 236 worms swarmed under conditions of "moonlight" out of phase with full moon. Those that swarmed in November and December 1989 showed an irregular swarming pattern but with definite peaks after ambient full moon (Fig. 5). Similar to in-phase conditions, very few swarmings occurred in January. From February through early July 1990, further treatment effects became appar- ent. During these months, swarmings occurred mainly on "moonless" nights (Fig. 5) with the highest percentage of swarmings on the 15th lunar day (Fig. 4B). A much smaller number (91 total) of worms exposed to constant "moonlight" swarmed (Fig. 6), and the pattern of swarming was significantly non-random (normal approximation to the mean square successive difference test, Z = 4.17, P < 0.0005). The mean time interval between peaks was 12.9 days.

DISCUSSION Critical events in the life cycle of numerous organisms have been shown to be rhythmic in nature, and under lunar or semi-lunar control. Such events include larval release in Sesarma haematocheir, a semi-terrestrial crab (Saigusa, 1988), emergence in Clunio marinus, a marine insect (Neumann, 1966), and gamete release in Dictyota dichotoma, a brown alga (Bunning and Muller, 1961). Many of these studies were stimulated by the seminal work ofHauenschild (1955, 1956, FONG: LUNAR CONTROL OF SWARMING IN PLATYNERE1S 917

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Figure 3. Running averages (calculated as in Fig. I) of swarmers exposed to "moonlight" for 14 consecutive nights during the period of ambient full moon from November 1989-June 1990. All worms collected on 12 November 1989. Open circles: ambient full moon; closed circles: ambient new moon. Open bars indicate times of artificial moonlight; closed bars indicate no nocturnal illumination. 918 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.3, 1993

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1 2 3 4 5 6 7 8 9 1011 1213 1415 1617 18 1920 21 2223 2425 262728 29 30 lunar day Figure 4, Percent of swarmers during lunar cycles (days after the first night of artificial moonlight) exposed to A) "moonlight" for 14 consecutive nights during the period of ambient full moon; solid line: from November 1989-January 1990; dashed line: from February-June 1990, B) "moonlight" for 14 consecutive nights during the period of ambient new moon; lines same as in A, and C) constant "moonlight" from November 1989-June 1990,

1960) on the polychaete Platynereis dumerilii. His studies using artificial moonlight at night were the first experiments to show lunar control of epitokous swarming in a marine animal. Lunar control of such swarming in polychaetes has now been well documented (see Schroeder and Hermans, 1975 and Olive and Clark, FONG: LUNAR CONTROL OF SWARMING IN PLATYNEREIS 919

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Figure 5. Running averages (calculated as in Fig. I) of swarmers exposed to "moonlight" for 14 consecutive nights during the period of ambient new moon from November 1989-June 1990. All worms collected on 12 November 1989. Open circles: ambient full moon; closed circles: ambient new moon. Open bars indicate times of artificial moonlight; closed bars indicate no nocturnal illumination. 920 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.3, 1993

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Figure 6. Running averages (calculated as in Fig. I) of swarmers exposed to constant "moonlight" from November 1989-June 1990. All worms collected on 12 November 1989. Open circles: ambient full moon; closed circles: ambient new moon. FONG: LUNAR CONTROL OF SWARMING IN PLATYNEREIS 921

1978 for reviews). The well known palolo worm, Eunice viridis of the tropical western Pacific swarms around the time of third quarter moon (Caspers, 1961; Hauenschild et aI., 1968; Caspers, 1984). Stolons of the syllid, Typosyllis prolifera swarm synchronously in the field just before full moon, and can be entrained to swarm in the laboratory by exposure to more than two nights of artificial moonlight (Franke, 1985). Peak stolon abundance occurs about 17 d after the "moonlight" was turned off suggesting that the cessation of natural moonlight is a cue for swarmmg. In the present study, Platynereis bicana/iculata exposed to artificial moonlight in phase with ambient full moon for 6-7 nights only swarmed on "moonless" nights over a two-month period. However, their response could have reflected field entrainment (i.e., the worms were already synchronized by previous monthly cycles of moonlight and were committed to swarm at the next new moon period independent oflaboratory conditions). Those worms exposed to "moonlight" out of phase with full moon showed an initial field-entrained swarming pattern, but by the second cycle, worms only swarmed on "moonless" nights. Particularly notable were the six-day periods from 18-24 May and 1-6 June. During each of these periods, worms in one box swarmed on "moonless" nights, while at the same time, in an adjacent box, no worms swarmed in "moonlight." Thus, it appears field entrainment can last for 1-2 months, after which, worms can be lab- entrained to swarm on cycles of artificial moonlight lasting 6-7 consecutive nights (Fig. 1) or 14 consecutive nights (Figs. 3, 5). In experiment 2, worms showed field entrainment in November and December, but very few swarmed from January to early February, and it is suggested that worms were "adjusting" or "re-setting" an internal clock to a cycle of 14 "moonlit" nights. The periodicity of such a clock is unknown but it might normally be set by the monthly cycle of moonlight. That worms in experiment 2 waited 14 "moonlit" nights before swarming suggests that P. bicana/iculata uses the end rather than the beginning of the moonlight period as a cue to synchronize swarming. The presence of small swarming peaks around the period of ambient full moon in the first month of experiment 1, together with the peak swarming intervals of about 13 days in the "constant moonlight" treatments of both experiments 1 and 2, suggests a possible semi-lunar component to the overt swarming rhythm. Such a circa-semi-lunar swarming rhythm has been recorded in Platynereis dumerilli from the west coast of France (Fage and Legendre, 1927; Durchon, 1970), and the Adriatic Sea (Georgevitch, 1938). However, in the present case, this rhythm cannot be considered truly free-running since the daylength regimes (in phase with ambient) were not "constant." Knowing the periodicity of such a free-running rhythm and how it is entrained by moonlight would be necessary in order to elucidate the mechanism of the lunar swarming periodicity. To my knowledge, this is the first experimental evidence for lunar-synchronized reproductive rhythm in any marine invertebrate from the west coast of North America, and the pattern of swarming is similar to that of P. dumerilii from the Mediterranean Sea. Hauenschild (1960) found that the cessation of nocturnal illumination was the cue for the completion of sexual maturation, onset of epitokal metamorphosis, and swarming in this species. Furthermore, in the laboratory, P. dumerilii responds to this cue by swarming about 18 d ("reaction time") after artificial moonlight was turned off. Hauenschild proposed that an underlying endogenous rhythm, entrainable by moonlight, caused the observed swarming synchrony. His evidence for this was the finding that the swarming synchrony was maintained for 4 cycles (months) under constant "moonless" conditions after 922 BULLETIN OF MARINE SCIENCE, VOL. 52, NO.3, 1993 the "moonlight" was turned off. Field-entrained laboratory swarming synchrony in P. bicanaliculata has been observed in the absence of any moonlight for 2 cycles (unpubl.). Olive and Garwood (1983) and Olive (1984) have proposed models to explain how exogenous factors act on endogenous rhythms to produce reproductive synchrony within individuals and populations of polychaete species. In P. dumerilii, moonlit nights act as entraining zeitgebers to an endogenous circa-lunar rhythm. This rhythm is of the "gated" type, and the gate delimits periods when the nnal stages of gametogenesis may be initiated ("gate-open" period). The results from the present study suggest that like Platynereis dumerilii from the Bay of Naples, P. bicanaliculata from Monterey Bay, California has an endogenous, moonlight-entrained rhythm which is manifested in an overt, circa- lunar swarming rhythm, and the gradual decline from full moon to last quarter moon is probably the cue that synchronizes swarming. In the neld, the "gate- open" period occurs around 7 d after full moon, with a reaction time of about 7 d. Thus, neld-entrained worms swarm about 14 d after full moon. This explains the high frequency of swarming around the time of new moon, and also the high percentage of swarming near the 14-16th lunar days in neld-entrained worms (Fig. 2C). In all experiments, worms were not exposed to a gradual decline in nocturnal illumination, rather "moonlight" was turned off abruptly. Hence, the "gate-open" period was about 1 d after the "moonlight" was turned off, with a reaction time of about 7 d. This explains the high percentage of swarmers on or near the 15th lunar day in experiment 1 (Fig. 2A) and near the 22nd lunar day in experiment 2 (Fig. 4A). It is difficult to explain the peaks in percent swarming around the 15th lunar day in experiment 2 (Fig. 4A, B). Hauenschild (1960) observed a similar pattern in P. dumerilii. He suggested that some worms were responding to the onset of the "moonlight" period instead of the end. Platynereis bicanaliculata represents a valid and useful North American model to tease apart the nuances of lunar-controlled reproductive rhythms in marine animals. Ascertaining the periodicity of the free-running rhythm under "constant" conditions, and incorporating "moonlight" for varying numbers of nights and night-lengths would be necessary in order to elucidate further the mechanisms controlling the lunar swarming rhythm in this species.

ACKNOWLEDGMENTS

I thank J. S. Pearse, A. T. Newberry, R. I. Smith, and an anonymous reviewer for commenting on the manuscript. J. T. Tomlinson suggested calculating running averages. Facilities at Long Marine Laboratory were provided by the Institute of Marine Sciences, and I thank its director Dr. W. Doyle. I thank the numerous undergraduates who faithfully checked our lab over the years, and M, E, Steele who coordinated the daily lab checking schedule. Funding was provided by the Biology and Marine Science Boards, University of California, Santa Cruz, and grants from Sigma Xi, the Earl and Ethel Myers Oceanographic and Marine Biology Trust, and the Friends of Long Marine Laboratory. This work was done in partial fulfillment of the requirements for the Ph.D. degree at the University of California, Santa Cruz.

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DATEACCEPTED: June 18, 1992.

ADDRESS: Biology Board oJStudies. University oJCalifornia, Santa Cruz, California 95064; PRESENT ADDRESS: Department oj Physiology, Wayne State University, Detroit, Michigan 48201.