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Il. H. Seliger, J. H. Carpenter, M. Loftus, W. H. Biggley, and W. D. McElroy2

McCollum-Pratt Institute, Department of Biology, Chesapeake Bay Institute, and Department of Earth and Planetary Sciences, The Johns Hopkins University, Baltimore, Maryland 21218

Bioluminescence and phytoplankton successions during 1969 indicate large oscillations from the stable Pyrodinium bahumense populations normally associated with bioluminescent bays. A mathematical model is proposed which relates meteo,rological conditions to positively and negatively phototactic dinoflagellate populations. The model and additional circumstantial evidence indicate that Bahia Fosforescente may no longer be a stable bioluminescent bay.

Bioluminescent bays provide unique opportunities for tho study of plankton dynamics in microco8sm, in a reasonably closed ecosystem where the bioluminescent species appears to be dominant. The relatively small areas of the bays and their mangrove drainage basins ( 2.C5.2 km2) simplify the logistics of following, on a regular basis, perturb,ations of water cxchange rates, flushing patterns, nutrient levels, turbidities, and distributions of organisms. The predictability elf species composition should provide controls for meaningful laboratory-culture stimulation of competition kinetics and nutritional physioIogy. In the biohmincscent bays Fire-Lake on New Providence Island in the Bahamas (Harvey 1952), Oyster Bay near Falmouth, Jamaica, W.I. (Sdiger et al. 1962), Bahia Fosforescente and Bahia Monsio Jos6 near La Parguera, Puerto Rico (Margalef 1957), and Puerto1 Mosquito, Vieques, Puerto Rico (Seliger et al. 1969)) the tropical marine photosynthetic dinoflagellate Pyrodinium bahamense has been reported to be responsible folr the
l Contribution No. 649 of the McColhnn-Pratt Institute, The Johns Hopkins University. Research supported by Atomic Energy Commission Contract AT (30-l) 3480 and by Office of Naval Research Contract Nonr. 4010 ( 16). 2 Present address: Director, National Science Foundation, Washington, D.C.

observed bioluminescence. It appears that bioluminescent bays contain persistent populations o#E P. bahamense in a dynamic equilibrium between effective flushing rate and generation rate (Seliger et al. 1970). However, dinoflagellate and particularly P. bahamense populations in Bahia Fosforescentc during 1969 were extremely unstab~le. Table 1 shows the temporal scqucnce observed folr the major dinoflagcllatcs in Bahia Fosforesccnte. Over and above the complex succession observed in the main central region of the bay, dense populations of Coch8ZicZinium polykrikoides were localized in the northwestcrm arm and dense populations of Peridinium quinquecorne were usually found in a localized arca of the northeast arm. In this paper we attempt to extend the mechanisms of dinoflagellate accumulatioa previously demonstrated for Oyster Bay (Scliger et al. 1970) to the different physiography and more variable meteorology of Bahia Fosforcscente. A model is proposed, with basic features applicable to all bioluminescent bays, which can predict the successions and distributions observed in Bahia Fosfo,rescente.

Margalef (1961) measured salinity, phyand chlorophyll distributions toplankton, of the so,uthwest coastal area of Puerto
JULY 1971, v. lG(4)


BIOLUMINESCENCE TABLE 1. Temporal sequence

AND PIIYTOPLANKTON of major dirioflagellutes

SUCCESSIONS in Bahia Fosforescente



P. bahamense

Concentrations C. furcahircus

G. splendens


May Jun Aug



high low, dying nbscnt very high very high absent absent

high low absent low low ? high

absent very high very high absent absent ? absent

P. bahamense P. bahamense

P. bahumense P. bahamense

Peridinium Polykrikos


* Personal observation G. Cintrh, University of Puerto Rico Marine Station. t Personal observation W. Maddux, University of Puerto Rico Marine Station. Only P. bahamense was looked for.

Rico, including Bahia Fosforcscente, during a 12-month period in 1957-19158. IIe identified 8 species of dinoflagellates regularly found in the bay. His abundance data were based on qualitative net tows and showed only relative population densities. For 23 of 25 samples in Bahia Fosforcscente during the 12-month interval P. hahamense was the dominant dinoflagellate species. If we arbitrarily set Margalcfs maximum net-tow values for P. bahamense at 100, the yearly mean relative dinoflagellate abundances (calculated from Table X of Margalef 1961) are as given in Table 2. There were periolds during 19571958 when P. bahamense concentrations decreased significantly, although it was never absent from the bay. There have been only occasional microscopic counts of dinoflagellate distributions in Bahia Fosforescente. Margalef ( 1961) determined P. bahamense surface concentrations of up to 100 P. bnhamense/ml 0x1 12 August 1958; Clarke and Breslau (1960) counted a single sample (8 P. bahamense/ml) on 9 February 1959; Gold (1965) reported a depth distribution at a single position on 5 February 1965, showing only 2 P. bahamense/ml. Very localized high concentrations of C. polykrikoides in the northwest arm have been reported by Margalef ( 1961) and by Burkholder ct al. ( 1967). There are in addition the follolwing qualitative ,descriptions of the dinoflagcllates in the bay: Coker and Gonzalez (1960) rcportcd

that a microscopic examination of drops of water taken from various parts of a jar of water that gave luminesccncc at night required some little searching to find occasional individuals of PyrodinHum, and one Ceratium furca, Prorocentrum, or two other dinoflagellates. This suggests that great density of populations of dinoflagellates is not requisite for bright luminescence. Glynn et al. ( 1964) reported, after Hurricanc Edith on 26-27 September 1963, that the concentration of dinoflagellates was typically high, but C. furca greatly outnumbered P. bahamense.

Distributions o,f bioluminescent intensity were measured with a tolwablle underwater photometer (Scliger et al. 19691). Plankton samples for microscopic identification and counting as l-ml samples were freshly captured and o,bserved both alive and stained in Rhodes iodine solution. Stimulable bioluminescence was measured in the laboratory by stirring (Biggley et al. 1969) or by injection of single isolated organisms: into a bmeakcr of folrmalin solution sitting on the flat fact of an electron multiplier phototube. Salinity was measured with a calibrated portable induction salinometer. Chlorophyll a was determined after filtration and extraction by grinding into 90%
3 These dinoflagellates have been identified as or C. hircus. We use Margalefs notation including both names.
C. furca




Yearly mean relative dinoflagellate TABLE 2. abundances (calculated from Margalef 1961) 1957-1958 mean (relative to max for P. bahnmeme) 70 Total opuf ation (%I 60

Species Pyrodinium bahamense Peridinium divergens Ceratium furca hircus Ceratium fusus Dinophysis caucluta ventricosa Pyrophacus horologium

21 17.5

18 15

2 1 0.8 0.5

1.7 0.9 0.7 0.4

Peridinium oceanicum Prorocentrum micans

acetone as described by Parsons ( 19$6). Exchange rates were measured using, the Rhodamine B dye-tracer technique (Carpenter and Seliger 1968).

Our microscopic counting data for 1969 for both P. bahamense and C. furca hircus are summarized in Table 3. The implications of the ratio in the last column will be discussed later. Pyrodinium baham,ense is confined to the main central area of the bay and is associated with four other g,enera, Ceratium (furca hircus), Profocentrum (micans) , Dinop hysis (caudata) and several species of the larger thecated Peridineae, ( depressum, diuergens, and oceanicum). Isocons (lines of equal concentrations) for P. bahamense during a period of high surface concentrations (January) are shown in Fig. 1. Isolum,es (lines of equal stimulable biolum,inescent intensity) for P. bahamense in a uniformly mixed bay during this same period are shown in Fig. 2. During the end elf April and the bcginning of May P. bahamense was repIaced completely by Gymnodinium splendens. This succession was accompanied by the death and decomposition of the P. bahaEvery water sample mense population. observed microscopically showed P. bahamense in various stages of decomposition, while C. furca hircus (in 101~ concentration), P. micans (in higher than normal concentrations), and G. spZendens all ap-

peared healthy and were actively swimming. Concentrations elf G. splendens, from several hundred up to several thousand per milliliter, visibly discolored the water and appeared as brown patches, By 3 May except for an occasional P. bahamense and C. furca hircus observed near its eastern short, the central bay was devoid of both of these dinoflagellates. Only G. splendens and P. micans, the latter up to lOO/ml, were present. The bay was not bioluminescent. Peridinium quinquecorne remained in the area of the northeast arm (Fig. 1). On 4 May strong southeast winds pushed G. splendens into the northwest arm and C. polykrikoides could not be found. During the latter half of May and the first half of June, high chlorophyll a concentrations in the bay (due to G. splendens) decreased exponentially. By 16 June the bay was again brightly biolumdnescent and a surface sampIe near its center contained many P. bahamense and few if any other dinoflagellates (Cintron 1x9). This condition continued through August. During Novcmbcr the visually observed bioluminescence was low. On 28 Novcmbcr P. bahamense was completely absent ( Maddux, personal communicatioa) . During December we observed an entirely different plankton ,distribution from that of the rest of the year; the mean concentration of P. bahamense was 15/ml and that of C. furca hircus was up to 55/ ml ( Table 3). In addition a) neither G. splendens nor P. micans could bc found; b) although predator populations were more than 10 times higher in December than in the previous January and August (Table 4), the chlorophyll a of ultraplankton standin.g crop (organisms passing through a 35-p net) remained essentially unchanged (between 2-3 mg/m3); c) stimulable bioluminescence was observable during the day as well as during the night, due to both Peridinium sp. (<35 p) and Polykrikos sp. Measurements of tem,peratures and salinities in Bahia Fosfo,rescente allow a description of the circulation patterns bc-

BIOLUMINESCENCE TABLE 3. Counting data for Pyrodinium




bahamense (A) and Ccratium furca hircus (B) both expressed

in No./ml ye?th m 0 0 0 No. of samples

Date (1969)

Location (see Fig. 1)


22 Jan 24 Jan 25 Jan 27 Jan

28 Jan 29 20 21 3 4 16 19 21 28 8 9 10 Jan Apr Apr May May JunS Aug Aug Nov Dee Dee Dee

11 Dee 12 Dee

Transect 3-6 Transect l-dock-5 Transect 3-6 Center of the bay 100 m SE of 4 Between dock-5 Transect 3-6 Mouth of bay Mouth of bay Mouth of bay Center of bay Center of bay Center of bay Center of bay Center of bay Transect 2-6 Entire bay Transect 2-3 Entire bay Center of bay Entire bay Entire bay Central area of bay Entire bay Entire bay Entire bay 50 m N of 2 Center of bay All stations

o-4* 0.3 0.5 O-3 0 1 2 0 04 0.5 0 0.3 0.15 o-2* 0.1 0.1 0 O-3 o-3* o-0.1* 0.15 O-3 0 0.3 O-3 0

12 9 13 8 1 11 20 3 3 3 2 : 1 2 8 30 3 13 1 22 13 9 5 19 9 6 3 7

40 34 16 26 68 19 34 0 10 2 50 65 19 25 11 10 -0 2-3 -0 100 49 43 0 2 2 1 2 0 1

37 32 26 56 103 65 51 1 3 2 20 :i 13 20-30 I-0 2-3 -0 low 12 12 45 55 41 74 62 70

0.52 0.52 0.4 0.3 0.4 0.2 0.4

0.5 0.7 0.5 0.3 0.7 <0.3

>0.8 0.8 0.8

0.04 0.04 0.02 0.03 0.00 0.01

* Integrated sample. $ Not determined. $ Cintrh 1969. 5 Net tow.

dicate the effects of seasonal conditions on the bay and adjacent coastal waters: In December, there was a calm period of several weeks; in August, the easterly winds blew daily. In this semiarid region the dry porous soil rapidly absorbs light rainfall. Only heavy downpours succeed in diluting the bay water. In view of these facts the difference in the T-S structure between December and August is taken crt = [ (0.97264 + 8~)~~- I] X 1W g/cm3, to be a funlction of the variation in daily where: 0.97264 = specific volume of 35,%0 evaporation effected by insolation and seawater at OC and l-aim pressure and & wind. is the thermosteric anomaly. In August ,thc isoplcths of ot were inThe August and December T-S plots inclined, indicating horizontal water flow

twcen the central portion of the bay and athe coastal waters. Vertical crags sectionIs of salinities along a north-south transect through the mouth of the bay are shown in Fig. 3. These vertical cross sections arc drawn to sholw isopleths of temperaturesalinity ( T-S) and density (at) under three different conditions. Values of ( ct) were calculated as :




bahamense in Bahia Fosforescente (No/ml) at 14 cm around 1400 FIG. 1. Isocons of Pyrodinium hours, 22 January 1969. Concentrations were determined by microscopic counting. The depth distribution of P. bahumense at the center of the bay (point A) is shown in the left inset. The hatched area in the northeast arm represents a zone of high concentration of a single Peridin8ium species, up to several hundred per milliliter. A small area of lower concentration was found in the center arm. The crosshatched area in the northwest arm is an extremely dense (up to 8,OOO/ml) population of CochZodinium polykrikoides. The strongly phototactic depth distribution of C. polykrikoides is shown in the top left inset. At the bottom of the figure are shown the mean relative abundances of the five major genera of dinoflagellates found in the central region of the bay (1-P. bahamme; 2-Cemtium fwca micans; S-Dinophysis cauduta uentricosa), excluding hircus; 3-Peridinium spp.; Prorocentrum the very localized Cochlodinium and Peridinium zones in the northwest, center, and northeast arms.





FIG. 2. Lines of equal nocturnal bioluminescent intensity in Bahia Fosforescente at OS m around 2030 hours on 28 January 1969 expressed as concentrations of Pyrodinium bahamenselml (Seliger et al. 1969).

under the influence of gravity. On the basis of the c+t isopleths, the outflow of bottom water and inflow of surface coastal water was greater in August than in Dc-

cembcr. The inequality between the volume of coastal water necessary to achieve any observed change in salinity and the volume provided by the tidal flow sug-


II. 11. SELIGER, J. H. CARPENTER, TABLE 4. Counting Sa.;$~w nique* data

M. LOFTUS, W. I-1. BIGGLEY, AND W. D. MCELROY populations expressed in NOB/liter Tintinnids small

for predator

Date (1969)




GastroAnBarOiko- pod ve- Bivalve nelid nacle Trochpleura ligcr veliger larvae nauplii ophore


plankton ) . -t Not determined. $ In order of dominance:

25 27 28 19 8 9 10 11 *

Jan Center Jan Center Jan Center Aug Center Dee Entire bay Dee Entire bay Dee Entire bay Dee Center l----two liters concentrated

1 1 : 2 2 2 2

20 13 10 # 500

71 31.5 14 I

11 ;-f $ -

6 -

3 2 2

4 l-2 I-

1 -

3 3 2

2 3-4 t t

ii t 3

500 1,500

tz1311 -

300 600 500 1,000

with 35-p netting; B-microscopic Oikopleura, copepods, tintinnids.

counting of l-ml samples (same samples as phyto-

Center Arm



Coasta I Water

Center Arm



Coasta I Water

- . . . . . . . . . . . . . . . . 22.5 . . . . . . . . . . . . . . . em.............






I 0.2

I 0.4

I 0.6





FIG. 3. Temperature, salinity, and density isopleths in a north-south vertical cross section through the mouth of Bahia Fosforescente in August when Pyrodinium bahamense was at maximum concentration (period of prevailing winds) and in December when it was absent (calm period). Dashed lines: temperature ( C) ; solid lines: salinity ( go) ; dotted lines: density ( it see text). (a) 19 August 1969; 0930-1130 hours; southeasterly wind 8-24 km/hr; clear sky; flood tide. (b) 21 August 1969; 0740-0900 hours; no wind; clear sky; low ebb tide. (c) 8 December 1969; 15001630 hours; no wind; clear sky.





gests that as much as 2/3 of the exchange of bay water with coastal water is due to density flow. The rate of exchange of Bahia Fosforescente waters with the coastal waters during January was observed by tagging the bay waters with Rhodamine B. The dye was released by injecting 16O-ml portions of a 30% solution ,through a tube that opcncd 1.5 m below the surface at positions throughout the bay. On the morning of the next day the dye was observed throughout the water column with uniform mixing to depths of 4 m. Within 24 hr, the water containing dye had mixed into the tributary arms and was observable outside the entrance to the b,ay. Samples were collected folr fluorescence analysis during the next 6 days. The inventory of dye in the bay, calculated for each day, is plotted in Fig. 4. The exchange process is exponential. The exchange rate constant for Bahia Fosforesccnte for January was 0.22&l.

X 1.0 090.6 07 0.6 -

0.5 0.4 0.3 -

0.2 -

0.1 I, 0




Exchange of dye tracer in Bahia Fosforescente with coastal waters as a function of time. The first order rate constant lc,O= 0.22&.

FIG. 4.

The model presented is an analytical extension of the partial mechanism proposed by Margalef ( 1961) for Bahia Fosforescente. As an accumulation mechanism it is based on dinoflagellate migration (Epplcy et al. 1968) and has features in common with several of the convergence mechanisms (LeFevre and Grall 1976) propssed to explain the appearance of red tides . The data of Tables 1 and 3 would hardly permit us, to predict the recurrence of P. bnhamense in Bahia Fosforcsccnte or to conclude that we are dealing with a stable bioluminescent bay, The year-round persistence and high concentrations of P. bahamense in Oyster Bay, Jamaica, WI., are characteristic of a precise and constant balancing of all driving forces (wind, tide, rainfall, sunlight, nutrients, temperature, competition, predation) and of a highly damped system. Bahia Fosforesccnte, as a result of rno,re variable and seasonal meteorological conditions than occur in Oyster Bay, oscillates

about its equilibrium state, that elf high concentrations of P. bicchamerwe. On the basis of the data presented and also of our previous description of dinoflagellate accumulations in Oyster Bay (Seliger et al. 1970) we can develop) a model for Bahia Fosfolrcscente. We propose the following three coaditions as sufficient for a model bioluminescent bay: 1. Shallow basin with confined shallow entrance from the sea. 2. Prevailing and daily-occurring winds blowing perpendicular to the entrance or into the bay, 3. Mangrove drainage area surrounding the bay. These conditions have been discussed by Margalef ( 1957, 1961). Wall and Dale (1969) present in addition a palaeoecological interpretation based on the occurrence of P. bahamerw spolres in semienclosed, shallow-water bays of a littoral facies. We will also estab,lish two pa.ram;cters to define the equilibrium state of a biolumincsccnt bay: the concentrations and the ratios of P. bahumense and C. furca hircus. Mean concentrations of P. bahamense greater than 40/ml and P.b. : P.b. + C.f.h. ratios greater than 0.9 (see last column of Table 3) define the equilibrium state.



Relative .04 .08 .I 2 Concentration .I6









FIG. 5. bahamense

Depth distributions of Pyrodinium ( l ) and Ceratium furca h&us (+ ) in Bahia Fosforescente in bright sunlight and in the presence of a wind sufficient to vertically mix the P. bahamense population (5-8, km/hr).

Lower values than these are evidence of (so far) periodic changes both in meteorological coaditions and organism distributions. Pyrodinium bahamense is positively phototactic in direct (97,060 lux) tropical sunlight (Seliger et al. 1970). Under these same conditions C. furca hircus exhibits negative phototaxis. In the presence of wind that tends to mix the water of the bay, the net (phototaxis masked by vertical mixing) depth distribution will depend strongly on the swimming rates of the olrganisms . Microscopic observation of both P. bahamense and C. furca hircus reveals that the latter swims at abolut twice the 30 cm/hr rate of the former and also tends to swim in straighter lines,. In the presence of a light wind (5-8 km/hr) sufficient to mix the P. bahamense population, C. furca h&us can maintain its negatively phototactic distribution ( Fig. 5). We divide the meteorological conditions under which Bahia Fosforescente is to, be examined into two general cases; the most frequent one in which the prevailing winds

are diurnal, coming up around 0900-1000 hours and dying down around 1600 hours, and the less frequent in which there are extended periods of calm. In the first case: 1. After dawn (060&0900) the positive and negative phototactic distributions for P. bahamense and C. furca hircus are es,tab,lished. 2. Beginning at 0900 the wind blows gently into the bay, forcing the surface layers ( enriched in P. to the ) rear of the bay. The wind acts to incline the isopleths of ot as shown in Fig. 3, and therefore there is an olutflow of higher density waters from the 2-3-m depths of the channel. Since the bay is hypersaline these outgoing waters will find their density level at much lower depths outside of the entrance and thus be lost to the bay. Owing to the negative phototaxis of C. furca hircus the waters at depths of 2-3 m which are forced out of the bay will have been enriched in these ,dinoflagellates. Thus in the presence elf daily winds, positive phototaxis reduces the loss of P. bahamense while negative phototaxis accelerates the loss of C. furca hircus. In the second case: 1. A flooding tide will tend to pile up the slightly lower salinity coastal waters on the hypersaline bay surface. 2. During the day the positively phototactic P. bahamense will migrate into this surface layer. 3. When the tide cbbs this surface layer will leave the bay. Since this. surface layer contains enriched concentrations oE P. bahamense there will be an accelcratcd loss of P. bahamense from the bay. By virtue of its negative phototaxis, C. furca hircus will be least affected by this sloshing movement 0E surface waters. 4. In the absence of wind the isopleths of ot will no,t be as steep and the outflolw of higher density waters at the 2-3-m depths will be reduced. The exchange rate determined by the dye-tracer technique is a measure of the mean volume exchange of the bay with





(4) Thus in bioluminescent bays the cell division rate constant can be less than that of dye-tracer exchange. This is indeed the case for P. bahumense, whose optimum division rate constant is. between 0.15-0.2 d-l (Biggley et al. 1969) as compared with kpo of 0.22&1. We must make a further assumption that the concentration of P. bahamense is partially self-limiting, presumably due to the depletion of chemical nutrients or to dA/dt = [k/ - k/ - k/PA] A + kfAo, ( 1) self-shading in sunlight. Otherwise the same division rate constant which would where kgA is cell division rate constant, kTA permit an inoculum; to thrive in the bay is the organism flushing-loss rate constant, kpA is the predation rate constant, PA is the would soon overpopulate it. We have alconcentration of predators elf A, and kl is ready demonstrated in laboratory cultures the exchange rate constant given by the that kg for P. bahamense can vary over a factor of 5 as a function of nutrient condye-tracer technique. Since we have observed essentially no centrations. WC can therefore express kgA change in the rate of accumulation of as natural populations elf P. bahumense as kgA= kgaA[l+P(Am-A)] (5) compared with unialgal ( predator-fret) where kgmAis the divisioln rate constant for laboratory cultures and with P. bahamense concentration (A = Aa), in filtered bay water, we assume that in the equilibrium Bahia Fosforescente PA N 0. We express and p is a scaling constant. Substituting into. equation (1) we obtain kfA in the form: kfA = kf(lcxd), (2) dA/dt = [kg&1 + pAn) - kpA]A - ( kgEAj?)A2 + kfoAo. From equation We now define (5) (7) (6)

coastal waters. The bay becomes uniformly mixed within a short time after introduction of the dye, so the technique does not discriminate between surface and bottom waters and therefore gives the exchange rate of all other uniformly distributed components of the bay, i.e., nutrients and plankton whose photoltactic displacements are negligible. The c.ffcctive exchange rate for phototactic organisms is therefore different from the dye exchange rate. If we let A and A,, represent the concentrations of P. buhumense in the bay and in the coastal waters respectively, we can write the following rate equation:

tration of P. bahamense, and dA/dt = 0. Since we approach a steady state only when the wind blows, or when aA > 0, we have from equation (3) kgA < kp?

where o!A is the correction to the dyeexchange rate constant due toI the phototaxis of P. bahumense and is positive when the diurnal wind blows and negative when it dots not. The cell division rate constant is a complex function of light intensity, available nutrient concentrations, and growth-promoting or growth-inhibiting substances washed out elf the mangrove drainage area or excreted by other species, which we label I, N, and X, rcspectively. Equatioln ( 1) then becomes : (3) For an ideal bioluminescent bay A N A, > AO where AH is the equilibrium concendA/dt = [k/(1, N, X) - kpo(l- a)]A + kfoAo.

(kgA)max = k,tiA(l + &b)-

which is positive when the wind and negative when it dots not. Equation (6) reduces to


1 dA 7cgEAp dt



The solution of equation (9) satisfying the initial conditions that A = AO at t = 0, and neglecting AO relative toi AB, is




KA Equation (10) can be further simplified. When the wind blows we have conditions leading to an equilibrium population denpLro;n;quations (5), (7), and (8),
A I#

A cd (1 + AI.7/Ao)e-A7t&! lwind) (I)


AkgA 1 = (kgA)rnnx (absolute - kfA1

value). (12,)

When there are periods, of calm following periods of diurnal wind, KA is negative and equal to -Aa ( AkgA) calm/(hk, ) wind. -KA
A = (I_ KA/&) e&,At-l (calm), ( 13)

During calm permds KB will be positive only if kgn is large enough to overcome both kfO and ankfO, This is different from the conditions for kgA above and in effect places more stringent requirements on the retention of negatively -pholtotactic orgaNordli nisms in bioluminescent bays. (1957) has reported optimum, cell division rate constants for C. furcu hircus between O.4-O.5&1, in agreement with the requirements of the model. Thus under corrditions where KA is positive, KD is negative and vice versa. In Oyster Bay, where KA is, always positive ( Carpenter and Seliger 1968), ratios of P.b. : P.b. + C.f.h. are 0.99 and P. bahamense mean concentrations are about lOO/md.


can be approximated
A N AEe-AkoAta


As defined in equation ( 8)) KA is a parameter of the system,. It is proportional to the net organism accumulation rate constant. When the wind blows, KA is positive and we observe exponential growth toi an equilibrium value oE AE. During calm. periocls, KA is negative and P. bahamense concentrations decrease exponentially. Equation ( 11) is characteristic of the conditions in Oyster Bay, Jamaica, and possibly in Puerto Mosquito, Vieques, where the wind patterns are constant for extended periods. In the case of C. furca. hircus we can write an equation in B the same as equation ( 1). However, owing to the negative phototaxis and the inclined isopleths of Fig. 3 ( a), aB of equation ( 2) an,d KR are negative when the wind blows. The solutions for C. furca hkcus have the same form as for P. bahumiensq except that when the wind blows, regularly C. furcu hircus decreases exponentially. B N Bae-AJgBt(wind), and during Bcalm periolds &3 (calm). 1 + ( Bn/Bo) e-A7cgut (16) (15)

Only a special combination of geololgic events will produce conditions for a bioluminescent bay. Bahia Fosforescente lies along the southern edge of the volcanic upland that forms the mountainous core of Puerto Rico (U.S. Dep. Interior 1968). The entrance to the bay is, formed by a steep downward fold in limestone that allows the sea to flow into the basin behind, formed by weathering and erosion of the contact zone between the limestone and bods of volcanic debris. It is some 3.2 km east of La Parguera on the southwest coast of Puerto Rico and within a rainshadow ( average yearly rainfall about 750 mm) produced by the high central mountains of Puerto Rico. The La Parguera area is protected from the force of the sea by a series of east-west parallel reefs. Many of the inner reefs rise above sea level and have mangrove growths, Because of the protection afforded by reefs there is essentially no wave action along the mangrove coastal areas and La Parguera is reported never to have suffered noteworthy damage even from hurricanes. The open water of the bay comprises about 19 ha surrounded by mangrove growth (Rhixophoru mungi%) of about the same extent (Coker and Gonzalez 1960). The approximate bo,ttom contours are shown in Fig. 6. Thcrc are








FIG. 6.

Depth contours of Bahia Fosforescente obtained by leadline sounding ( 1969).

several arbitrary regiolns that can be de:lineated. The first is the main central area of the bay encompassed by the 3-m contour. Second are the shallow areas occupied by the three drainage arms of the bay, l-1.5 m deep. Third is the secondary buffer basin comprising the mouth of the bay and extending south of the mouth foIr a distance of about 200 rn,. Farther south the bottom contours drop to about 6 m. There are therefore two) impediments to

rapid exchange of bay waters with coastal waters, the constrictive mouth of the bay itself and the shallow basin of which it is a part. Were it not for this initially low value of k!O, positively phototactic dinoflagellates could not begin to accumulate against the exchange gradient. The concentrations 0.f P. bahamense and C. furca hircus measured in Bahia Fosforesccnte during 1969 arc plotted in Fig. 7. The lines through the points have been








FIG. 7. Concentrations of Pyrodinium bahamense (solid lines) and Ceratiunz furca hircus (dashed lines) during 1969. The points plotted are taken from the microscopic counting data of Table 4 and are the weighted averages for any particular day. The arbitrary curves through the points have been drawn to agree with the mathematical model and with the qualitative visual observations reported in the text.

drawn to be self-consistent with the mathematical model. The disappearance of P. bahumense during April is not pre.dicted by this model, since C. furca hircus also disappeared. The second loss of P. bahumense in December is consistent with the model and with the observations of a lack of wind, since C. furca h&us was folund at high concentrations. A slight modification is required toI explain the April data. Like P. bahamense, G. splendens is positively pholtotactic at the full intensity of tropical sunlight. It is an even stronger and m,orc persistent swimmer than C. furcn h&us. Positively phototactic depth distributions were maintained by G. splendens even in the presence of normal 8-16 km/hr southeasterly winds. The average value of ac will therefore be greater than the average value of aA and of the same sign. In addition WC have observed values of 7cgcin laboratory culture between 0.4-0.7d-l. Thus in the presence of diurnal winds Ku > KA and

dC/dt > dA/dt. Even though Co < AO, the model predicts that G. spZenSdens should rapidly overtake and overwhelm P. bahamense. Thus, G. splendens should bc the dominant dinoflagellate in Bahia Fosforesccnte and presumably in any other bsioluminescent bay. Why do we normally observe P. bahamense to the exclusion of G. splendens? We will make only one assumption relative to kg0 for G. spkendens, which is consistent with our experim,ental observations. This is that the requirements of G. spZendens for nutrients, growth factors, or bolth, are much different than for P. bahamense so that in the pristine bay kg 4 kgA, and in the coastal waters Co N 0. Margalef ( 1957, 1961)) although listing dozens of rare dinoflagellate s,pecies in the La Pargucra area including Bahia Fosforescente, as the result of extensive net tows over many months in 1956, 1957, and 1958, did not note this large (70 p), highly pigmcntcd dinoflagellate. Since this area is semiarid and the





ground is porous, only heavy rains will produce any appreciable runoff into! the bay, For about 2 weeks during the latter half oS April 1969, there were very heavy rains followed by diurnal winds. It was only after this extensive runoff into the bay that the G. splenclens succession was observed. We believe that the decomposition of P. bahamense during the G. splendens succession is due to the fact that the P. bahamense were shielded from sunlight, which appears to be an absolute t daily requircmcnt for them, by the dense brown surface patches of G. splendens kl covering the ceater of the bay. Since heavy rainfalls are quite common in this area, we might infer that in 1969 the runoff contained soIm,erequirement for G. splendens which was not present in previous years. A further link in the chain of circumFIG. 8. ProDosed variation of k, with nutrient or growth factor concentrations (N, X) for PyTostantial evidence comes from our predadinium bahamense ( A), Gymnodinium splendens tor observations. Ultraplankton show very limited excursions due to) phototaxis, and ( C ) , and ultraplankton ( U ) in order to account for observed plankton distributions. au N 0. The solution of equation ( 1) fair ultraplankton must include predation, with net-filtered concentrations of bottle-captured (whole bay) samples. In Decembler the whole bay samples were nolt concentratcd, since we observed a copepod, a In Oyster Bay and previously in Bahia tintinnid, or both, in almost every one of Fosforesccntc it has always been possible the l-ml samples colunted (n = 66). to collect predator-free blay water (filtered Coker and Gonzalez (1960) do not prothrough a 20-p net) and to keep it folr 1 or vide quantitative estimates of predator 2 days without its becoming visibly turbid populations in Bahia Fosforescente. Holwand dense with ultraplankton. However in ever the conccntratioas we observed in December even predator-free b,ay water di- Deccmbcr were so high that it is unlikely lutcd 1 : 20 with 0.45p-filtered bay water these authors would have allowed similar became turbid within 12 hr, indicating a high concentrations in 1960 to pass unThis is noticed. rapid turnover of ultra-plankton. corroborated by the unusually high predThe December observations of the cxator concentrations sho;wn. in Table 4. tremely rapid growth of ultraplanktoa For plankton examination whole bay when the predators, were removed imply samples were captured in a codleeting bot- that kgu in the bay water was very large, tle and live and preserved subsamples in much larger than kfo. small petri dishes were compared under In August and December the concentra10-100~ magnification. Next aliquots of tioas of ultraplankton standing crop were the preserved wholle bay sam,ples were dc- the same, based on chlorophyll CL. If we livered to l-ml counting cells, and all now compare the August and December dinoflagellates and zooplankton within the predatosr concentrations in the light of l-ml volume were tabulated. The conccnequation (17) we conclude that kgu in the trations referred to in Table 4 ( * 1) are bay can undergo extremely large variations.





On the basis of separate experiments with confined populations in Oyster Bay, we found that k,U increased tremendously with added nutrients in the form of fcrtilizcr, while kgA remained essentially constant. Combining this information with our assumption of a threshold in N, X for kgCywe propose that the types of relationships shown in Fig. 8 ( No, X0) for the pristine bay are well below the threshold values for G. splendens. Thus it is possible that at present the nutrient levels in coastal waters and in runoff into the bay can accommodate high predator concentrations where kgu is appreciably greater than ktO. In periods of calm G. splendens as well as P. bahanzense will be absent and C. furca h&us will dominate. In periods of diurnal wind G. splendms will dominate. It is possible therefore that the development of this area of Puerto Rico1 has, resulted in much higher average coacentrations of ( N, X ) in Bahia Fosforescente as well as in coastal waters and in the elimination of P. bahameme as the dominaz dirroflagellate species in the bay.

B 1111. using a portable bathyphotometer. Inst. Oceanogr. 1171, p. 1-31. COKER, R. E., AND J, G. GONZALEZ. 1960. Limnetic copepod populations of Bahia Fosforescente and adjacent waters, Puerto Rico. J. Elisha Mitchell Sci. Sot. 76: 8-28. EPPLEY, R. W., 0. HOLY<-HANSON, AND J. D. STRICKLAND. 1968. Some observations on the vertical migration of dinoflagellates. J. Phycol. 4: 333-340. GLYNN, P. W., L. R. ALMODOVAR, AND J. G. GONZALEZ. 1964. Effects of Hurricane Edith on marine life in La Parguera, Puerto Rico. Carib. J. Sci. 4: 335-345. GOLD, K. 1965. A note on the distribution of luminescent dinoflagellates and water constituents in Phosphorescent Bay, Puerto Rico. Ocean Sci. Eng. 1: 77-80. HARVEY, E. N. 1952. Bioluminescence. Academic. 646 p. LEFBVBI, J., AND J. R. GRALL. 1970. On the relationships of Noctiluca swarming off the western coast of Brittany with hydrological features and plankton characteristics of the environment. J. Exp. Mar. Biol. Ecol. 4:


spontaneous bioluminescence in the marine dinoflagellates Pyrodinium bahamense, Gonyaubax polyedra and Pyrocystis lunula. J. Gen. Physiol. 54: 96-122. BURKIIOLDER, P. R., L. M. B-OLDER, AND L. R. ALMODOVAR. 1967. Carbon assimilation of marine flagellate blooms in neritic waters of southern Puerto Rico. Bull. Mar. Sci. 17: l-15. CARPENTER, J. H., AND H. H. SELIGER. 1968. Studies at Oyster Bay in Jamaica, W. I., 2. T. Mar, Res. 286: 256-272. CINT~N, G. 1969. Seasonal fluctuations in a tropical bay. M.S. thesis, Univ. Puerto Rico, Mayaguez. CLARKE, G. L., AND L. R. BRESLAU. 1960. Studies of luminescent flashing in Phosphorescent Bay, Puerto Rico and in the Gulf of Naples

1957. Fitoplancton de las costas de Puerto Rico. Invest. Pesq. 6: 39-52. -. 1961. Hydrografia y fitoplancton de un area marina de la costa meridional de Puerto Rico. Invest. Pesq. 18: 33-96. NORDLI, E. 1957. Experimental studies on the ecology of Ceratia. Oikos 8: II, 200-265. PARSONS, T. R. 1966. In The determination of photosynthetic pigments in sea-water. A survey of methods. Monogr. Oceanogr. Method. 1, p. 21-31. SELIG~, II. H., J. H. CARPENTER, M. LOFTUS, AND W. D. MC~ELROY. 1970. Mechanisms for the accumulation of high concentrations of dinoflagellates in a bioluminescent bay. Limnol. Oceanogr. 15: 234-245.


1969. Towable photometer for rapid area mapping of concentrations of bioluminescent Limnol. Oceanogr. marine dinoflagellates.



- 1962. rine dinoflagellates. 1003-1017.

14: 80&813. W. R. TAYLOR, AND W. D. -3

Bioluminescence of ma1. J. Gen. Physiol. 45:

US. DEPARTMENT OF THE INTERIOR. 1968. The bioluminescent bays of Puerto Rico. 48 p. WALL, D., AND B. DALE. 1969. The hystrichosphaerid resting spore of the dinoflagellate, Pyrodinium bahamense, Plate 1966. J. Phycol. 5: 140-149.