Energetics, competency, and long-distance dispersal of planula larvae ...

Marine Biology

Marine Biology 93, 527-533 (1987)

. . . . . . .

9 Springer-Verlag 1987

Energetics, competency, and long-distance dispersal of planula larvae of the coral Pocillopora damicornis R. H. Richmond Marine Laboratory, University of Guam, UOG Station; Mangilao, Guam 96923, USA

Abstract

Pocillopora damicornis (Linnaeus) were collected from Enewetak Atoll, Marshall Islands, in 1980-1981) and Kaneohe Bay, Hawaii, in 1982. Their planula larvae contained 17% protein, 70% lipid, and 13% carbohydrate by dry weight. Calculations based on stored energy reserves and daily metabolic expenditure indicate that planulae could survive approximately 100 d and still settle successfully. Competency experiments demonstrated that larvae settled and metamorphosed after 103 d. This period of time is sufficient to allow immigration of larvae from the Central Pacific to the eastern Pacific, and supports the hypothesis of long-distance dispersal of larvae for the origin of present eastern Pacific populations of P. damicornis.

Introduction

The scleractinian hermatypic coral fauna of the tropical eastern Pacific is relatively poor (11 species), compared to that of the Central Pacific (approximately 250 species), the Indo-West Pacific (over 300 species), and the Caribbean Sea (over 50 species) (Wells, 1954; Smith, 1971; Stehli and Wells, 1971; Glynn and Wellington, 1983). Two opposing (yet not mutually exclusive) types of hypotheses have been proposed to explain the origin of this eastern Pacific fauna: vicariance hypotheses that emphasize the roles of tectonic activity, extinctions, and speciation in the modification of pre-existing faunas (Rosen, 1975; Heck and McCoy, 1978) and dispersal hypotheses that emphasize the importance of long-distance dispersal of coral larvae (planulae) and rafting of adult colonies from the Central Pacific to the eastern Pacific (Dana, 1975; Jokiel, 1984). In the present paper, I demonstrate that planulae of the panPacific coral Pocillopora damicornis (Linnaeus) remain competent for periods long enough to allow immigration from the Central Pacific to the eastern Pacific, I describe a

technique for predicting the amount of time larvae are able to maintain the ability to settle successfully and metamorphose (competency period), and I discuss the implications of long-range dispersal of coral planulae.

Materials and methods

Pocillopora damicornis (Linnaeus) in Hawaii and the Marshall Islands is a simultaneous hermaphrodite, which releases brooded planula larvae each month of the year, with a lunar periodicity (Richmond and Jokiel, 1984). The larvae are lipid-rich, averaging 7.5 cal per mg ash-free dry weight, receive translocated metabolites from their zooxanthellae, and can feed while in the planktonic stage (Richmond, 1982, 1985 a). Two distinct forms of P. damicornis occur in Hawaii: Type "B" is brown, has fine branch tips and small planulae; Type "Y" is yellow, has stout branch tips, and large planulae. The two types co-occur on the reef flat, but reproduce at different times (Richmond and Jokiel, 1984). Larvae from both types ofP. damicornis, collected from Enewetak Atoll, Marshall Islands, in 1980-1981 and from Kaneohe Bay, Hawaii, in 1982, were used in the following experiments. Larval constituent analysis Three pellets, containing 100 planulae each, were combusted at 500 ~ for 3 h to determine percent ash. Protein of newly released larvae was measured using a modified Lowry protein technique (Umbreit etal., 1972), with NaOH as the extraction solvent (n=3 samples of five larvae, 2 replicates). Lipid of newly released larvae and of larvae maintained under light and dark treatments for 10 d prior to analysis was measured gravimetrically. Fifty to 100 planulae from each treatment were placed into gelatin capsules, frozen, and lyophilized. Lipids were extracted in three 1-ml washes of 2:1 (vol) chloroform: methanol (Christie, 1973). Virtually all of the lipid was

528 removed from the larvae by the third wash, as determined in preliminary tests. Total lipid content was measured by placing 0.1 ml aliquots of the extractions into pre-ashed, pre-weighed aluminum pans. The solvent was evaporated at 60 ~ and the pans were reweighed. The total weight of lipid for each treatment was divided by the total weight ofplanulae used in the treatment to give percent lipid by dry weight (Table I). Additional 0.1 ml aliquots were placed onto thin-layer chromatography (TLC) plates, which were coated with a 250#m layer of silica gel G (Analtech, Inc.). The TLC plates were heat-activated and run with chloroform to remove the plasticizer prior to adding the samples. The plates were run in a solvent system of hexane:ether: formic acid, 80:20:2 by volume (Christie, 1973). The plates were developed in an iodine gas environment. Because ash level was less than 2% dry weight, dry weight is considered equivalent to ash-free dry weight for the larvae, and carbohydrate level was approximated by subtraction. For the purposes of this study, such an estimation was assumed to be satisfactory.

Larval metabolism Oxygen production and consumption by planulae were measured with a Yellow Springs Instruments Model 53 microrespirometry apparatus, using YSI No. 5331 oxygen electrodes. Oxygen levels were simultaneously measured in one chamber containing between 30 and 50 planulae and a control chamber containing only the incubation medium. Two milliliters of aerated Millepore-flltered seawater (0.45ktm) were added to each chamber. The chambers were housed in a constant-temperature water bath maintained at ambient seawater temperatures (28~ Each chamber contained a small stir bar to keep the water in motion. The planulae in the chambers behaved normally. At the beginning and end of each experiment, the two probes were run with seawater alone to assure they were matched and reading uniformly. Photosynthesis versus irradiance experiments ( P - / ) were performed to determine the light level at which the planulae/zooxanthellae association was light-saturated. The light source was a Kratos-Schoeffel Model SS 2500 solar simulator with a xenon arc lamp. Light levels were measured with a Li-Cor model LI-188 B integrating quantum radiometer/photometer, and were adjusted by the use of neutral-density filters. Once the saturation light-level was determined, experiments were performed to measure peak oxygen production. Experiments run in complete darkness measured combined respiration rates of the symbiotic zooxanthellae along with the animal host. Planulae were kept for one day in 75% seawater diluted to induce them to expel their zooxanthellae. These aposymbiotic larvae were run in light and dark trials to test for effects of light on the animal tissue, and to isolate the

R.H. Richmond: Competency and dispersal of coral planulae animal respiration component. These larvae behaved and swam normally during the course of the experiments. The P - I data were plotted using a hyperbolic tangent function for best fit (Chalker, 1981).

Competency experiments Larvae were collected at Enewetak as described by Richmond and Jokiel (1984). Batches of 100 larvae were pipetted onto a 125/~m screen, washed with Millepore-filtered seawater (0.45 ~m) to remove extraneous matter, and placed into 250 ml Erlenmeyer flasks. The flasks contained 200 ml of Millepore-filtered seawater, to which penicillin G was added to a concentration of 60/~g per ml (Switzer-Dunlap and Hadfleld, 1977). The flasks were placed in a flowing seawater table to maintain ambient seawater temperatures (ca. 28 ~ These outdoor tables had translucent fiberglass roofs, which filtered out ultraviolet light and reduced light levels to approximately 70% of ambient when the sun was directly overhead. Flasks were rewashed and the water was changed every two to three days. Larvae were removed at various times and placed on natural carbonate substrata which had been preconditioned in seawater. The longest experiments were terminated after 103 d.

Results

Larvae of Pocillopora damicornis contained less than 2% ash by dry weight (3 replicates, 100 planulae each). Newly released planulae averaged 17% protein, 70% lipid and 13% carbohydrate by dry weight (pooled values including both Types "B" and "Y"). Planulae which remained at the water surface (buoyant) contained approximately 17% more lipid than those that remained at the bottom of experimental vessels (non-buoyant). The planulae contain primarily wax and sterol esters and triglycerides (Fig. 1). Lipid levels of planulae (expressed as percent of total content) decreased over time (Table 1). Table 1. Pocillopora damicornis. Lipid content of planulae (buoyant and non-buoyant) measured soon after (10 to 11 d) or immediately after release from parent colony. Except for planulae designated buoyant and non-buoyant, individuals were selected at random. Numbers of planulae in pellets analysed are shown. Each determination was replicated and the two values averaged Larval type and no. ofplanulae Type B 300 75, 74, Type Y 100, 100, 50, 75,

% lipid by dry wt

10dinlight 10 din dark

70 54 66

non-buoyant ~ buoyant 11 dinlight 11 din dark

57,59 68 73 71

a Two pellets of 100 each

R. H. Richmond: Competency and dispersal of coral planulae

529 The planulae of the two Hawaiian forms of PocilIopora

damicornis differed in size and behavior, with the larger

Type Y larvae usually settling sooner than the smaller Type B (see Jokiel, 1985). Type B planulae that were maintained

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The resultant P - I cuives are presented in Fig. 2. Planulae reached light-saturation at light intensities between 200 and 250 # E m -2 s -1. The half-saturation constant (Ik) values were calculated as approximately 80/~E m -2 s -1. At saturation intensities, Pocillopora damicornis planulae produced a mean of 1.72 ( _ + 0 . 5 2 S D ) x 1 0 - 4 m g oxygen planula -1 h -~ (n = 15; Table 2). Oxygen consump-

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