Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude...

JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 100, NO. C4, PAGES 6527-6547, APRIL 15, 1995

Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude 59.5 ø N, longitude 21 ø W

Elijah Swift, James M. Sullivan, Harold P. Batchelder 1, Jeffrey Van Keuren, and Robert D. Vaillancourt

Graduate School of Oceanography, University of Rhode Island, Kingston.

Robert R. Bidigare Department of Oceanography, University of Hawaii, Honolulu.

Abstract. We investigated mixed-layer bioluminescence from early April to late September (in April 1989, May 1991, July 1983 and 1990, August 1991, September 1988 and 1989) at stations near the Marine-Light - Mixed Layers (MLML) bio-optical moorings site. Volume-specific bioluminescence potemial (BPOT, photons per unit volume) from epipelagic organisms was estimated directly with a pump-through bioluminescence photometer (BP) in 1983, 1988, and 1991. For all cruises, BPOT was also estimated by summing for a volume of seawater, the measurements of each species' total stimulable bioluminescence multiplied by each species'numerical abundance in the volme. The abundance data were taken from bottle casts, net tows, and BP effluent nets. After the onset of the spring bloom, from May through September, mixed layer BPOT was fairly constant, ~ 1-4 X 10 TM photons m 3. On one early April cruise (1989) before the spring bloom, BPOT was two orders of magnitude lower. Heterotrophic dinofiagellates in the genus Protoperidinium generally produced most (90% or more) of the •xed layer BPOT in the spring, summer, and fall. On one cruise in September (1988), the autotrophic dinofiagellate Ceratium fitsus produced the bulk of the mixed layer BPOT (more than about 4 X 10 TM photons m3). Other autotrophic dinoflagellates in the genus Gonyaulax and mesozooplankton produced a minor part of BPOT at most stations. The relative contribution of all autotrophic dinofiagellates to BPOT increased from a few percent during the May-June-July period to ~ 10% during the August-September period. In situ mechanically stimulable bioluminescence was reduced when underwater scalar irradiance (wavelengths 400-700 m) was greater than 0.1 pmol photons m -2 sq.

Introduction

To understand the seasonal and spatial patterns of oceanic bioluminescence, one must know what organisms are responsible. In this paper we describe several methods used to identify the organisms responsible for biohlminescence in the mixed layer, and where possible, in the seasonal thermocline beneath it. Along with identifying the causative organisms, we also estimated the amount of the bioluminescence they produced. We also investigated factors that might modulate their bioluminescence responses. These investigations occurred primarily in the Irminger Sea about 500 km south of Iceland. They were carried out during the April to September period.

Many of our measurements were taken near bio-optical moorings at latitude 59.5 ø N, longitude 21 ø W, (from now

•Now at U.S. Globec Office, Department of Integrative Biology, University of California at Berkeley.

Copyright 1995 by the American Geophysical Union.

Paper number 94JC01870. 0148-0227/95/94JC-01870505.00

on, the Marine Light-Mixed Layer or MLML station). This position is reported to be close to the boundary between two zoogeographic regions, the subarctic and transitional regions [Van der $poel and Heyman, 1983, Figures 1 and 6]. The instrumented moorings recorded optical and hydrographic data at the site during April-June 1989 and May-September 1991 [Stramska and Dickey, 1993; Dickey et al., 1994; Plueddemann et al., this issue]. The mooring data in 1991 included time series measurements of bioluminescence at 55

m for the May to mid-August period [Nedson et al., this issue]. These same authors also describe profile data from a submersible biohminescence photometer (from now on, BP) which they deployed in May 1991 and August 1991 near the MLML station. Ondercin et al. [this issue] also measured bioluminescence in this region in August 1991 using instruments including a BP on a vertically undulating towed parvane.

We obtained data in the region of the MLML mooring through shipboard sampling during cruises in April 1989, May 1991, July 1983, July 1990, August 1991, September 1988, and September 1989. In addition, we have augmented our observations on mixed layer bioluminescence with plankton abundance data published from two Naval Oceanographic Office (NAVOcEANO) cruises in September 1980 and April 1981 [Willet 1982; Willet et al., 1982]. In

6527

6528 SWIFT ET AL.: NORTH ATLANTIC BIOLUMINESCENCE

1983, we made measurements in Icelandic slope waters, again to identify key bioluminescent species and to learn the amount of BPOT, and these data are included here.

These subarctic waters have a biological production cycle that shows strong seasonal change [e.g., Corlett, 1953; Williams and Robinson; 1973]. More than thirty-five years of Hardy plankton recorder data for this region have been summarized by Colebrook and coauthors [e.g., Colebrook et al., 1982ab; Colebrook, 1986] with descriptions of seasonal, interannual, and regional distributions of some bioluminescent plankton and the nature of the variance in their distributions. For this region, Colebrook and Taylor [ 1986] reported changes in plankton abundances due to the seasonal cycle were "far larger than the year-to-year changes." Both seasonal changes and mesoscale spatial patchiness of phytoplankton in the region have been indicated by chlorophyll distributions viewed from the coastal zone color scanner on

the Nimbus 7 satellite and by National Aeronautics and Space Administration airborne oceanographic lidar (laser induced detection and ranging) overflights [Esaias et al., 1986; Yoder et al., 1993]. All these investigations suggest considerable mesoscale and seasonal variability.

The bioluminescence which will be described here was

mechanically stimulated and is an assay of the total amount of light that an organism could produce when mechanically stimulated to exhaustion (total mechanically stimulable light, TMSL) originally deftned as total stimulable light (TSL) by Seliger et al., [1969]. The sum of the TMSL from all the organisms in a volume of seawater was deftned as its (volume) specific bioluminescence potential (BPOT) by Rudyakov [1968]. We used BPOT because measuring mechanically stimulated bioluminescence helped to locate concentrations of bioluminescent organisms, and at times, to assess aspects of their physiological state [Swift et al. ,1981; Buskey et al., 1992; Sullivan and Swift, this issue]. Light is one of the factors affecting the physiological state of dinoflagellates. A number of investigators have reported that daylight reduces the effectiveness of mechanical stimulation of bioluminescence during daylight hours [e.g., Sweeney et al., 1959; Yentsch et al., 1964; Biggley et al., 1969; Filimonov and Sadovskaya, 1986; BatcheMer et al., 1992; Lapota et al., 1992a; Sullivan and Swift, 1994]. In the present paper, we have examined instances where light inhibited the in sire mechanically stimulable bioluminescence produced primarily by populations of dinoflagellates.

Materials and Methods

Two main methods were used to estimate BPOT. First, mechanimlly stimulated bioluminescence was measured in

the sea with a pump-through BP. BPOT was estimated from these BP measurements by assuming a "biological efficiency" of the BP, which varies with the taxonomic composition of the bioluminescent organisms stimulated by the BP [Buskey, 1991; Swift et al., 1984; Widder et al., 1993]. Organisms in the effluent of our BP were collected in 25-1•m mesh nets and later identified and counted in order to associate the

measured bioluminescent signals with bioluminescent organisms. Second, BPOT was estimated from concentrations of bioluminescent organisms (from net tows or the BP effluent) combined with measurements of their TMSL. The contribution of mesozooplankton to estimates of BPOT may

be low because of presumed avoidance by strongly swim- ming zooplankton of (1) slow net hauls [Clutter and Anraku, 1968] and (2) the intake to the BP, particularly when it is small and pumping rates are low [Swift et al., 1984].

Net Collections

We used 0.5-m diameter nets with General Oceanics flow-

meters mounted one-third of the way across the mouth of the nets for collections. Net tows at discrete depths with these nets were commonly made using a General Oceanics double tripping apparatus. For dinoflagellates, we used either 20- or 25-1•m mesh nets towed at speeds less than a 2 km]h (weather permitting). For zooplankton we usually used 100-1•m mesh nets towed at speeds of" 4 km•.. In August 1991, we also used a 1 m: multiple opening-closing net with environmental sensors (MOCNESS) fitted with 333-1•m mesh nets. Plankton samples were thoroughly rinsed from the nets and preserved in 5% buffered formalin in seawater for later enumeration.

Dinoflagellates were enumerated in Settling chambers using Zeiss inverted microscopes with phase-contrast illumination, at magnifications from 25X to 480X. Depending on the cruise, various fractions (including 100%) of the samples were counted in the samples, with any fraction taken being counted to completeness. For individual samples, from '• 30 to 1000 of the most common bioluminescent dinoflagellate species were counted. Their identification was based on several authorities [Dodge, 1982, 1985; Lebour, 1925; Schiller, 1931-1937; Taylor, 1976]. Zooplankton were sorted from the samples or subsamples after splitting the samples with a Folsom plankton splitter, and sorting the individual groups into vials for later identification by various authorities (for copepods, Rose, M. 1933, Wilson, E.B., 1932; Brodskii, K.A., 1950, Vidal, J., 1971; for euphausiids, Lomakina, N.B., 1978, Einarsson, H., 1945; for ostracods: Deevey, G.B., 1968, for larvaceans; Buckmann, A. 1969].

Prof'des of Mechanically Stimulated Bioluminescence Prior to 1991, we used a BP with a design modified from

that published by Seliger et al., [ 1962] and Clarke and Kelly [1965], as described by Swift et a1.,[1984]. The BP used from 1983 to 1988 had a flow rate of ~ 12-18 L/rain and the residence time of the detection chamber was '• 1.0 s. For the

1991 measurements, we wished to resolve individual dinoflagellate flashes and to measure their magnitudes. We decreased the flow rate to ~4 L/rain, and decreased the volume of the sampling chamber to 18 mL, for a detection chamber residence time of ~ 0.3 s. We used a blunt body to produce turbulence in the flow-through chamber to stimulate bioluminescence. For all cruises the efficiency of the BP optics ("optical calibration") was measured by mining off the pump and filling the detection chamber with a known number of light-adapted dinoflagellates. We then injected sufficient acid to drop the pH to <4.5; this low pH stimulated "complete"dinoflagellate bioluminescence. Parallel determinations of the acid- stimulated dinoflagellate bioluminescence were run in a radiometrically calibrated photometer (for calibration methods, see Seliger et al., [1969]). Dinoflagellates used were Pyrocystis spp. prior to 1991 and Ceratium fitsus and Protogonyaulax tamarensis for the 1991 field year. A biological calibration [for definition, see Widder et al., 1993 ] was run using the above autotrophic

SWIFT ET AL.: NORTH ATLANTIC BIOLUMINESCENCE 6529

dinoflagellates to ascertain what percentage of their TMSL the BP recorded in its normal pump-through mode. The BP recorded between 10% and 14% the BPOT of solutions

containing dark-adapted dinoflagellates. In order to report seawater BPOT from measured BP signals in this manuscript, unless otherwise noted, we multiplied the BP signal by an order of magnitude. Periodically, we split a single sample into two parts, operating half of the time with a low voltage on the BP photomultiplier robe (PMT) and the other half operating at a higher voltage. This allowed checks for signal variation (e.g., flash number and magnitude) due to PMT voltage selection. Many of the calibration procedures and their justifications are described previously [Swirl et al., 1984; BatcheMer and Swift, 1988, 1989].

After organisms were mechanically stimulated in the BP, they were pumped into a 20- or 25-1•m net. In 1983, the nets were attached directly to the effluem hose from the BP. The insmnnent was brought to the surface after each depth was sampled to retrieve the organisms out of the net. After 1985, the nets were arranged in an apparatus where a manifold could be rotated to direct the seawater into a

circular arrangemere of nets. With the rough weather at the site, we found with this arrangement in 1988 that we were "losing" organisms. Thus, for our i99i depioymems, we covered the nets with 4-inch-diameter polyvinylchloride (pvc) plastic pipe during deployments and installed a modified sampling manifold to prevem "leakage" of organisms.

Laboratory Photometer Measurements Dinoflagellates to be tested at sea were routinely collected

during the late afternoon when they were photoinhibited (not susceptible to mechanical stimulation of their bioluminescence) during the collection and isolation processes. Individual cells were isolated under a dissecting microscope and pipetted into filtered seawater. Cells were held in the dark for 4 hours or more in a temperature-controlled incubator, at the temperature of the seawater in which they were collected. Previous work had shown that cells reached

their maximum BPOT in 1.5 to 2 hours of darkness [Biggley et al., 1969]. Cells were then mechanically stimulated to exhaustion in a photometer. Values given in Table 1 are mean values in that we were collecting the dinoflagellates when they were photoinhibited and thus we did not exhaust their bioluminescence in the collection process.

Zooplankton were collected during the period starting 2 hours or more after sunset when the ship's acoustic Doppler currein profiler signal (150 mHz) indicated that they had begun vertical migration toward the surface [Batchelder et al., this issue]. Zooplankton were kept at ambient temperature and isolated in filtered seawater. They were allowed to recover from handling for 4 hours or more and then their TMSL was measured in a photometer. Latz et al. [1990] have suggested that a more complete recovery from the •' ..... • "'-•0• .... • isolation might have occurred ff the zooplankton had been held for 24 hours. Their experiments suggest that our shorter holding period and methods of data reduction might underestimate the in situ TMSL values by as much as 40%, at least for the copepods they tested. We used the "most probable value" of zooplankton bioluminescence because we also recognize that we are exhausting some of the zooplankton's bioluminescence in the collection process [Batchelder and Swirl, 1989]. Our photometer was

absolutely calibrated using dinofiagellates, following the procedures outlined by Lee and Seliger [ 19721 and Seliger et al. [1969] which produces an absolute value with an error of about + 20 percem. Procedures used for photometry have previously been described [BatcheMer and Swirl, 1989; Biggley et al., 1969].

Where measurements of dinoflagellate biohminescence were not known, we estimated bioluminescence capacity of the cells based on an allometric relationship from Seliger and Biggley [1982], who presented arguments as to why dinoflagellates would produce ~ 8 X 1012 photons cm -2 of cell surface area. Their allometric relationship was developed using mostly autotrophic dinoflagellates. Recently, Buskey et al. [ 1992] reported that heterotrophic dinoflagellates in the genus Protoperidinium collected from Texas coastal waters were capable of producing twofold to threefold more light than would be predicted from Seliger and Biggley's [1982] allometric relationship. We have also observed that Proto- peridinium spp. at the MLML site produced - 2-3 times more bioluminescence than predicted by the allometric relationship. Thus, to the extent we have had to rely on the allometric relationship to estimate TMSL (see Table 1), we may have underestimated the contribution by heterotrophic tm•mmgeumes.

The laboratory photometer and BP have blue sensitive photomultiplier detectors (color responses S-5 and S-20, respectively). The detectors are only accurate when used for measurements with the same spectral characteristics as that of dinoflagellate bioluminescence [Seliger et al., 1969]. The photometer would record more photons from organisms than they produced if they have "bluer" bioluminescence than dinoflagellates (e.g., euphausiids, caridean prawns -[Swirl et al., 1977; Biggley et al., 1981]). The reverse would be true for bioluminescence "greener" than that of dinoflagellates (e.g. larvaceans - [Biggley et al., 1981]. However, these spectral corrections (20-30%) are rather small in the context of the variation found between individuals tested from natural

samples (see Table 1), and they should not affect the conclusions presemed here about the relative importance of the different taxonomic groups of organisms in producing bioluminescence.

Nutrients and Piginents Prior to 1989, nutrient analyses were done with "and

chemistry" using the procedures outlined by Strickland and Parsons [1968]. During 1989-1991, nutrient analyses were performed with a Technicon TrAAcs-800 autoanalyzer system following the methods outlined by Spears et al. [1988]. Chlorophyll was done by the standard extraction- fluorometer method [Strickland and Parsons, 1968]. For 1989-1991, some phytoplankton pigment concentrations,, were determined by high-performance liquid chromatography (HPLC). Filters (47 mm, glass fiber type F) were extracted in 90% acetone (vol./vol.) for 24 hours at -20øC in the dark following the addition of a known amount of internal standard (canthaxanthin in acetone). After extraction, samples were centrifuged to remove the filter and cellular debris. The acetone-extractable pigments (chlorophylIs and carotenoids) were separated using a Spectra-Physics model SP8700 liquid chromatograph following the methods described by Bidigare et al. [1989]. The amount of dinoflagellate chlorophyll a biomass relative to total


Table 1. Total Mechanically Sfimulable Light (TMSL) Values in Photons per Individual for Species Found in the MLML Region •

Mean Standard Number Refer- TMSL b Deviation Tested ence

Dinoflagellates Autotrophic Ceratium fitsus 3.0 X l0 s _+1.7 X l0 s 422 8 Gonyaulax 1.0 X l0 s 4 G. digitale 2.1 X 107 _+1.1 X 107 3 G. grindleyi 1.0 X 108 4 G. parva 9.7 X 107 4 G. polygramma 1.6 X l0 s 2 G. spinifera 3.0 X l0 s _+1.7 X 107 3 G. spp. 1.0 X l0 s 4

Heterotrophic Protoperi-

dinium spp. 5.0 X 10 s 4 P. brevipes/breve. 2.0 X l0 s 4 P. ceraseus 4.8 X l0 s _+3.0 X l0 s 3 P. concoides 2.0 X 109 4 P. conicum 3.4 X 109 -+0.8 X 109 3

P. crassipes 8.7 X 109 -+1.7 X 109 3 P. depressurn 5.0 X 109 _+1.7 X 109 3 3 P. globulum 4.5 X 109 _+1.7 X 109 2 1 P. granii 8.1 X l0 s _+2.0 X l0 s 3 P. leonis 3.3 X 109 _+ 1.1 X 109 3 P. minutum 2.0 X 109 4 P. ovaturn 1.0 X 109 -+0.3 X 109 3

P. pallidurn 1.4 X 109 _+2.8 X l0 s 3 1 P. pellucidurn 2.0 X l0 s _+0.6 X l0 s 3 P. pentagonurn 5.0 X 109 _+0.9 X 109 3 P. pyriforme 1.0 X l0 s 4 P. saltans 2.0 X l0 s 4 P. sinaicum 2.0 X 10 s 4 P. sournia 2.0 X l0 s 4 P. steinii 1.4 X l0 s _+0.3 X l0 s 3 P. subinerme 1.5 X 109 _+0.3 X 109 3 P. tuburn 2.0 X 109 4

P. spp. 2.0 X 109 1

Table 1. (oontinued)

Mean Standard Number Refer- TMSL • Deviation Tested ence

Zooplankton Copepods Heterorhabdus

norvegicus 1.6 X 10 • 14 5 H. spinifrons 1.6 X 10 • 2 5 Metridia longa 1.5 X 10 • 18 5 M. lucens 8.5 X 10 •ø 70 5

2nd copepodite 9.0 X 109 6 5 3rd copepodite 2.0 X 10 •ø 4 5 4th copepodite 2.2 X 10 •ø 26 5 5th copepodite o • 6.8 X 10 •ø 22 5 5th copepodite • 7.9 X 10 •ø 48 5 Adult • 3.5 X 10 •ø 22 5 Adult • 1.1 X 10 • 48 5

Pleuromamma

robusta 7.1 X 10 •ø 24 1

Euphausiids Thysanoessa longicauda 1.1 X 10 • 32 1

Ostracods

Conchaecia spp. 6.3 X 10 •ø 154 5 Annelids

Tomopteris spp. 9.8 X 10 •ø• 52 2 Larvaceans

Oikopleura labradoriensis 5.0 X 10 • 6

a References are 1, Swift et al., (laboratory photomerry, published here); 2, Buskey and Swift [1990]; 3, Esaias [1972]; 4, estimation from cell size, Seliger and Biggley [1982]; 5, BatcheMer and Swift [1989]; 6, Galt and Grober [1985]; 7, Batchelder et al. [1992], 8, Sullivan and Swift [1994]. b MPV described by Batchelder and Swift [1990]. Number of

organisms used to calculate MPV is the highest half of the assayed organisms. MPV values are reported in references 1, 5, 7, and 8. Conchoeica species values were pooled

for this Table.

ORange reported was 2 to 15.4 X 10 •ø photons per organism.

phytoplankton chlorophyll a biomass was calculated following Letelier et al. [1993].

Other Water Column Measurements

All times in this manuscript are in UT. In 1983, total photosynthetically available radiation (PAR) was measured on deck with a scaler irradiance detector (LICOR 186). Underwater attenuation of PAR was estimated by lowering a matching sensor to depth and normalizing the underwater values with the concomitant deck values. On subsequent cruises, on-deck PAR was measured with a Biospherical Instruments scaler irradiance sensor to normalize both a

scaler irradiance sensor at depth and (after 1987) a downwelling spectral irradiance sensor (Biospherical Insmtmems, model MER1010).

To calculate the underwater irradiances associated with

photoinhibition during the day and dawn profiles in 1988,

and for the dawn and dusk time series in August 1991, we used a variety of techniques. For on-deck light measurements at night, dawn, and dusk, we used the "low light" sensor described by BatcheMer et al. [1992] and Van Keuren [1994]. Spectral attenuation in the water was measured during the day with the MER 1010 profiler. During the dawn profile in 1988, the low light sensor was recording light intensities when the bioluminescence sample at 30 m was collected, but the instrument saturated before the bioluminescence sample at 10 m was collected. About 7 minutes after the 10 m sample was collected the MER1010 was on deck and light intensities were high enough for it to record spectral downwelling inadiance. To extrapolate the downwelling speclxal irradiance back to the time of the 10 m sample, we modified a software program which calculated how daylight intensities should change with time based on the geometry of the Earth-Sun system. To calculate irradi-


ance at depth from the on-deck measurements taken at dusk, underwater spectral attenuation was assumed to be the same as on the previous day when it was measured with the MERlOlO. This assumption may be justified because chlorophyll fluorescence measured by our profiler was very similar in the mixed layer during night, dusk, and day casts, and corresponded to an extracted chlorophyll value of ~ 2,800 ng L 4. A similar set of extrapolations was used to calculate underwater irradiance in August, 1991.

Naval Oceanographic Office Plankton Data Details of the collection methods and lists of enumerated

plankton are contained in the data reports from the April 1981 and the September, 1980 NAVOCEANO cruises [Willerr, 1982; Willett et al., 1982]. To summarize, the authors collected zooplankton about once a day using paired 1-m -diameter bongo nets with 303- and 555-1•m mesh netting, the oblique tows were made to 200 m. These authors collected dinofiagellates, while under way, from a depth of 3 m (once an hour) by pumping 6- to 15-L samples through a 20-1•m aperture mesh net. To remove some of the variability due to counting error and spatial variability, we combined their concentrations of bioluminescent organisms from the region closest to the MLML site, using their data from April 14-17, 1981 and their data from September 21- 26, 1980. While mesozooplankton concentrations derived from theft bongo net-collected samples were not available in the September 1980 cruise data report [Willett, 1982,] the data were made available to the authors for these estimations of BPOT.

Results

In the following sections we will describe results from cruises to the MLML site from 1980 to 1991. Taken

together, the results should indicate that heterotrophic dinoflagellates in the genus Protoperidinium had the potential for producing the most mechanically stimulated bioluminescence. Autotrophic dinoflagellates, primarily Ceratium fusus, had a secondary role as potential sources of bioluminescence. Mesozooplankton were also a secondary source of bioluminescence. The BPOT was mostly found in the surface isothermal wind mixed layer in conjunction with the highest chlorophyll concentrations. The results in this section also indicate that scalar irradiance intensities above

~0.1 ½mol photons m -2 may photoinhibit the mechanical stimulability of bioluminescence in these waters.

September 1980 and April 1981 We used photometric measurements (Table 1) to estimate

the amount of bioluminescence that would be produced by organisms collected and enumerated from NAVOCEANO cruises in the region of the MLML station in April 1981 and September 1980 (Tables 2 and 3). There were 25 dinoflagellate samples for April and 46 for September. The mean values in Tables 2 and 3 do not report the variability in BPOT based on single samples. For both April and September the standard deviation of BPOT based on individual samples was larger than the mean value of BPOT indicating the spatially variable nature of the populations. For April and September, the range of individually estimated BPOT was from "0" to 5 times the mean value. The

standard error of the mean value for BPOT in April was

Table 2. Mean Concentrations of Bioluminescent

Dinoflagellates and Mesozooplankton and Their Estimated Contributions to the Bioluminescence

Potential (photons m '3) on April 14-17, 1981, Near the MLML Station.

Number, m -3 BPOT

D ino fia g e llat es * Autotrophs Ceratium fitsus 9,200 2.8 X 10 •2 Gonyaulax parva 514 5.1 X 10 •ø

G. spinifera 657 2.0 X 10 •ø G. spp. 57,485 5.7 X 10 •2

Total 8.6 X 1022

Heterotrophs Protoperidinium

brevipe/breve 6,514 1.0 X 1023 P. crassipes 4,086 3.6 X 10 •3 P. globulunl/gbbulus 42,971 1.9 X 10 TM P. granii 95,057 7.7 X 10 •3 P. leonis 200 6.6 X 10 •

P. minisculum 102,700 6.5 X 1023 P. spp. 17,000 3.4 X 1023

Total 4.1 X 10 TM

Mesozooplankton'• Metridia longa 4.4 3.8 X 10 • Pleuromamma robusta 1.3 9.2 X 10 •2

Thysanoessa longicauda 0.76 8.4 X 10 • Larvaceans 0.35 0

Radiolarians 1.1 0

Total 2.1 X 10 •2

* Three-meter depth, 15-1 sample, 201•m aperture mesh net. '• Bongo net tows from 0-200 m, 303 and 505 micron mesh

aperture nets.

+_30% of the mean value, in September _+17%. Counting error (Poisson statistics) should have contributed about +_1% to the variability of the mean.

For April 1981 the mean value of BPOT estimated from dinoflagellate samples was 3.8 x 10 TM photons m -3 (Tables 1 and 2). Protoperidinium spp. made up 97% of the total dinoflagellate TMSL in April, with autotrophic dinoflagellates producing the remainder. Zooplankton samples from 0 to 200 m were estimated to have had a mean TMSL of 2.6

X I0 n photons m 3. Of the mesozooplankton present, the copepods Pleuromamma spp. and Metridia spp., and the euphausiid Thysanoessa spp., were about co-equal in producing bioluminescence.

To estimate the relative importance of dinoflagellates and zooplankton in April, we made assumptions about the vertical distributions of the dinoflagellates and zooplankton. If, for example, we assumed both populations were in a 200 m mixed layer, as indicated by one conductivity-temperature- depth (CTD) cast to 70 m and one to 200 m in the region, then the bioluminescent zooplankton would have contributed less than 1% to the BPOT, and dinoflagellates the remainder. On an areal basis, the MLML region had a BPOT of about 5.2 X 10 •6 photons m -2, equivalent to that of the



Dinoflagellates and Mesozooplankton and Their Estimated Contribution to the Bioluminescence

Potential in September 1980 at the MLML Site.

Number, m '3 BPOT, Photons m '3

Dino fla gella te s * Autotrophs

Ceratium fusus 23,200 7.0 X 10 •2 Gonyaulax spinifera 1,420 4.3 X 10 •ø G. parva 4,110 4.0 X 10 • G. spp. 3,090 3.1 X 10 •

Total 7.7 X 1012

Hetertrophs Protoperidinium

brevipes/breve 6,440 1.3 X 1013 P. crassipes 4,420 3.9 X 1013 P. globulum/globulus 42,000 1.9 X 10 TM P. granii 26,600 2.2 X 1013 P. leonis 39,000 1.3 X 10 TM P. minisculum 75,200 1.5 X 10 TM P. pellucidum 4,700 8.4 X 1011 P. steinii 14,000 5.2 X 1013 P. spp. (unidentified) 9,800 3.4 X 1013

Total 5.6 X 10 TM

Mesozooplankton• Copepods

Metridia lucens 0.65 9.8 X 101ø Pleuromamma robusta 0.18 1.3 X 101ø

Heterorhabdus norvegicus 0.31 5.0 X 101ø Heterorhabdus spinifrons 0.008 1.3 X 109

Euphausiacea 0.18 3.2 X 1012 Total 3.4 X 1012

* Three-meter depth, 15-1 sample, 20gm aperture mesh nets. •' Bongo net tows from 0-200 m, 303 and 505 micron mesh

aperture nets.

Sargasso Sea [Batchelder et al., 1990; Swift et al., 1984, 1985]. This is probably an overestimate of the areal BPOT as deep mixed waters would be associated with low biomass of bioluminescem dinofiagellates [½orlett, 1953; Colebrook, 1986], with the high concentrations being associated with shallower mixed layers.

The mean values reported in Table 2 for April 1981 were some of the highest and found on any cruise to the area. The values for individual plankton samples closest to the MLML station were very low, similar to those we report for early April 1989. Further away, there was a "patch" of very high estimated dinofiagellate bioluminescence. The "patch" was associated with a high number of diatoms and other phytoplankton, suggesting the water there was undergoing a "spring bloom." Heterotrophic dinofiagellates, which produced most of the estimated BPOT, apparently had increased in numbers in response to the available phytoplankton food there.

Estimates of total bioluminescence in September 1980 (Table 3) are similar to April 1981 in that dinofiagellates were estimated to produce the bulk of the BPOT, about 5.5

X 10 TM photons m -3 (5.6 X 10 TM photons m -3 with the addition of unscreened Protoperidinium spp). Assuming a 50-m mixed layer, the areal BPOT would be again be similar to that for the Sargasso Sea [BatcheMer et al., 1990]. Assuming a homogeneous distribution from 0 to 200 m, bioluminescence from mesozooplankton was estimated as about 3.4 X 1012 photons m -3'. If mesozooplankton were concentrated in the upper 50 m at night, they might have contributed as much as about 2-3% to near-surface BPOT

then. Of the mesozooplankton, euphausiids were estimated to produce about 90% of the bioluminescence.

July 1983 There were two stations from cruise 103 of RV Endeavor

in the MLML region where bioluminescence was investigated. They were station 4 at latitude 63 ø 59 • N, Long. 12 ø 58 • W, just south of the subpolar front in slope waters east of Iceland and Sta. 6, Lat. 61 ø 56 • N, Long. 27 ø 45 • W, to the southwest of Iceland. For both stations, calculations suggest that dinofiagellates were responsible for >90% of the BPOT at all (but one) depths sampled. Heterotrophic dinoflagellates in the genus Protoperidinium produced more than 90% of the estimated dinoflagellate BPOT, with the exception of two depths at Sta.. 6 (20 m and 60 m). The autotrophic dinoflagellates C. fusus and Gonyaulax spp. made up the remainder of the BPOT. Mesozooplankton provided a minor contribution and were only important at a few depths (less than 10% of total BPOT). There was good agreement between the estimated BPOT and the BPOT measured with

the BP if the "biological efficiency" of the BP was assumed to be about 1/3. High efficiency probably resulted from the large size of Protoperidinium's first flash (J. M. Sullivan, personal communication, 1991). The discrepancies found between the estimated bioluminescence and that measured

with the BP during this cruise would be explained by photoinhibition of mechanically stimulable bioluminescence, and it appears from the proides that the "saturation intensity" for photoinhibition was about 0.1 i•mol photons m -2 s -1 as scalar irradiance (light in the wave lengths from 400 to 700 nm).

Organisms At sta. 4, we sampled on the nights of July 20-21 and 21-

22, and during the day on July 23. On the night of July 21- 22 July, we sampled about 40 L each at 20-, 40-, 60-, 80-, 100-, 120-, and 140-m depth with the BP. The BP's bioluminescence signal came primarily from dinofiagellates. Although about 275 L were pumped during the profile, we did not find bioluminescent copepods in the genus Metridia or Pleuromamma in the samples. We did f'md just over 200 copepods (mostly Oithona and Macrosetella, with some Calanus). Two bioluminescent annelids (Tomopteris spp.) were found in one net sample. The relative composition of the bioluminescem dinofiagellates did not change systemati- cally with depth from 20 to 140 m. Protoperidinium spp. were 62% (range 51 to 71%), Gonyaulax spp. were about 28% (range 21 to 35%), and ½. fusus was 9% (range 3 to 15%) of the total by number. As an example, Table 44 lists species considered bioluminescent for this station at 20 m, where the cell counts were highest and the counting statistics robust.

In contrast to sta. 4, sta. 6 had much higher numbers of bioluminescent mesozooplankton, which were estimated to produce more bioluminescence at 1.5 m than the dinofiagel-


Table 4a. Bioluminescent Dinoflagellate Species Present at Sta. 4 (lat. 63.59 ø. N, long. 12.58 ø W) on July 21, 1983, at 20 m Depth.õ

Genus and Dinoflagellates, m -3 Species

Autotrophs Ceratium fusus 9,147 Gonyau lax digitale 502 G. grindleyi 13,869 G. spinifera 6,129 G. tricantha 134

G. sp. (unidentified) 20,941 Heterotrophs

Protoperidinium bipes 100 P. brevipes 6,573 P. ceraseus 2,782 P. depressurn 201 P. globulus 435 P. granii 34 P. ovaturn 25,999 P. pallidurn 133 P. pellucidurn 6,778 P. pyriforme 4,721 P. saltans 168

P. steinii 67

P. tuburn 3,692 P. spp. (unidentified) 6,491

{}Abundances are in cells per cubic meter. One cell enumerated was tabulated here as ~34 cells per cubic meter.

lates. Also, in contrast, autotrophic dinoflagellates were more important than heterotrophic ones in terms of estimated BPOT (C. fusus about 61%, Gonyaulax spp. about 14%, and Protoperidinium spp. about 24% of estimated dinoflagellate BPOT). At greater depths (20 to 160 m), protoperidinia dominated the dinoflagellate-derived and the total estimated bioluminescence signal. For the 20- to 160 m dinoflagellate BPOT, protoperidinia produced 91% (range 80-96%), C. fusus 6% (range 3-18%), and Gonyaulax spp. 2% (range 1- 4%).

At both stations the BP chart recordings of bioluminescence intensity indicated that the sources were extremely numerous and dim. The flashes mn together, so that the concentrations of organisms (if greater than about 4-6 per liter with this BP configuration) could not be determined. However, at sta. 4 at the 80-, 100-, and 140-m depths, it was possible to examine individual flashes to determine the distribution of signal sizes. There was reasonable agreement between the number of bioluminescent dinoflagellates and the number of small flash evems. In the 80-m sample there were 376 small flashes and 219 bioluminescent dinoflagellates, in the 100-m sample there were 548 small flashes and 584 bioluminescent dinoflagellates, and in the 140-m sample there were 136 small flashes and 95 bioluminescent

dinoflagellates.

BPOT and Hydrography Figure 1 depicts the hydrographic information and the

bioluminescence profile for this station. The estimated

2o

•, 4o • 60

a. 100

• 120

140

1606 2'0 IO0

0

20

40 60 8o-

•oo

120 140

.

160

180; BPOT (1012photons m '3)

Figure 1. Sta. 4, July 1983, south of the subpolar front. The upper panel shows the vertical profries of temperature (T, or dotted line with solid dots) multiplied by 10 in degrees Celsius, the vertical profile of extracted chlorophyll (Chl, dashed line with solid triangles) in ng L -1, and bioluminescence potemial (BPOT, or solid line with solid squares) in 1012 photons m -3 for the night profile. The lower panel shows two daytime (dotted and dashed lines with solid squares) and one nighttime (solid line with solid square) vertical profiles of measured stimulable bioluminescence at sta. 4.

BPOT for sta. 4 during the night is shown in Table 4b. As in most BPOT profiles, there was a close association between BP-bioluminescence, the warmest water, and chlorophyll concentrations (if correlated, r 2 = 0.94-0.95).

Table 4b. Biolnminescence Budget for Sta. 4.ô

Depth, m

Estimated BPOT, Measured Bioluminescence, photoIlS m -3 photons m -3

20 7.7 X 1013 3.0 X 1013 40 3.2 X 1013 2.4 X 1013 60 3.1 X 1013 2.0 X 1013 80 0.7 X 1013 1.6 X 1013

100 1.4 X 1013 0.5 X 1013 120 0.8 X 1013 0.4 X 1013 140 0.3 X 1013 0.3 X 1013

ô A least squares linear regression between the BPOT estimated from plankton net collections and that estimated from BP measurements has a sample coefficient of determination, r 2 = 0.71. The equation of the line was Y (photons m -3 X 1013) = 0.35 * (x) + 0.59, where BPOT estimated from the BP is the dependent variable.


There was ah:o a strong correlation of all three parameters with the BPOT we estimated from cell counts and our

photometric measurements (? = 0.7 - 0.8). Protoperidinia ingest phytoplankton and bacteria [Gaines and Taylor, 1984; Lessard and Swift, 1985; Jacobson and Anderson, 1986; Buskey et al., 1992]. If chlorophyll was a good surrogate for the concentration of this "food" of Protoperidinium spp., then food decreased by about 15-fold from the surface to 120 m, from 75 ng L 4 to 4.5 ng L 4' cMor a (Figure 1), but interestingly, the TMSL per dinoflagellate measured by the BP did not decrease over this depth range. This might indicate that the water column had only mixed vertically quite recently.

0

100

150

Possible Photoinhibition

Two daytime profiles of mechanically stimulable bioluminescence were taken at sta. 4 and may be compared to the nighttime profde (Figure 1, lower panel). The day profiles appeared to diverge from the night profile above 60 m in the first profile and above 80 m in the second profile, with lower bioluminescence at the surface during the day. If we assigned the dinoflagellates a "saturation intensity" value of photoinhibition of 0.1 I•mol photons m -2 s 4 (ambient PAR, as scalar irradiance), this would explain features of these profiles (and others described below). The calculated light intensity at 20 m during the night was ~0.04 I•mol photons m -2 s 4, below the saturation intensity, so at night we might expect better agreement of the estimated and measured values. For the first daytime profile, we calculated a PAR of ~32 I•mol photons m -2 s -• at 20 m, and ~0.2 I•mol photons m 2 s4at 70 m. At both depths there appears to be less bioluminescence than at night. At 80 m, where the daytime bioluminescence value was similar to the nighttime value, we calculated ambient light of ~0.06 I•mol photons m- 2 s-• or less. In the second daytime profide, the scalar irradiance at 20 m was lower, ~ 9 I•mol photons m -2 s -•, whereas at 60 m and below, where light was ~0.1 I•mol photons m -2 s -• or less, the profile was similar to the nighttime profile. Ship drift combined with horizontal organism patchiness would confound these comparisons of night time and daytime profides. However, we did follow a surface drogue during the measurements to attempt to stay in the same water "patch".

In support of using 0.1 I•mol photons m -2 s 4 as a saturation intensity, we found that Protoperidinium pallidurn collected from the MLML site had its mechanically stimulable bioluminescence totally photoinhibited by PAR of 0.14 I•mol photons m -2 s 4 using cool white fluorescent lamps. We were unable to photoinhibit P. globosum bioluminescence, and this lack of photoinhibition and possibly that in other Protoperidinium spp. may explain some of the continued stimulable biohminescence observed

during the day at the MLML site and elsewhere. At sta. 6, it is difficult to ascertain any photoinhibition

effect in the 1.5-m depth sample because the bioluminescence was very low, and thus the values reported are not robust. Also, there was a potentially high contribution by zooplankton (many of which are not photoinhibited, [Neidhardt, 1989]). Below the surface, our measurements suggest that the reason the estimated and the measured BPOT show the discrepancy at 20 m (Figure 2) was that ambient scalar irradiance (PAR) at that depth was ~0.1-0.2 I•mol photons m -2 s 4, e.g., potentially photoinhibitory. From

200 I I I I 0 20 40 60 80 100

BPOT (1012photons m -3 )

Figure 2. Sta. 6, July 1983, The vertical profile of mechanically stimulated biohminescence (solid line) and BPOT estimated from enumeration of the dinoflagellates captured in the nets (dashed line).

40 m to depth, light intensities were well below the saturation intensity for photoinhibition of mechanically stimulated biohminescence, and the shape of the measured and estimated biohminescence profiles agreed.

September 1988

Data were collected at USNS Bartlett station Sierra, (lat. 59 ø 29-38 • N, long. 21 ø 14.5-35•W). One night profile, one dawn profile, and one daytime profile were taken on September 11, 13, and 12, respectively. The high values of the BP-measured BPOT were associated with surface mixed layer. The chlorophyll maximum was also found in the mixed layer (Figure 3). Net collections made in conjunction with the BP profile were enumerated for September 12 and 13 with profiles to 200 m. These data indicated that 87% of the dinofiagellate bioluminescence was from C. fusus. A minor fraction of the signal was from Gonyaulax and Protoperidinium spp. As Figure 3 illustrates, there was little or no BP stimulated bioluminescence below the mixed layer, although C. fusus was present. We suggest that the C. fusus cells below the mixed layer must have had greatly reduced bioluminescence capacity relative to those in the mixed layer, as would be predicted from the dim light intensities there [Sullivan and Swirl, this issue, Sullivan and Swirl, 1994].

Like the previously described profries, "signal analysis" of the data from the BP showed that most of the biohminescence signal at night in the mixed layer was due to numerous "small" flashes (Figure 3). During the daytime profile, the small flashes were not observed, but some of the large flashes persisted. During the dawn profile, the last (and shallowest) depth (10 m) exhibited reduced mechanically stimulable bioluminescence relative to that of the sample taken in the mixed layer below it (30 m). As in 1983, an explanation of the difference between the deep and shallow mixed layer samples at dawn, day, and night, is that mechanically stimulable dinoflagellate biohminescence was being photoinhibited by ambient light.

SWIFt ET AL.: NORTH ATLANTIC BIOLUMINESCENCE 6535

TEMPERATURE (C.) CHLOR a (mg m '•) 9 10 11 12 0 1 2 3 4

•.•0 ............... 0

50 ,50

200 • 200

50

150

200

BPOT (10•=Photons m '=) 10 20 30 40 50 60 70 80

Figure 3. Sta. Siena, September 1988. The upper panel indicates the vertical distributions of temperature and extracted chlorophyll a. The lower panel showed BPOT measured with the bathyphotometer during one day, one night, and one dawn profile. The daytime signals were separated into signals from small flashes (dotted line) and

,

total signal (solid line). The dawn signals were separated similarly into signals from small flashes (dotted line with solid dots) and total signal (solid line with solid dots), and nighttime signal into small flashes (dotted line with solid squares) and total flashes (solid line with solid squares).

We made specwal scalar irradiance calculations to test ff the observed reduction in biohminescence would be explained by the spectral photoinhibition model of Sullivan and Swift [1994]. The model was developed from laboratory studies of C. fusus. In the laboratory, the peak photoinhibition wavelength was at 490 nm, with little activity from light in the green and red parts of the spectrum. MLML waters had a transmission peak in the green part of the spectrum, according to our measurements of spectral downwelling irradiance. The shift away from the blue part of the spectrmn was presumably associated with fairly high phytoplankton concentrations (~3 mg m 3 extractable chlor a) in the waters. The mismatch of the colors for peak transmission and peak photoinhibition means that photoinhibition occurs deeper in the water column than might be predicted from the attenuation of total scalar irradiance or PAR with depth. For the dawn profile, we calculated (Table 5) that there should have been ~26% photoinhibition in the 10 m sample (with no photoinhibition in the 30-m sample). If the 30-m sample is assumed to represent 100% of the stimulable Ceratium bioluminescence, then we observed a -30% reduction in TMSL at 10, a fair agreement between the model and the observations.. Similarly, we examined the laboratory study to seek an explanation of the profde of

Table 5. Photoinhibition of Mechanically Stimulable Biolnminescence for C. fitsus by Spectral Domwelling Irradiance at 45 m Depth (Daylight) and 10 m Depth (Dawn) at the MLML Station in September, 1988.

Wavelength (nm) Moles Photons at center of m -2 s 4 waveband

Predicted

per cent inhibition

Daylight Calculation for 45 m, Bottom of the Mixed layer 410 2.1 X10* 0 441 1.1 X10 -8 14 488 7.6 X10 's 61 507 9.1 X10 's 25 532-694 25.1 X10 's 0 Total

400-700 nm 43.1 X10 -8 100

Dawn Calculation for I0 m 410 3.4 X109 0 441 7.4 X109 5 488 1.0 X10 -8 21 507 7.3 X109 0 532-694 1.6 X108 0 Total

400-700 nm 4.4 X10 -8 26

*From the action spectrum for photoinhibition developed by Sullivan and Swift [1994].

bioluminescence found during the day. The measured downwelling irradiance (as PAR) was ~ 0.8 I•mol photons m -2 s-' at 45 m (Table 5). With the spectral corrections, the laboratory study predicted that there would be ~100% photoinhibition at 45 m where we sampled with the BP. These Ceratium fusus-dominated waters were apparently about an order of magnitude less sensitive to photoinhibition than the Protoperidinium-dominated waters we sampled in 1983 (Figure 1), and also than the Protoperidinium- dominated waters we will describe for August, 1991.

First M•M• Mooring Cruises: April 1989, September 1989, and July 1990

During the cruise to launch the first MLML bio-optical mooring (April 1989) and the two mooring retrieval cruises (September 1989 and July 1990), we were able to obtain whole water samples for phytoplankton populations present, along with pigment and nutrient concentrations. Net tows for mesozooplankton were not possible.

The April 12 data from an RV Atlantis H cruise represented winter conditions at the MLML site (Table 6), according to the 1989 mooring data, summarized by Dickey et al., [1994]. Their results indicate that our data were taken before the onset of stratification and the spring bloom at the MLML site. Dinoflagellate numbers from a hydrographic cast were low, resulting in large counting errors. It appeared that both C. fitsus and protoperidinia were present, and that they might contribute about equally to the BPOT signal, which was about 2 orders of magnitude smaller than the "stratified season" values we have estimated for the area.

Mixed layer depth was greater than our deepest hydrocast bottle (70 m).


Table 6. Mean Concernrations of Bioluminescent

Dinofiagellates and Their Estimated Contributions to the Bioluminescence Potential on April 12, 1989, Near the MLML Stations

Dinofiagellates Number, m -3 BPOT, Photons (Whole Water Samples) m -3

50 m 70 m

Table 7. Mean Concentrations of Biol-minescent

Dinoflagellates and Mesozooplankton and Their Estimated Contributions to the Bioh•minescence

Po•ntial on September 25 and 27, 1989 Near the MLML Station.¾

Genus Number, m -3 BPOT, and Species Photons m '3

Autotrophs Ceratium fusus 5,260 1,200

Total

Heterotrophs Protoperidinium. bipes 0 1,200 P. spp. (unidentified) 0 1,200

Total

9.7 X 1011 9.7 X 10 •

3.0 X 10 • 1.2 X 1012 1.5 X i 0•2

, , ,

:[ Mixed layer depth was >150 m. Surface temperature was ~ 8.1 ø C. Cell numbera were low, and each cell enumerated is represented by '• 1.2 X 103 cells m 3 in this tabulation.

In conjunction with the September 1989 cruise on the RV Endeavor, we collected similar samples. Table 7 summarizes the dinoflagellate counts. The contribution to estimated BPOT was as follows: C. fusus ~20%, Gonyaulax spp. ~20- 30%, Protoperidinium spp. ~60 to 70%, and the zooplankton (captured in the bottles) contributing ~2%. Most of the estimated bioluminescence was associated with the nearly 100-m-deep mixed layer. Bioluminescem organisms were not found at 120 m or deeper on September 27 and there were almost none at 145 m and none deeper on 25 September. BPOT estimated for the mixed layer was about ~3 X 10 TM photoIls m -3, which for the 100-m mixed layer gave an areal value of ~3 X 10 •6 photons m 2.

On a cruise on the RV Ewing in July 1990, we again made a hydrographic cast. The estimates of dinoflagellate BPOT are shown in Table 8. The estimated mixed layer BPOT was 3.4 X 10 TM photons m -3. There was an order of magnitude more bioluminescence estimated from the heterotrophic Protoperidinium spp. than autotrophic species. Ceratium fusus dominated the signal from the autotrophs. The mixed layer depth at the station was ~42 m, producing an areal BPOT estimate of ~ 1.4 X 10 •6 photons m -2.

Pigment data support the conclusion from the plankton enumerations that autotrophic dinoflagellate abundance increases from the spring to the end of summer. HPLC analyses were performed on samples collected on April 12, 1989. Only trace amounts of the autotrophic dinoflagellate marker pigment, peridinin, were detected in the upper 70 m. This April station probably represented pre-bloom conditions. Nutrient Concentrations, given as mean and standard error of the mean, were high and constant in the upper 70 m of the water column ([nitrate] = 14.02 ñ 0.1 gM, [silicate] = 6.38 ñ 0.38 gM, and [phosphate] = 0.89 ñ 0.02 gM and extractable chlorophyll a concentration was only ~ 300 ng L- •. In contrast, apparently representing postbloom conditions, in the mixed layer on July 17, 1990, autotrophic dinoflagellates accounted for 4ñ2% of the total chlorophyll a biomass, which was ~1000 ng L -•. Also, mixed layer nutrients were low compared to the April 1989 values.. They were also low relative to water below the mixed layer at 90 and 170 m

Sept. 25 Sept 27 5 and 50 m 5,50 and 100 m

Dinoflagellates$ Autotrophs

Ceratium fusus 69,000 60,000 2.0 X 10 •3 Gonyaulax polygramma 70,000 20,000 7.2 X 10 •2 G. scrippsae 30,000 16,000 2.3 X 10 •2

Total 3.0 X 109

Heterotrophs Protoperidinium

brevipes/breve 5,300 18,000 2.3 X 109 P. cerasus 3,000 0 3.6 X 10 a3 P. crassipes 0 Z000 8.7 X 10 •2 P. minutum 11,300 0 1.9 X 10 x4 P. pellucidum 700 2,000 2.7 X 10 • P. steinii 3,300 0 2.3 X 10 xx P. tuba 2,000 6,000 8.0 X 101• P. spp. 3,300 2,000 5.3 X 101•

Total 2.7 X 1014

Mesozoop !a nktuo n ? Thysanoessa

longicauda 1 1.1 X 10 xx Larvaceans 2 1.0 X 101•

Total 1.1 X 101•

¾ Mixed layer depth was 100 m. Surface temperature was decreasing from 9.4øC on September 25 to 8.4øC on September 27 due to strong sustained winds (mostly > 65 km h'l), mixed layer chlorophyll a was - 0.85/tg L '•.

$ whole water samples. • Bongo net tows from 0-200 m, 303 and 505 micron

mesh aperture nets.

(mixed layer concentrations were [nitrate] -- 5.96 ñ 0.35 pM, [silicate] -- 1.23 ñ 0.31 !•M, [phosphate] '-0.56 ñ 0.08. Below the mixed layer values resembled those from April, [nitrate] = 16.62 ñ 0.02 !•M, [silicate] = 6.48 ñ 0.02 !•M, [phosphate] = 1.21 ñ 0.05 I•M). Pigment analyses from September 27, 1989, suggested a 10ñ4% contribution by dinoflagellates to total chlorophyll a biomass, which was ~500-800 ng L -• in the mixed layer. Mixed layer nutrient concentrations measured on September 27, 1989 ([nitrate] = 8.59 ñ 0.02 !•M, [silicate] = 2.09 ñ 0.02 !•M, and [phosphate] = 0.52 ñ 0.04 !•M), and were also depleted relative to those measured during April 1989.

May 1991: Mesoscale Mapping Cruise We sampled dinoflagellates and mesozooplankton in the

mixed layer (depth ~25 m) from May 7 through May 10, and dinoflagellates only on May 11 (see Figure 4a for •e



Dinoflagellates from the Mixed Layer and Their Estimated Contributions to the Bioluminescence

Potential, July 21, 1990, at the MLML Station*

Number, m -3 BPOT, Dinoflagellatesõ photons, m 3

Autotrophs Ceratiumfusus 34 X 103 1.0 X 1013 Gonyaulax grindleyi 5 X 10 3 5.0 X 10 l• G. minima 1 X 10 3 1.0 X 1011

G. polygramma 1 X 10 3 3.0 X 1011 Total 1.1 X 1013

Hetertrophs Protoperidinium

bipes/breve 106 X 10 3 2.1 X10 TM P. cerasus 4 X 10 3 2.0 X 1012 P. crassipes 8 X 10 3 7.2 X 10 •3 P. globulurn/globulus 1 X 103 6.0 X 10 •2 P..heteracanthus 1 X 10 3 2.0 X 10 x2 P. minutum 6 X 10 3 1.2 X 1013 P. pellucidurn 3 X 103 7.0 X 10 •2 P. steinii 18 X 103 3.0 X 10 •2 P. sUbinerme 8 X 10 3 6.0 X 1012 P. tuba 1 X 10 3 2.0 X 1012 P. spp. (unidentified) 30 X 103 6.1 X 1013

Total 3.3 X 10 TM

*Surface temperature was ~11 ø C. Secchi depth was "8.2 m.

{}Mean counts of whole water samples from the surface, 10, and 30 meters

sampling map). Figure 4b shows the distributions of estimated BPOT at the different stations, partitioned among autotrophic dinoflagellates, heterotrophic dinoflagellates, and mesozooplankton. BPOT associated with the mixed layer seemed remarkably constant, within a factor of 2, in the presence of variable distributions of pigments [Batchelder et al., this issue; R.R. Bidigare, personal communication, 1993]. A great deal of the pigment found was due to the presence of a Phaeocystis bloom [Marra et al., this issue]. In all samples taken on this leg, autotrophic dinoflagellates were estimated to have produced <1% of the BPOT. Ceratium fusus, G. striata, G. polygramma, and Gonyau!ax spp. were present in the mixed layer in low numbers. Mesozooplankton from the 100 I•m mesh aperture nets were estimated to have produced "10% of the total bioluminescence. The rest of the estimated BPOT was due to heterotrophic Protoperidinium species. The most prevalent bioluminescent Protoperidinium was P. pallidum/pellucidum, which was estimated to produce -75% of the estimated dinoflagellate BPOT, while P. breve/brevipes and P. globulum were both responsible for "10% each. A minor contribution to BPOT was made by P. depressurn (<5 %) and P. crassipes (< 1%).

May 1991: Processes Leg We were able to deploy our modified BP probe during the

May processes cruise, in the vicinity of the second MLML mooring. Night profiles were taken May 18-19, 20-21 and

•60 .... ...'May 1'0 ß

• 'May-8 ß ..

'•lvlay 7 '" ':':: 5 ' 2• '

Longitude (øVV)

s,.::May 9 '

BPOT (1012photons m '$)

4O

3O

2O

10

- / / / / /

_ /

- / /

_

May7 May8 May9 May10 May11

Figure 4. Mesoscale mapping of BPOT, May 1991. The upper panel shows the position of net tows taken at night from the mixed layer, with the dotted line indicating the cruise track. The lower panel shows the BPOT estimated from organism concentrations. The lower cross-hatched part of the bar represents the contribution by mesozooplankton, the central solid zone represents the contribution by autotrophic dinoflagellates, and the upper open part of the bars represents the contribution of heterotrophic dinoflagellates. Zooplankton were not collected on May 11.

22-23, and "dawn" samples were taken on May 21 and 23. There was agreement (usually less than a factor of 2) between the BPOT estimated by counting cells in the BP nets and that estimated from measurements of mechanically stimulated bioluminescence in the BP.

Table 9a shows the estimates of BPOT and the bioluminescence measured from the BP on the nights of May 20 and 23. On May 18, the mixed layer depth was" 35 m, the chlorophyll fluorescence from the CTD-BP-fluorometer system was "1000" (relative units), and the mean BPOT was - 4.4 X 10 TM photons m 3. Following this, we had a wind event which diluted out the plankton in the mixed layer with water from below the thermocline which had little plankton in it. For example, on May 20 when we profiled the mixed layer depth was 90 m, the chlorophyll fluorescence was -"400" units, and the mean mixed layer BPOT was -1.4 X 10 TM photons m -3. During the calm weather on 22 May, the upper 20 m of the water column stratified. However, we did not detect any increase in BPOT per cell on May 23 in the upper layers due to the 1 day of stratification, the ratio of measured bioluminescence to cell number was not signifi- cantly different at different depths, and mixed layer BPOT was still -1.4 X 10 TM photons m -3.


Table 9a. Mean Concentrations of Bioluminescent Dinofiagellates in the BP Effluent and Their Estimated Contributions to the Bioluminescence Potential on May 20 and 23 near the MLML Station. {}

Genus May 20 May 23 and Species Number of cells, m -3 Number of cells, m -3

20m 30m 50 m BPOT 15m 30m 50m BPOT

Autotrophs Ceratium fusus 556 556 1667 5.0 X 1011 1762 3133 1958

Gonyaulax spp. 8889 19444 11667 1.3 X 1012 2742 5483 14883 G. polygramma 0 0 0 2838 0 0

Total 1.8 X 1012

Heterotrophs Protoperidiniurn brevipe•/breve 12778 23333 33333 4.6 X 1013 0 0 392

P. crassipes 556 0 0 1.6 X 1012 392 392 1958 P. curvipes 0 0 0 196 0 0 P. depressurn 0 0 0 979 3133 0 P. ovaturn 2778 28333 8333 1.3 X 1013 3721 5092 7442

P. pallidium 8333 7778 5556 1.0 X 1013 6463 6842 13317 P. pellucidurn 33889 53333 36667 8.3 X 1012 17429 25458 24283 P. steinii 1111 1111 0 1.0 X 1011 0 0 0 P. subinerrne 2778 3333 2222 5.6 X 1012 1175 10575 19581 P. thulense 0 0 0 0 392 392

P. spp. 30556 22222 28333 5.4 X 1013 4308 7442 13317 Total 1.4 X 1014

6.9 X 1011 3.4 X 101ø 1.6 X 10 n 1.2 X 1012

2.6 X 101• 8.0 X 10 •2 1.3 X 1011 7.0 X 1012 5.4 X i012 2.8 X 1013 4.5 X 1012

9.1 X 10 •2 3.9 X 1011 1.7 X 1013 6.9 X 1013

BPOT Estimated by Dinoflag;ellate Counts from Bathyphotometer Nets. 15 m 20 m 30 m 50 m

May 20 no sample 1.2 X 1014 1.5 X l0 in 1.5 X l0 in May 23 3.7 X 1'013 no sample 9.1 X 1013 8.1 X 1013

BPOT Estimated

From the Bathyphotometer Signals. 10 m 20 m 30 m 50 m

May 18 3.0 X 101 4. X 101 5. X 101 1.5 X 101 May 20 no sample 1.6 X 1014 1.7 X 1014 1.7 X 1014 May 23 6.2 X 1013 no sample 1.5 X 1014 2.2 X 1014

õ Mixed layer depth was 80 m on May 20, but there was some restratification of the top 20 m by May 23 during (unusual) calm weather. Each cell counted May 20 and 23 is represented by 556 and 196, respectively, in the table.

Table 9a shows, as during the mesoscale mapping leg, that autotrophic dinofiagellates were estimated to make only a small contribution to the BPOT (-1%) relative to that from the heterotrophic Protoperidinium species. Of the autotrophic dinofiagellates, C. f-usus contributed the most to BPOT. Among the heterotrop•, there were a small number of species that appear to have dominated the BPOT signal, P. brevipes/breve, P. depressurn, P. subinerme, and P. pallidum/pellucidum. BPOT was -3 times higher than during the mesoscale mapping leg. A set of vertically stratified mesozooplankton net tows on the night of May 23 (Table 9b) suggested that the mesozooplankton contribution to estimated BPOT was similar to that of the autotrophic dinoflagellates, "1-2% of the total BPOT.

August, 1991: Processes Cruise Only by the end of the cruise did we have relatively calm

weather with some restratification. We were able to make

one nighttime vertical profile (four samples) and to observe what were apparently photoinhibition effects during dusk and dawn. For the nighttime profile made on the night of August 31-September 1, cell numbers from the BP nets, estimated BPOT, and the BPOT per cell are given in Table 10a. For this profile, the heterotrophic dinoflagellates were estimated to produce almost two orders of magnitude more BPOT than the autotrophs. The numbers of dinoflagellates as predicted by net counts or by the number of bioluminescent flashes did not show much variation with depth, as might be predicted by considering the proceeding wind mixing events.

SWIFT ET AL.: NORTH ATLANTIC BIOLUMI•SCENCE 6539

Table 9b. Zooplankton Counts From Opening-Closing Nets Deployed on May 24, 1991 and the Estimated BPOT From These Counts

Genus Number, m -3 BPOT, Photons m '3 and Species

20 m 50 m 20 m 50 m

,

Metridia lucens

4th Copepodite 0 0.04 0 1.4 X 109 5th Copepodite• 0 0.04 0 3.2 X 109 Adult4 0 0.04 0 1.4 X 109 Adult • 0 0.2 0 2.4 X 10 xø

Pleuromamma robusta 0 0.3 0 2.0 X 10 n

Oikopleura labradorensis 0.2 0.6 1.2 X 10 n 2.8 X 10 n Thysanoessa longicaudata 7.8 20.3 8.6 X 10 n 2.2 X 10 e Tornopterus spp. 0.5 0.2 4.6 X 10 •ø 2.2 X 10 •ø Conchaecia spp. 0.2 2.7 1.2 X 10 xø 2.1 X 10 n Total 1.0 X 10 e 2.9 X 10 •

Table 10a. Mean Concentrations of Bioluminescent Dinofiagellates in the Nets Straining the Effluent of the Bathyphotometer and Their Estimated Contribution to the Bioluminescence Potential on the Night of August 31, 1991, With a Comparison to Results from the Bathyphotometer

Genus and Species Number of Cells, m -3 20 m 30 m 40 m 50 m

BPOT, photons m -3 •Mixed Layer Yrhe••e

Autotrophs Ceratiurn fitsus 28,000 18,000 29,000 17,000 2.7 X1012 Gonyaulax

polygrarnrna 0 1,000 1,000 2,100 8.0 X 101ø Gonyaulax spp. 2,000 0 0 0 1.0 X 1011

Total BPOT 2.9 X 1012

Hetero•xophs Protope ridiniurn brevipes/breve 34,000 12,300 13,000 6,300 4.6 X 1013

P. crassipes 6,000 3,100 7,000 2,100 4.0 X 1013 P. globulurn 0 4,100 0 1,000 1.1 X 1013 P. nudum 4,000 7,200 7,000 2,100 1.5 X 1013 P. oceanicurn 0 1,000 2,000 1,000 1.0 X 1012 P. palladium 3,000 3,100 8,000 6,300 4.3 X 1013 P. steinii 3,000 2,100 1,000 0 2.8 X 1012 P. spp. 24,000 7,200 27,000 6,300 3.1 X 1013

Total BPOT 1.6 X 10 TM

2.4 X 1012

4.7 X 1011

0

2.9 X 1012

1.9 X 1013 4.0 X 1013 2.3 X 1012 3.4 X 1012

2.0 X 1012 1.0 X 1013 7.0 X 1011 3.3 X 1013 1.3 X 10 TM

20 m 30 m 40 m 50 m

BPOT From the BP

8.0 V 7.9 X 1013 7.8 X 1013 4.4 X 1013 6.2 V 9.4 X 1013 1.0 X 10 TM 4.8 X 1013

BPOT From Dinoflagellates in the BP Nets 2.0 X 10 TM 1.1 X 10 TM 1.7 X 10 TM

Flashes m -3, From the BP 8.0 V 114,000 49,000 41,000 6.2 V 66,000 52,000 42,000

Number Dinoflagellates m-3 From BP nets 116,000 57,000 88,000

1.6 X 1013 3.4 X 1013

6.8 X 1013

46,000 49,000

43,000

Samples from 20 and 30 m are from the mixed-layer, from 40 and 50 m from the thexmocline.

6540 SWIFT ET AL.' NORTH ATLANTIC BIOLUMINESCENCE

Table 10b. Mesozooplankton Abundances Estimated From MOCNESS Tows on August 30, 1991, and With BPOT Estimated From These Abundances ô

Genus Numbers, m -3 BPOT, Photons m -3

and Species 0-26 m 26-51 m 0-26 m 26-51 m

Metridia lucens

4th Copepodire 0 5th Copepoditee 0 Adult • 5.2

Pleuromamma robusta 4.2

Thysanoessa longicaudata 16.6 Tomopterus spp. 0.5 Conchaecia spp. 4.8 Heterorhabdus spp. 0.2 Total

.10 2.2 x 109 0

0.2 0 1.5 x 1011

1 5.7 XlO 11 1.1 x 101• 1.3 3.2 x 1012 9.8 x 1011

23.5 1.8 X 1012 2.6 X 1012 0 4.9 X 101ø 0 0 1.5 X 101ø 3.6 X 1011

0.7 4.0 X 101ø 1.4 X 1011 5.6 X 1012 4.4 X 1012

ô With nets having a mesh aperture of 333 lxm, tow taken near midnight.

We towed a MOCNESS on the night of August 30-31 and on the night of September 1-2. The mixed layer and thermocline zooplankton abundances paralleling those for the BP prof'de samples are shown in Table 10b and Table 10c. These abundances and the accompanying estimates of BPOT suggest that the mesozooplankton contributed about as much to the total BPOT as the autotrophic dinoflagellates, and that their BPOT was expressed primarily in the mixed layer at night. Again, heterotrophic dinoflagellates were the primary source of bioluminescence.

During the dawn of August 28, we took five measurements of bioluminescence over a period of 2 hours at 30 na (Figure 5a). The BPOT based on the BP measurement was '•4 X 10 TM photons m -3 for the fLrst two readings. We observed that the stimulable bioluminescence was reduced

by an order of magnitude when the calculated underwater PAR (as scalar irradiance) reached '•0.1 I•mol photons m-: s- 1. The lack of more data points makes it difficult to establish a close association between ambient PAR and stimulable bioluminescence. The final BPOT value of about 5 X 1013

photons m -3 was similar to that observed at the beginning of the dusk time series on the evening of 1 September.

During dusk on September 1, we obtained 5 measurements of BPOT with 4 accompanying net collections (Figure 5b). The BP was at 20 m, and the measured stimulable bioluminescence began to increase when the underwater PAR fell below 0.1 I•mol photons m-: s -1. Table 11 shows that with increasing darkness, the numbers of stimulated flashes recorded from dinoflagellates only increased- 30%. The increase in BPOT was primarily due to about 5-fold increase in the amount of light measured per flash, and in an approximate four-fold increase in the mean value of the measured peak intensity of the flashes. The final value of BPOT was close to that observed on the night of May 28- 29.

Cell counts from the nets were more variable than the

counts of flashes in the instnm•ent. However, there was good agreement between the number of flashes recorded per liter and the numbers of dinoflagellates collected in the nets (within the limits of counting error), except for the sample at 2129. During sampling at one depth, the ship was drifting

slowly, thus we assumed that the dinoflagellate concentrations were relatively constant, and that the "low" count in the 2129 sample should be disregarded. The associated flashing rate is much higher than the count, and is consistent with flashing rates for the other samples.

Table 12 shows the composition of the dinofiagellates sampled during the dusk time series and their BPOT, with the low cell abundances from the sample at 2129 disre- garde& Again, ½. fusus dominated the autotrophic dinoflagellate contribution to BPOT. The numbers of autotrophic and heterotrophic bioluminescem dinoflagellates are about equal in the samples, but because of their higher TMSL, the Protoperidinium spp. produced '• 90% of the estimated BPOT, and the autotrophs, '•10%. The total estimated BPOT was about one-third that measured by the BP at the end of the time series. Here, as before, we have used a BP biological calibration based on ½. fusus, where BPOT is an order of magnitude greater than measured bioluminescence in the BP. But, here, as in 1983, with Protoperidinium spp. dominating the estimated BPOT signal,, a factor of three was probably more appropriate for the biological calibration than the ten we used. Using three we have good agreement between estimated and measured BPOT. Knowledge of the composition of the bioluminescent plankton is helpful in interpreting the results from a bathyphotometer.

Discussion

Organisms Producing BPOT A summary of the estimated contributions of autotrophic

dinoflagellates, heterotrophic dinoflagellates, and mesozooplankton to BPOT in the chronological order of the cruises, from 1980 to 1991 is shown in Figure 6. Several general trends are evident. First, dinoflagellates are primarily responsible for mixed layer BPOT on all the cruises. Second, the relative contribution of autotrophic dinoflagellates is larger in late summer and early fall than earlier in the year. Third, heterotrophic dinoflagellates appear to produce the bulk of the mixed layer BPOT (with the exception of September 1988). The results summarized in

SWIFt ET AL.: NORTH ATLANTIC BIOLUMINESCENCE 6541

Table 10c. Mesozooplankton Abundances Estimated From MOCNESS Tows on September 1, 1991, and With BPOT Estimated From These Abundances ô

Genus Numbers, m -3 BPOT, Photons m -3 and Species

12-22 m 22-32 m 12-22 m 22-32 m

Metridia lucens

4th Copepodite 0.1 0.1 2.2 X 109 2.2 X 109 5th Copepoditeo • 0.1 0.1 6.8 X 109 6.8 X 109 5th Copepodite• 0.1 0.03 8.0 X 109 2.4 X 109 Adult o • 0.1 0.03 3.6 X 109 1.1 X 109 Adult • 5.2 1.7 5.7 X 10 • 1.9 X 10 •

Pleuromamma robusta 2.3 2.3 1.7 X 10 •2 1.7 X 10 •2 Oikopleura labradorensis 0.2 0.5 1.0 X 10 • 3.0 X 10 • Thysanoessa longicaudata 5.3 11.0 5.8 X 10 • 1.2 X 10 •2 Tomopterus spp. 0 0.1 0 5.9 X 109 Conchaecia spp. 0.7 1.5 5.3 X 10 •ø 1.1 X 10 • Heterorhabdus spp. 0.3 0.4 6.0 X 109 1.0 X 101ø Total 3.0 X 10 •2 3.6 X 10 •2

Genus Numbers, m-3 BPOT, Photon m -3 and Species

32-42 m 42-62 m 32-42 m 42-62 m

Metridia lucens

2nd Copepodite 0.02 0.02 1.8 X 10 ? 1.8 X 108 3rd Copepodite 0 0.01 0 2.0 X 10 • 4th Copepodite 0.03 0.04 1.1 X 10 9 1.4 X 10 9 5th Copepoditeo • 0 0.02 0 1.4 X 109 5th Copepodite• 0.02 0.02 1.6 X 109 1.6 X 109 Adult o • 0 0.01 0 3.5 X llf Adult • 0.3 0.02 3.3 X 10 •ø 2.2 X 109

Pleuromamma robusta 1.2 0.1 9.0 X 10 • 7.5 X 10 •ø Oikopleura labradorensis 0.4 0.1 2.0 X 10 • 5.0 X 10 •ø Thysanoessa longicaudata 10.1 1.6 1.1 X 10 •2 1.8 X 10 • Tomopterus spp. 0.8 0.3 7.8 X 10 •ø 2.9 X 10 •ø Conchaecia spp. 7.7 9.5 5.9 X 10 • 7.2 X 10 • Heterorhabdus spp. 0.5 1.2 1.0 X 10 •ø 2.4 X 10 •ø Total 2.9 X 1012 1.0 X 1012

With nets having a mesh aperture of 333 Ftm, tow taken just before midnight.

Figure 6 extend geographically the evidence that dinoflagellates are a predominant source of bioluminescence in the mixed layer of oceanic and coastal regions [cf.. Kelly and Tett, 1978; Tett and Kelly, 1973]. In an extension of the Noxth Atlantic Drift Current along the East Coast of Norway, Lapota et al. [ 1989] also found C. fusus and Protoperidinium spp. as dominant sources of bioluminescence in September. This contrasts to •e region to the northwest of Iceland in cold (sub-zero) waters of the East Greenland Current [Buskey, 1991]. There, the copepods Metridia spp. and the larvaceans Oikopleura spp. appear to be the dominant source of stimulable biohminescence. Protoperidinium spp. are present, but in low numbers.. In warmer tropical and subtropical waters, autotrophic dinoflagellates and mesozooplankton make up a more significant component of BPOT [Buskey and Swirl, 1990; Lapota et al., 1988; Swirl et al., 1985; Swirl et al., 1983]

Seasonal Cycles in BPOT

Colebrook's [e.g., 1982a] summaries of the Hardy plankton recorder survey data near the MLML mooring site suggest that many bioluminescent species develop their maximum populations in middle to late summer (e.g., C. fusus, P. depressurn, Pleuromamma spp.) in the mixed layer. The plankton recorder sampled at a depth of 10 m . From Colebrook's summaries, one might have predicted that BPOT in the mixed layer would be highest in late summer. However, most of the Protoperidinium spp. (which we suggest here would normally dominate BPOT in the mixed layer) would be too small to be caught in the relatively coarse meshed nets of the plankton recorder. In contrast to the bioluminescent species reported by Colebrook, Proto- peridinium spp. numbers appear to increase at the time of the spring bloom and remain fairly constant through the summer


E 40

• •o

+ 20

•o

BPOT UW PAR

e-2e-91 '-.../

3 0 ITle•-......... •,..... o

o o

ß

4,5 5 5,5 6 6.5

0.1 •

0.01 E .__

0.001 LU

0,0001 • 0,00001 •

E 30

a. 20

-i-

•o

UW PAR BPOT

ii

9-1-91 ...'

20 meters.......' i ii i i

20.5 21 21.5 22

0.01 c

0,001 '-'

0.0001 0,00001

Hours (UT)

Figure 5. Effects of ambient light on mechanically stimulable bioluminescence, August-September 1991. (a) Decrease over time of the stimulable bioluminescence at 30

m as measured by the BP at dawn, August 28, 1991, plotted against the logarithm of calculated scalar irradiance. The bottom panel (b) is a similar plot at dusk (9/1/91) showing the increase of stimulable bioluminescence against the logarithm of estimated scalar irradiance at 20 m.

and early fall. This may explain why our estimates of BPOT in the mixed layer appeared to remain rather constant from spring to fall once the MLML region stratified.

We found, in agreement with Colebrook's data [ 1982a, 1982b, 1986], that the number of autotrophic dinoflagellates (including the bioluminescent species C. fitsus and G. polygramma) increased toward the end of the summer. This increase was shown both in our plankton counts and by the increased concentrations of peridinin in the mixed layer. However, except for one depth at sta. 6 in 1983 and for the mixed layer near the MLML station in 1988, in our samples, the autotrophic dinoflagellates were a small component of the BPOT in the mixed layer.

The one "wintertime" unstratified condition we sampled in early April 1989 suggested that both autotrophic and heterotrophic dinoflagellates were present in low numbers. Our sample suggests that autotrophic and heterotrophic dinoflagellates would make similar contributions to the BPOT, and that BPOT would be several orders of magnitude lower than after stratification set in. These "wintertime"

abundances and species were in agreement with previously reported observations on the plankton from ocean station India [Corlett, 1953; Williams and Robinson, 1973; e.g. Williams and Wallace, 1977]. The report of Colebrook [ 1986], summarizing all plankton recorder collection regions, suggests that C. fitsus at MLML might be expected be undetectable in late March, reach its maximum abundance in July associated with the peak in sea surface temperature, and then decrease to undetex'mble concentrations by November.

Among all the North Atlantic oceanic regions covered by the plankton recorder surveys, it appears that the region south of Iceland where we sampled has some of the highest midsummer concentrations of C. fitsus.

From culture and other studies, it appears that C. fitsus does not grow well at temperatures typical of the April-May period (8-9øC) [Nordli, 1957; Colebrook, 1982b] and temperature may in fact limit its growth rate at the MLML site until late summer. This dinoflagellate might be advected from south of the Grand Banks and serve as a seed population when growth conditions are favorable [R.N. Sambrotto et al., The role of coastal population dispersal in the initiation of oceanic diatom blooms in the sub-arctic Atlantic Ocean, submitted to Journal of Geophysical Research, 1994]. From the accompanying nutrient and pigment profiles taken in April 1989, it appeared that all nutrients were present in high concentrations in what was to become the mixed layer. By early May, when we were present at the site in 1991, the mean mixed layer light intensities may have exceeded that needed for maximal division rate [Sullivan and Swirl, this issue].

We speculate that the increase in populations of phytoplankton provided some of the particulate food that allows populations of Protoperidinium spp. to increase their concentrations [Gaines and Elbr&zhter, 1987; Jacobson and Anderson, 1986; Lessard and Swirl, 1985]. During the May 1991 cruise, high chlorophyll a concentrations were present ( >2,000 ng L), although mixed layer temperatures were -8øC. These high chlorophyll concentrations appear to persist in this region until late in September [Colebrook, 1982a, 1982b; Esaias et al., 1986] and may represent the phytoplankton food that sustains the populations of Protoperidinium species. In late summer, the higher surface temperatures (12øC) prevent storms from mixing surface waters as deeply as they did in the spring, and this should result in an increase in the mean mixed layer light intensity. In agreement with Colebrook [1986], we suggest that the higher temperature and mean mixed layer light intensities allowed C. fitsus and Gonyaulax spp. to grow and divide, and to produce an increased amount of the mixed layer BPOT in the fall.

Interannual Variability In producing a composite in Figure 6 based on the time of

year of various research cruises, we are assuming that year- to-year differences are small. This assumption is primarily based on Colebrook and Taylor• [ 1986] report that plankton abundances due to the seasonal cycle were much greater than the year-to-year changes. If interannual variability is in fact small, then the unusual features we found on certain cruises are probably due to spatial variability. For example, the high abundance of C. fitsus in 1988 would represent a patch of that species, and not an unusual "C. fitsus year" in 1988. In support of this, there are reports of C. fitsus patches in other years [Lapota et al., 1992b]. This is not to suggest that there is no interannual variability in this species' abundance. Colebrook and Taylor [1986], and Colebrook [1982a] also reported that the interannual abundances in the Ceratium group (including C. fitsus) were negatively associated with sea surface temperature and the frequency of cyclonic weather throughout the plankton recorder survey region. Ceratium fitsus was a species which was reported to show


Table 11. A Comparison of BPOT, Hash Intensity, Hash Duration, and Bioluminescence per Hash During Dusk on September 1, 1991, at 20 m Depth During the Apparent Release of Photoinhibitionô

Start Time

6.2V, 8.0V BP's Flash Numbers Dinoflagellate Counts

BPOT Intensity Flashes, BP Total Heterotrophs Autotrophs (photons m '3) (photons s 'l) (m '3) (m '•) (m '•) (m 's)

2031 7.5 X 10 x3 3.0 X 109 52,000 48,000 9,000 40,000 2035 5.7 X 10 x3 2.2 X 109 65,000

2049 7.8 X 10 x3 3.3 X 109 72,000 87,000 42,000 46,000 2054 7.4 X 10 •3 2.3 X 109 74,000

2110 1.4 X 10 •4 4.8 X 109 60,000 2114 1.8 X 1014 6.0 X 109 63,000

2129 2.4 X 1014 6.5 X 109 113,000 8,000 6,400 1,700 2133 2.6 X 1014 6.8 X 109 88,000

2200 3.1 X 1014 1.0 X 10 lø 82,000 95,000 40,500 55,000 2204 2.9 X 10 •4 9.8 X 109 79,000

ô BPOT is calculated from the BP signal or from the dinoflagellate counts in the nets collecting the effluent from the BP, Number of flashes is flashes stimulated by the BP per cubic meter, Flash intensity. is the mean peak flash intensity in photons per second. In order to correct for any coincident flashes, a residence time of 0.1 s was assumed. For each 8-min sample, the first four minutes was run with the voltage of the PMT at 620 V, for the second 4 min. reading, the voltage was raised to 800 V. Values recorded at PMT voltage -800 V were normalized to the readings at - 620 V.

* Net sample not taken

little seasonal variability over its geographical distribution [Colebrook, 1982b].

Aebischer et al. [1990] have reported on the long-term biomass trends in zooplankton and phytoplankton in the eastern North Atlantic. Despite the greater persistence of zooplankton in the water column, their abundances tend to co-vary with phytoplankton. Thus we anticipate that the relative importance of zooplankton and dinoflagellates will not show a great deal of interannual variability. The relative abundances of bioluminescent zooplankton (e.g. Metridia) between abundant and scarce years appears to be about threefold [Colebrook, 1985]. The zooplankton generally produced "1-2% of the BPOT in our samples, so whether we were sampling an "abundant" or a "scarce" year, we expect that they might normally produce a minor component of BPOT.

Other Estimates of BPOT

Nellson et al. [this issue) have compared areal values of relative brightness for different regions of the ocean, and noted that at the MLML station, summer season values of biohminescence intensity are not dissimilar to those reported for "...the Beaufort, Caribbean, Greenland, and Sargasso Sea .... " However, as the authors report, the MLML region is not as bright as the Arabian Sea, or some inshore locations. Their BP measured brightness, and the numbers they report for the MLML region are derived from the optical calibration of the Msmnnent [Widder et al., 1993]. Ondercin et al. [this issue] measured biohminescence intensity in the MLML region in August, 1991 before

Hurricane "Bob" broke down the late summer water column

stratification, and reported values of 0.4 to 1.0 X 10 TM photons s 4 m -3. Ondercin et al.'s bioluminescence brightness measurements seem in agreement with the measurements taken by Neilsen et al. [this issue] before Hurricane Bob.

The conversion from bioluminescence "brightness" to the BPOT values estimated here depends on the bioluminescent organisms present, their physiological state, and the pumping rate and intensity of stimulation in the BP (These data are needed for the biological calibration of these BlYs [Widder et al., 1993]). To attempt such a conversion for the BP used by Nellsen et al., we used values of bioluminescence intensity for the mixed layer from Table 2 in Nellson et al. [this issue], and calculated that they measured 2 X 1013 photons m 3 in May and 6 X 10 •3 photons m -3 in August. In calculating the August values, we excluded their first cast which occurred before Hurricane Bob, as we have no measurements before then to compare with theirs. Next, we convened their BP optical calibration to BPOT via an assumed biological calibration: With their BP having a residence time of •'1 s, similar to our BP (as our BP was configured in 1983-1988), and with the sampled populations in 1991 dominated by Protoperidinium spp, as they were in 1983, we assume that a factor of 3 would also be appropriate to convert their optical signal to BPOT. With these assumptions, Neilsen et al. L• estimated BPOT in May 1991 (Leg 2) would be -6 X 10 TM photons m 3, whilst our estimate from plankton counts on Leg 2 was -4 X 10 TM photons m 3. For August (Leg 1), the Neilsen et al. estimated BPOT would be" 2 X 10 TM



Dinoflagellates in the Nets Capturing the Effluent of the Bathyphotometer, and Their Estimated Contribution to the Bioluminescence Potential During Dusk Measurements, Described in Table 11•'

Genus Dinoflagellate Estimated and Species Abundance BPOT,

m -5 photons m -5 , , ,

Autotrophs Ceratium fusus 4.6 X 10 • 1.4 X 1013 Gonyaulax polygramma 2 X 10 a 2.9 X 1011 Gonyaulax spp. 1 X 1!f 5.9 X 101ø

Total 1.4 X 1013

Heterotrophs Protoperidinium brevipes/breve 1.1 X 1!f 2.1 X 1013

P. concoides 0.2 X 10 • 3.9 X 1011

P. crassipes 5 X 10 a 4.1 X 1013 P. globulum 2 X 1!f 1.1 X 1013 P. minutum 1 X 1!f 3.2 X 1011 P. nudum 2 X 10 • 2.7 X 1013 P. oceanicum 0.4 X 10 a 8.0 X 1011 P. ovatum O. 4 X 10 a 4.0 X 1011

P. palladium 3 X 1!f 4.0 X 1012 P. steinii 2 X 10 • 2.8 X 1012

P. spp. 10 X 10 a 2.0 X 1013 Total 1.0 X 1014

•- Net collections have been combined and averaged (with the exception of the "low" sample at 2129 UT).

photons compared to our estimate from plankton enumerations of 2 X 10 TM photons m -3. Our own BP measurements in August estimated a BPOT of 1.3-1.6 X 10 TM photons m -3. Due to the spatial and temporal patchiness in the bioluminescence signal, these data suggest reasonable agreement between BPOT estimated from the different BPs as well as

agreement between BPOT estimated from plankton enumerations and from BP signals.

Nutritional Effects:

$weeney et al. | 1959] described two effects of light on the stimulable bioluminescence of autotrophic dinoflagellates. The first effect, photoenhancement, referred to the enhance- ment of nighttime stimulable bioluminescence by light the cells received the previous day. Increasing amounts of light allowed the cells to produce increasing amounts of subsequent nighttime biohminescence. According to a recent laboratory and field study on photoenhancement [Sullivan and Swirl, this issue], a fivefold to ten-fold increase in biohminescence capacity per cell can occur in C. fusus over the light range spanning from the compensation intensity to intensities producing supersaturation of photosynthesis. With the exception of 1988, we did not observe clear examples of the effects of photoenhancement for C. fusus or other autotrophic dinoflagellates in the at-sea data from our BP reported here. Sullivan and Swirl [this issue] also

600 BPOT (1012photon s m '•)

500

400

300

200

IO0

Apr. U,y,, duly Apr. 89 July •ug 89 Sept

Figure 6. A summary of the estimated contributions of different groups of the organisms to BPOT. The lowest section of each bar represents the contribution of mesozooplankton, the middle represents the contribution of autotrophic dinoflagellates, and the top represents the contribution of the heterotrophic dinoflagellates.

measured the bioluminescence capacity of individual C. fitsus cells from the MLML site and found examples where cells isolated from the mixed layer had a larger biohminescence capacity than cells isolated from the thermocline (May !991) as would be expected, but also the unexpected case where the opposite was true (August, 1991).

The amount of nocturnal biohminescence produced by Protoperidinium spp., in an analogous fashion, might be due to their nutritional state as affected by the concentration and quality of food available to them. Buskey et al. [1992] have reported that the bioluminescence capacity of heterotrophic dinoflagellates decreased by about a factor of 3 when they were put in seawater which had been filtered to remove their food. In our at-sea measurements of bulk biohmines-

cence, we did not observe a trend in the bioluminescence per cell when the chlorophyll decreased from 75 ng L -1 to 4.5 ng L 1 and BPOT was dominated by heterotrophic dinoflagellates. This may mean that the dinoflagellates had not been exposed to the low food concentrations long enough to lose bioluminescence capacity, or that the low chlorophyll concentrations were above the saturation value for maintain-

ing BPOT, or that chlorophyll is a poor surrogate for the food used by Protoperidinium to maintain its BPOT (some species appear to feed exclusively on bacteria according to Lessard and Swirl 11985]).

Photoinhibition

A second phenomenon described by Sweeney et al. [ 1959], photoinhibition, describes the suppression of mechanically stimulable bioluminescence' by light. While not all heterotrophic dinoflagellates appear to exhibit photoinhibition, a notable example being Noctiluca [Nicol, 1958], some species of Protoperidinium have been shown to exhibit this phenomenon [Filimonov and Sadovskaya, 1986; Buskey et al., 1992]. At the MLML site, where Protoperidinium is the primary source of bioluminescence, the changes in BP measurements taken during the day, at dawn and at dusk, as described in this manuscript, can only be explained if

SW-I• ET AL.: NORTH ATLANTIC BIOLUMI•SCENCE 6545

photoinhibition of most of the species of Protoperidiniurn was occurring.

We have described here the agreement between the spectral response of C. fitsus photoinhibition in the sea and in laboratory cultures. Taking into account the spectral nature of the photoinhibition response may improve our ability to predict its occurrence in the sea. For example, the optical nature of the water at the MLML site is that of productive waters, in the sense that the wavelengths of maximum transmission are in the green, and that the amount of shifting from the blue to the green is related to the amount of chlorophyll found in the water (also, K. Carder and R. G. Stewart, Optical models of the spectrum of downwelling light at the ML-ML site, submitted to J. Geophysical Research, 1994). In our earlier studies, we have associated photoinhibition with a broad-band measure of submarine light (PAR). With photoinhibition being a blue light response, and the underwater light increasing in "greenness" with depth and with chlorophyll concentration, there is an increasing mis-match between the light measured as PAR and the amount of photoinhibition it causes. With all these caveats, 0.1 l•mol photons m -2 s -• of ambient PAR (as scalar irradiance) did seem to be a reliable value to associate with complete photoinhibition of the Protoperidiniurn-dominated populations. If the Protoperidiniurn action spectrum of photoinhibition is similar to that of C. fitsus, as it appears to be [Li and Swift, unpublished data, 1993], the sensitivity of these "unpigmented" cells to blue light is even greater than that of C. fitsus.

Previous studies have shown that while dinoflagellates might produce small amounts of stimulable bioluminescence in the light, the amount of stimulable bioluminescence can increase by as much as 3 orders of magnitude when cells are placed in the dark [e.g. Biggley et al., 1969]. The degree of photoinhibition appears to be related to the log of light intensity [Sullivan and Swift, 1994] which implies that in the sea at a depth where the light is dim, there would be little change in stimulable dinoflagellate bioluminescence between day and night. This was shown in some of our profiles from 1983 and in September 1991, and suggested in measurements by Yentsch et al., [1964].

Acknowledgments We wish to thank Donna Van Keuren and Sharon Northby for their meticulous enumerations and identifications of dinoflagellates. Zooplankton enumerations were kindly made available to us for calculations of BPOT for September 1980 and April 1981 by M. Geiger, NAVOCEANO, Stennis Space Center, Mississippi.. Our 1983 cruise on RV Endeavor was supported through a grant to E.S. from the U.S. National Science Foundation, OCE-81-17744, and with funds from the Office of Naval Research, N00014-18-0062. The 1988 cruise on USNS Bartlett was supported by an ONR (N00014-87- K-0235) grant to E.S. and our participation was possible through the kind invitation of Rudy Hollman, Ocean Optics and by support from Ken Ferer, both at NOARL, Stennis Space Center, Mississippi.. Extracted chlorophylIs for 1988 were kindly provided by J. Matra, Lamont Døherty Geological Observatory. Cruises from 1988 through 1991 were made in conjunction with the Office of Naval Research Accelerated Research Initiative, Marine Bioluminescence and Upper Ocean Physics, grant N00014-87-K-0235 to E.S. Pigment analyses by R. Bidigare were supported by an ONR contract, N00014-89-J-1691. In the extremely rough weather at the MLML site, many over the side operations were only possible through the superb seamanship

and experience of the ships officers and crews. Many students and fellow professionals made key contributions at sea to this study: we particularly wish to thank Bill Hahn (1983), James Griffin (1983), Barbara Nowicki (1983), P. Verity (1983), Deneb Kateritz (1983), Henry Rines (1983), Carol Knudson (1988), David Buffer (1988), Dave Nelson (1991), and Ken Ikeson (1991). Three anonymous reviewers and the guest editor made valuable suggestions to help improve the manuscript.

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H. P. Batchelder, U.S. Globec Office, Dept. of Integrafive Biology, University of California at Berkeley, Berkeley, CA 94720. (email: [email protected])

R. R. Bidigare, Department of Oceanography, University of Hawaii, Honolulu, HI 96822. (email: [email protected]. hawaii.edu)

J. M. Sullivan, E. Swift, R. D. Vaillancourt, and J. Van Keuren, Graduate School of Oceanography, University of Rhode Island, South Ferry Road, Narragansett, RI 02882-1197. (email: jsully-, lige-, jvankeur-, and vaill @ gsosunl.gso.uri. edu)

(Received November 5, 1993; revised July 6, 1994; accepted July 18, 1994.)

Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude...

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