diel patterns of planktonic bioluminescence in the northern sargasso sea

Marine Biology 113, 329-339 (1992)

Marine Biology @ Springer-Verlag 1992

Diel patterns of planktonic bioluminescence in the northern Sargasso Sea Harold P. Batehclder, Elijah Swift and Jeffrey R. Van Keuren

Graduate School of Oceanography, University of Rhode Island, Narragansett, Rhode Island 02882, USA

Date of final manuscript acceptance: January 29, 1992. Communicated by J. Grassle, New Brunswick

Abstract. Day-night changes in the vertical distribution, intensity, and size of bioluminescence flashes were inves- tigated during a series of cruises to the northern Sargasso Sea in 1987 and 1988. Overall, depth integrated bioluminescence potential and flash density estimated from in situ measurements with a pumping bathyphotometer were 2 to 5 x higher at midnight than at midday. Depths from 50 to 100 m exhibited the most substantial day to night increases in bioluminescence potential and flash density. When classified by flash size (photon output per flash event), the increase from day to night was significant for all flash sizes, but was most dramatic for small flashes producing < 7 x 1 0 8 photons flash- ' . Biolu- minescence potential and flash density increased 2 to 3 x during bathyphotometer measurements made at dusk. Bioluminescent light budgets estimated from day and night net collections in May and August 1987 also predicted 2.5 x higher nighttime than daytime mesoplankton bioluminescence. However, large bioluminescent taxa (mesoplankton) capable of significant vertical migrations only contributed on the order of 15% of the total bioluminescence in surface waters. Our results do not support the idea that most of the nightly increase in bioluminescence potential and flash density are due to vertical migration of bioluminescent organisms; rather they are consistent with an alternate view that photoinhibition of bioluminescent flashing by dinoflagellates may be primarily responsible for the diel patterns.

Introduction

Recently there has been a renewed interest in understand- ing the distribution of bioluminescence in the world's oceans (Marra and Hartwig 1984, Marra 1989) and in determining which types of organisms are principally responsible for the bioluminescence (Swift et al. 1985, Batchelder and Swift 1989, Lapota et al. 1989; Buskey and Swift 1990). Partly, this is due to the development of in situ probes (pumping bathyphotometers) which provide near-real time vertical profiles of stimulable bioluminescence (Yentsch etal. 1964, Clarke and Kelly

1965). One of the goals of the Biowatt Program (Biolu- minescence and Optical Variability in the Sea) was to study the temporal and spatial distribution and dynamics of bioluminescence in the northern Sargasso Sea (Marra and Hartwig 1984, Dickey et al. 1986). Batchelder et al. (1990) reported on longer-term (seasonal) variability of bioluminescence intensity and distribution near the Biowatt Site (ca. lat. 34~ long. 70~ in the northern Sargasso Sea. In the present paper we report the results of field studies investigating shorter time-scale variation in the planktonic bioluminescence fields of the upper ocean of the northern Sargasso Sea.

In the Sargasso Sea, epipelagic bioluminescence intensity and flash rate (or flash density) are known to vary dielly (Lapota and Losee 1981, Neidhardt 1989). The amount of in situ measured stimulable bioluminescence in surface waters is 4 to 10 times greater during nighttime hours than during the daylight hours. Macroplanktonic bioluminescence potential in the upper 200 m is less during the day than at night in the Sargasso Sea due to verticaI migration of some of the brightest bioluminescent light sources, the Pleuromamma spp. copepods, to depths greater than 200 m during the day (Batchelder and Swift 1989). Microplankton may also be important in generating diel cycles in bioluminescence through photoinhibition of stimulable bioluminescence in the dinoflagellates (Haxo and Sweeney 1955, Yentsch etal. 1964, Hamman et al. 1981, Neidhardt 1989). There is no consensus on the extent to which daytime depression in bioluminescence potential and flash density in the surface waters of the Sargasso Sea are caused by photoinhibition of non-migratory bioluminescent organisms vs departure of migratory bioluminescent organisms (Swift et al. 1983, Swift et al. 1985, Batchelder and Swift 1989, Neidhardt 1989). In this part of our Biowatt studies at an oceanic station in the northern Sargasso Sea, we documented the daytime and nighttime vertical distributions of bioluminescence potential (BPOT) and flash density (FD), measured the changes in these parameters and organism abundances during the transition periods from day-to- night and vice versa, and attempted to determine the importance of various mechanisms in causing these diel changes.

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Materials and methods

S t a t i o n l o c a t i o n s a n d d a t e s

The distribution of bioluminescence and the abundance of plankton were measured on five cruises, in March, May, August, and Novem- ber 1987 and in March 1988, in the vicinity of the Biowatt mooring site (34~176 Table 1 lists the sampling dates and locations for the bathyphotometer deployments and plankton collections reported in the present paper.

B i o l u m i n e s c e n c e m e a s u r e m e n t s

We evaluated day/night differences in specific bioluminescence potential and flash density (hereafter BPOT and FD, respectively; for definitions see Batchelder et al. 1990) using a pumping in situ bathyphotometer [for instrument description see Batchelder et al. (1990) and Swift et al. (1983, 1985)]. Paired daytime and nighttime profiles (CTD and bathyphotometer) from 0 to 200 m were obtained twice in August 1987 using the methods described by Batchelder et al. (1990). The effluent from the light-detection chamber was directed to one of ten plankton nets so that organism abundances could be estimated later. The low pumping rate of ca. 15 liters m in - 1 prob- ably resulted in only small and/or weakly motile organisms being sampled (Swift et al. 1985).

In addition to the midday/midnight comparisons, we measured bioluminescence intensity at a fixed depth, 70 m, during five dusk periods: twice in May 1987, once in August 1987, and twice in

H.P. Batchelder et al.: Sargasso Sea planktonic bioluminescence

March -Apr i l 1988. During each of these dusk periods, bioluminescence was measured during discrete 8 to 12 min samples (total time of sampling usually covered 2 to 2.5 h). Six to ten discrete samples of the organisms passing through the bathyphotometer light-detection chamber were collected in 25 ~tm plankton nets and preserved in 4% buffered-formalin for taxonomic analysis.

M e s o p l a n k t o n c o l l e c t i o n s

Large ( > 153 p.m), motile planktonic organisms, were sampled during May and August 1987 using a 1 m 2 MOCNESS plankton net (Wiebe et al. 1985) to supplement information about the organism densities obtained from the pumping bathyphotometer, and to specifically evaluate the importance of vertical migration of bioluminescent mesoplankton as a mechanism for diel changes in bioluminescence. Two net sampling strategies were used: a series of vertically non-overlapping samples covering the upper 200 m of the water column in ca. 25 m depth strata, and a series of time consec- utive samples from a constant depth. The first sampling strategy was used to sample near midday and midnight and was intended to identify the gross day/night differences in the vertical distribution and abundance of larger bioluminescent taxa. The second strategy was used at dawn or dusk to evaluate temporal changes in the abundance of vertically migrating bioluminescent zooplankton. Upon retrieval of the sampling gear to the deck, the nets were rinsed down and the contents preserved with 5 to 10% buffered formalin- seawater.

Table 1. Sampling stations for (a) time series measurements of bioluminescence parameters, (b) daytime and nighttime profiles ofbio- luminescence parameters, and (c) zooplankton net collections in the

northern Sargasso Sea in 1987 and 1988. Time is zone time (ZD + 5 h); latitude is North; longitude is West; depth is in meters

Stn Date Time (hrs) Lat. Long. Depth Comments

(a) Time series measurements of bioluminescence:

E1C16 18 May 1987 19:43-21:00 34~ ' 69~ ' 70 Dusk E1C19 22 May 1987 19:49-21:26 34~ ' 70000 ' 75 Dusk E2C11 25 Aug 1987 18:55-21:00 34~ ' 69059 ' 71 Dusk B2C5 23 Mar 1988 17:06-19:45 30~ ' 69055 ' 71 Dusk B2C18 02 Apr 1988 17:09-19:42 30048 ' 72051 ' 70 Dusk

(b) Day/night comparisons of bioluminescence parameters: E2C7 23 Aug 1987 14: 50-16:33 34~ ' 69~ ' 0 -151 Day E2C8 24 Aug 1987 00 :32-02:07 34~ ' 69059 ' 0-151 Night

E2C9 24 Aug 1987 23:06-00:46 34~ ' 69058 ' 0 -150 Night E2C10 25 Aug 1987 13: 37-15:18 34~ ' 70~ ' 0 -150 Day

(c) Zooplankton net collections: E1Mocl 12 May 1987 22 :52-00:07 34003 ' 70~ ' 0 -200 E1Moc2 14 May 1987 01 :33-03:07 34o00 ' 70~ ' 0 -200 E1Moc4 14 May 1987 22:31-23:57 34~ ' 70~ ' 0 -200 E1Moc5 18 May 1987 19:29-20:42 34004 ' 69~ ' 64-120 E1Moc6 19 May 1987 19:54-20:56 34005 ' 69~ ' 50-120 ElMoc7 20 May 1987 04 :43-05:52 34006 ' 69~ ' 83-125 E1Moc8 23 May 1987 00:33-01:28 34006 ' 69~ ' 0 -200 E1Moc9 23 May 1987 13:35-14:24 34007 ' 69~ ' 0 -200 E1Mocl0 24 May 1987 19:35-20:36 34o05 ' 69058 ' 90-100 E2Moc2 18 Aug 1987 22:23-22:55 34044 ' 69059 ' 0 -200 E2Moc3 21 Aug 1987 02 :59-03:37 33058 ' 68050 ' 0 -200 E2Moc5 24 Aug 1987 04 :37-06:56 34o02 ' 70~ ' 75 - 85 E2Moc6 24 Aug 1987 15:45-16:28 33~ ' 70001 , 0 -200 E2Moc7 25 Aug 1987 02:07-02:47 34004 ' 70~ ' 0 -200 E2Moc8 26 Aug 1987 01 :28-02:06 34005 ' 69o59 ' 0 -200

Night, full moon clear Night, full moon, hazy Night, cloudy Dusk, sunny Dusk, hazy Dawn Night, before moonrise Day, sunny Dusk, clear Night Night Dawn Day, partly cloudy Night Night


Taxonomic analysis

Pumped samples

All organisms retained by a 160 gm screen were removed and the bioluminescent individuals (ostracods, larvaceans, some copepods, euphausiid juveniles, and the large dinoflagellates Pyrocystis noc- tiluca and P. lunula) were identified and counted using a dissecting microscope. Organisms < 160 gm were enumerated by the Uterm6hl method (Hasle 1978). The < 160 p~m fraction was adjusted to 0.4 liters total volume and then a 50 or 100 ml subsample was settled in an Uterm6hl chamber for at least 24 h. Armored dinoflagellates were enumerated using phase-contrast microscopy (authorities for identifications were Lebour 1925, Taylor 1976, and Dodge 1985). Protozoans suspected of being bioluminescent (Lee et al. 1985), as well as the immature life stages of taxa having known bioluminescent members (such as copepods and small ostracods), were also counted in the < 160 gm fraction.

Net samples

Bioluminescent plankton abundances from MOCNESS and ring- net samples were estimated from Folsom splitter (McEwan et al. 1954) subsamples. All counts were corrected for sampling volume and fraction of the sample counted and are reported as the density per sample volume (usually per liter for dinoflagellates or per 100 m 3 for zooplankton).

Light measurements

Light intensity at the sea surface was measured continuously from dusk until dawn using a photomultiplier-based low intensity scalar irradiance sensor mounted on top of the ship's mast (Van Keuren et al. 1987). A light shield mounted below the sensor was used to block light produced by the ship. During some daytime observations, spectral irradiance was recorded at deck level using a Bio- spherical Instruments MER-1010. In May 1987, photon flux in the photosynthetic bandwidth (400 to 700 nm) was measured continuously throughout the cruise with a LICOR Model LI-190SB Quan- tum Sensor with a LI-550 printing integrator. Occasionally, daytime casts to 150 m were made with the MER-1010 to measure spectral attenuation coefficients.

331

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Fig. 1. Vertical profiles of temperature, density (sigma-t), relative fluorescence (Fluor.), bioluminescence potential (BPOT), and flash density (FD) for daytime (dashed line; filled squares) and nighttime (continuous line; filled triangles) bathyphotometer deployments on (A) 23-24 August, and (B) 24-25 August 1987. FU: fluorescence units

Results

Bioluminescence measurements - day vs night

Two pairs of day and night profiles were obtained with the pumping bathyphotometer during August ]987. The hydrographic results from the paired comparisons of these four profiles (two nights/two days) were alike in most respects (Fig. 1). Temperature and sigma-t indicated a well-mixed layer ( ~ 27 ~ from the sea surface to 38 m and a strong thermocline region from ca. 40 to 60 m. Below ca. 60 m, temperature declined gradually to a minimum of 19 ~ at 200 m. Chlorophyll concentration as measured by a flash fluorometer was low [ < 15 fluorescence units (FU)] and fairly constant from the surface to 60 m. A subsurface chlorophyll maximum ( > 30 FU) occurred at 75 to 125 m, with peak fluorescence between 85 and 105 m. The magnitude of the fluorescence maximum did not differ in a consistent way between day and night profiles, although the peak was higher ( > 80 FU) on the

first day and night than during the second day-night pair (,-~ 60 FU).

Unlike the hydrographic data, FD and BPOT showed marked differences between day and night measurements (Fig. l). FD (flashes m - 3) was much more uniform with depth and significantly lower at most depths during the day than during the night. The profiles of FD differed most at depths where nighttime maxima occurred. For example, FD at 70 to 90 m on the second day was only 20% of FD on the second night at those depths.

Highest nighttime BPOT ( > 16 x 1013 photons m - 3) occurred at ca. 90 m, coincident with the depth of maximum fluorescence. BPOT at night in the uppermost 25 m and at depths > 120 m was only 20% that found at the depth of maximum BPOT, although all depths except 200 m had BPOT >1 x 1013 photons m -3. During the day all samples from depths < 30 m had less than 1 x 1013' photons m - 3. The "replicate" daytime profiles of BPOT indicated the presence of substantial variability. For in- stance, there were depths at which BPOT was as high

332

during the day as at night (Fig. 1 A), although most depths, especially from 60 to 100 m, had significantly lower BPOT during the day than at night. BPOT on the second day was nearly uniform with depth and, except at 200 m, less than BPOT during the second night.

When comparisons were made on a 0 to "150 m depth- integrated basis, daytime BPOT was 33 to 60% of nighttime BPOT, and daytime FD was 21 to 51% of nighttime FD (Table 2). For both BPOT and FD the difference between day and night was greatest for the second data set. To evaluate the role of different individual flash sizes

Table2. Depth integrated (0-150m) bioluminescence potential (BPOT), flash density (FD), and flash size analysis from August 1987 profiles in the Sargasso Sea

Date BPOT Day/night FD Day/night (photons BPOT ratio (flashes FD ratio m -z) (%) m -2) (%)

(a) Depth integrated BPOT and FD for all sized flashes combined:

23 Aug 1987 Day 5.0x 1015 60 43 600 51 Night 8.3 x 10 i5 85 200

25 Aug 1987 Day 4.1 x 1015 33 22 600 21 Night 12.4 x 1015 107 800

Date <7 x 10 s 7 x IO s to >7 x 101~ photons 7 • 101~ photons flash -1 (%) photons flash -1 (%)

flash- 1 (%)

(b) Depth integrated daytime FD as percentage of depth integrated nighttime FD: 23 Aug 1987 25.4 56.4 68.5

25 Aug 1987 15.9 18.4 22.0

Table 3. Taxon, trophic/size category and estimated bioluminescence potential of the dominant bioluminescent groups in the Northern Sargasso Sea. TMSL: total mechanically stimulable light

Trophic Species ID Effective TMSL category (photons ind.- 1)~

Autotrophs Gonyaulax spp. 1 x 108 Pyrocystis spp. 5 • 101~ Ceratium fusus 5.4 • 10 s Ceratium horridum 5.4 • 10 s

Micro- Protoperidinium spp. 2 • 109 heterotrophs Copepod nauplii 8 • 10 s

Macrozoo- Ostracods 4 x 101~ plankton Oikopleura spp. 1 x 1011

Euphausiid juveniles 2 x 1011 Pleuromamma gracilis 1 x t 011 Other Pleuromamma spp. 1.5 x 10 il Lucicutia spp. 3.2 x 101~ He terorhabdus spp. 2 x 101 o Unidentified small copepodites 3 X 10 9

a Sources for TMSL values are Batchelder and Swift (1989), Buskey and Swift (1990), Lapota et al. (1988), and Batchelder (un- published observations)


(measured as the total output of photons flash- 1) in contributing to the observed diel signal in FD, flash sizes were classified into three categories: dim flashes producing < 7 x 10 s photons flash-1, intermediate flashes producing > 7 x 108 but < 7 x 101~ photons flash - i , and bright flashes producing > 7 x 1 0 1 ~ photons flash -1. These flash size categories were chosen, as they roughly correspond to the trophic categories of autotrophs, microheterotrophs, and macroheterotrophs, respectively (Table 3). As Table 2 shows, the daytime reduction in FD was greatest for the smallest size flashes and least for the brightest flashes. The 0 to 150 m integrated daytime reduction in FD as a function of flash size was significant for each flash size category and for each day-night comparison (paired t-test; p < 0.002), although the daytime decrease was much greater overall and for each size class individually on 25 August than on 23 August.

Bioluminescence measurements - dusk

FD and BPOT increased during sunset in all five time series, although there was high variability among the time series in the details of the changes (Fig. 2). In two cases (18 May 1987, 23 March 1988) the BPOT increase was gradual and nearly continuous, while in three instances (22 May 1987, 25 August 1987, 2 April 1988) there appeared to be short term pulses of high BPOT, almost as if there were a passage of migrating bioluminescent organisms through the sampled depth stratum. Generally, FD and BPOT did not increase in parallel throughout the time series, which may be caused by a few bright flashes contributing heavily to BPOT, while incrementing FD only slightly. The period when FD and BPOT increased most rapidly on 22 May (Fig. 2 B) was ca. 1 h later, and at lower light intensity, than on 18 May (Fig. 2 A).

Profiles in BPOT and FD were measured at midnight and midday preceding the 25 August time series measurements (Fig. 1 B). Comparing the data taken at 70 m at sundown on 25 August with that obtained at midday and midnight at the same depth, suggests that ca. 50% of the day-to-night increase in BPOT and one third of the day- to-night increase in FD occurred during the 2 h dusk measurements at sunset. F D increased from ca. 250 flashes m -3 to a peak of 660 flashes m -3 at 19:51 hrs local, then gradually declined over the next hour to ca. 450 flashes m-a ; this compares to 131 flashes m -3 at 7 0 m during midday (50 to 9 0 m range of 130 to 280 flashes m-3) , and 1 345 flashes m-3 at 70 m at midnight (50 to 90 m range of 800 to 1 400 flashes m-3). BPOT during the 2 h sampling period at dusk increased from 0.7 x 1013 to 8.2 x 1013 photons m -3. Midday and midnight BPOT at 70 m were 1.2 x 1013 photons m -3 (50 to 9 0 m range of 0.8 to 6.5x1013 p h o t o n s m -3) and 16.6x 1013 photons m -3 (50 to 9 0 m range of 10 to 26 x 1013 photons m-3) , respectively. This suggests that the remaining day-to-night increase in BPOT in August occurred later (i.e., when it was darker) than the period in which we sampled. The data for May 1987 and M a r c h - April 1988 are less complete, but comparisons of the final BPOT and FD estimates from the dusk time-series with

H.P. Batchelder et 21.: Sargasso Sea planktonic bioluminescence 333

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Fig. 3. Mean (_+95% confidence interval) hourly change in flash density (FD) for small flashes (< 7 x l0 s photons flash- 1) (left bar), intermediate flashes (7 to 700 x i0 s photons flash-1) (center bar), and large flashes (> 7 x 10 l~ photons flash-1) during the five dusk time series. ND indicates no data for the smallest flashes in May 1987

midnight measures of BPOT and FD at 70 m (Figs. 4, 5 and 7 of Batchelder et al. 1990) suggest that more of the nightly increase was completed by the end of the dusk period (range of 60 to 125% of change complete by time of last dusk sample) compared to August 1987.

Linear regression analysis of the dusk time series FD using individual flash size categories (< 7 x l0 s photons flash -1, > 7 x 1 0 s but < 7 x 1 0 1 ~ photons flash -1 > 7 x 101~ photons flash- 1) did not indicate significant trends common to all cruises and/or replicates. Many of the confidence intervals for the hourly change in FD for most sized flashes encompassed zero, primarily due to large short-term (< 0.5 h) temporal variability in the FD estimates (Fig. 3). However, FD of both intermediate and large-sized flashes increased significantly during dusk in the March and April 1988 series. For these time series, intermediate-sized flashes increased most rapidly as night progressed (300 to 400 flashes m- 3 h- 1). Densi- ty of the smallest flashes either remained constant or decreased slightly during dusk in March and April.

Depth dependent K4s 8 (attenuation coefficient at 488 nm) obtained from MER-1010 casts during the prior or succeeding day were used to estimate dusk changes in light intensity at 70 m (ETom) from light intensity recorded at the surface during the period of most rapid BPOT and FD increase. On 18 May 1987, BPOT increased most rapidly at 20:00hrs when Evom=l.6• 1012 photons cm -2 s- t. On 2 April 1988, BPOT increased by 50% and FD tripled from 17:50 to 18:50 hrs. During that time E7o m decreased from 2.4x ]014 to 2.7x 1011 photons

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Fig. 4. Bioluminescence potential estimated from organism abundances in bathyphotometer net samples and taxon specific per capita TMSL (total mechanically stimulable light) for dusk time series at 70 to 75 m on (A) 18 May, (B) 22 May, (C) 25 August 1987, (D) 23 March, and (E) 2 April 1988. Note scale change in C and E. Local time in hrs

cm -2 s-1. On 23 March 1988, first FD and then slightly later BPOT increased over a more extended time interval while E7o m decreased from 1.6 x 1015 to 3.8 x 10 9 photons c m - 2 s- 1.

Time series bathyphotometer samples

Organisms known or presumed to be bioluminescent (Table 3) were enumerated from the bathyphotometer net samples. The abundance of each taxon was multiplied by an estimated per capita stimulable bioluminescence to predict BPOT (Batchelder and Swift 1989). Organisms were classified as autotrophs, microheterotrophs, or macrozooplankton, and the amount of light produced was summed by trophic type (Fig. 4). Overall, organism abundance in the bathyphotometer nets would predict less than 10% (7.2+1.4%; mean+_SE for all dusk samples from all cruises; n=40 ; range of 0.5 to 51%) of the BPOT estimated from direct in situ bathyphotometer measurements. That calculation, plus the absence of sig-

nificant trends in the abundances or predicted BPOT for any of the bioluminescent taxa (or trophic groups) paral- leling those seen in FD and BPOT, suggest that the net sampling system on the bathyphotometer was not quanti- tative. The data suggest that vertical displacements of the sampling gear due to ship motion caused sloshing of the sample within the nets and loss of organisms through extrusion, disintegration, and leakage. Attempts to re- duce these losses were not successful. I f we consider the data from the bathyphotometer net samples to indicate the presence of common bioluminescent taxa, then we observe that except for several samples that had the large, bright dinoflagellate, Pyrocystis noetiluea, autotrophs contributed little to the total light budget. Based on this assumption, microheterotrophs, especially Protoperi- dinium spp., produced much of the bioluminescent light throughout the dusk period, except in August when there may have been a consistent and significant contribution to the light budget by macrozooplankton. Because of the limitations mentioned and the large temporal variability within a single time series, we do not generalize temporal trends from this data set.


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Net plankton abundance and estimated bioluminescence

Bioluminescent plankton were enumerated from five (four night/one day) MOCNESS deployments in both May and August 1987 (Table 1). Numerically important bioluminescent groups were the copepods, euphausiids, Iarvaceans, ostracods, Pyrocystis dinoflagellates, siphonophores, and tomopterid polychaetes. Only the bioluminescent copepods and larvaceans were identified to species. Bioluminescent copepods encountered included PIeuromarnrna gracilis, P. xiphias, P. abdominalis, Luci- cutia flavicornis, and Heterorhabdus spinifrons.

Except for seasonal near-surface warming in May, temperature and fluorescence profiles from MOCNESS sampling nights within a cruise (May and August) were similar, suggesting that the zooplankton tows were rea- sonable replicates from a single water mass. A 3-way analysis of variance for unbalanced data (SAS Inst. 1988) on log-transformed abundances revealed that all three of the Pleuromamma spp. exhibited significant diel vertical migration, but that none of the other bioluminescent groups had consistent and robust vertical migration pat-

terns. Migration in the three species of Pleuromamma would affect the vertical distribution and intensity of bioluminescence over the diel cycle. The vertical distributions of Pleuromamma spp. within the upper 200 m in paired day/night samples (separated by <13 h) are shown in Fig. 5.

Estimates of bioluminescence potential for each bioluminescent taxon collected by MOCNESS were obtained as described by Batchelder and Swift (1989). Simply, organism abundance is multiplied by its per capita total mechanically stimulable light production (see Table 2 of Batchelder and Swift 1989). Since bioluminescent flashing by Pyroeystis dinoflagellates is photoinhibited (Ham- man et al. 1981), their contribution was assumed to be insignificant during the day. Calculated bioluminescence potential integrated over the interval 0 to 150 m at night ranged from 4.2 to 14.0x 1014 photons m -2 (Fig. 6). Daytime values were 38 and 40% of mean nighttime values in May and August, respectively. Pyrocystis spp., copepods, and ostracods were approximately equally important (24 to 34% of total apiece) as mesoplankton light producers at night in both May and August.

336

Twilight net plankton abundances

Our investigations of plankton migratory activities at dawn and dusk were only partially successful. In May 1987 we obtained four samples from 90 to 100 m span- ning 0.75 h slightly after sunset. Pleuromamma xiphias were not present at 90 to 100 m prior to 20:20 hrs, whereas P. gracilis abundance increased by an order of magnitude (from ca. 100 to 1400 per 100 m 3) during this 0.75 h interval. P. abdominalis abundance increased 3-fold. None of the other taxa showed trends in abundance during this sampling period.

In August 1987 we repeatedly and consistently sampled at 75 to 85m (Dawn Tow E2Moc5, Table 1) throughout an extended period (> 2 h) during twilight. Light intensity at 80m and bioluminescent meso- zooplankton abundances from that MOCNESS time se-

-~ 0 4~ ~ 12 6 O 'E 10

~, p= s

E ~ 4 -

m

Pyrocystis

[ ~ Ostracod Larvacean Euphausiid Copepod

0 T l i l 'H I . . . . . . . . . . . . . . ~ . . . . . . . . . . . . . . . . . ~ . . . . . . . . . . . . . . . . ; . . . . . . . . . . . . . . . . : . . . . . . . . . . . . . . . . . . . . . . . . . . . , " : .

ElM1 ElM2 ElM4 ElM8 ElM9 E2M2 E2M3 E2M4 E2M7 E2M8 E2M6 1 May/Night [ ~1, [ --Aug/Night I ~

May/Day Aug/Day

Fig. 6. Depth integrated (0 to 150 m) bioIuminescence potential estimated from organism abundances in MOCNESS net samples and taxon specific per capita TMSL (total mechanically stimulable light). The light budget is partitioned by producing organism, zooplankton taxa (ostracods, larvaceans, euphausiids, copepods) and the large bioluminescent dinoflagellate, Pyroeystis noctiluea


ries at dawn are shown in Fig. 7. The next to last sample had consistently low abundances of all bioluminescent taxa, which may reflect patchiness, or possibly an error in correcting abundances for the volume of water filtered. Clearly, the abundances of Pleuromamma gracilis and P. abdominalis declined during the sampling period. We assume that this temporal decline indicates their departure from the surface layer.

Discussion

During the transition from daylight to darkness, two phe- nomena occur in near-surface Sargasso Sea waters that influence the amount of bioluminescence of those waters. The first is the release from high light photoinhibition of their bioluminescence capacity in the autotrophic (and possibly heterotrophic) dinoflagellates. In laboratory populations, flash intensity in many bioluminescent autotrophic dinoflagellates, such as in several Gonyaulax and Pyrocystis spp. is inhibited by high light intensity (Sweeney et al. 1959, Biggley et al. 1969, Esaias et al. 1973, Hamman et al. 1981). Similar photoinhibitory effects have been demonstrated for heterogeneous field populations of dinoflagellates, including Ceratium fusus and numerous species of Peridinium (Filimonov and Sadovskaya 1986). In those experiments, dark adapted cells lost 50 to 75% of their bioluminescence potential within 2 to i0 min. Photoinhibition was also related to light intensity, with higher light levels producing greater and more rapid photoinhibition. Recovery of phytoplankton bioluminescence following the onset of darkness was somewhat slower than the onset of photoinhibition; recovery to full light output took ca. 30 min (Sadovskaya and Filimonov 1985). Thus, the rapid changes of ca. two orders of magnitude in downwelling light intensity occurring during 30 min near dawn and dusk might be expected to lead to rapid changes in the photoinhibitory state of individual cells within the mixed layer.

16 800 �9 o~ [ Light at 80 [ ~oE 14 m / / ~

12 400 "6 (9 8 ' ~ j 0 ~ O 350 40

d I I Siphonophores z o ~ / Pyrocystis ~ 2500 1 70001

1250 3500

O/ / 0 I loooo00oo I 0442 0630

�9 P a

. . . . .

~Polychaete I1~176176 lil ~ P xiphias [5ooi

0 "

I 900 i Lucicutia 100

0 0

Local Time

Fig. 7. Downwelling light intensity at 80 m estimated from measured surface light intensity attenuated to depth (upper left panel) and abundance of various plankton taxa at 75 to 85 m during a time series of MOCNESS net samples at dawn on 24 August 1987. P. grac.: Pleuromamma gracilis, P. abd.: P. abdominalis, Euph: Euphausiid spp. Time in hrs

H.P. Batchelder et al.: Sargasso Sea planktonic bioluminescence 337

The second phenomenon occurring at dusk which af- fects the vertical distribution (and indirectly, the intensity) of bioluminescent flashes is vertical migration of bioluminescent zooplankton to surface waters from the greater depths they inhabit during the day. Many species of copepods, euphausiids, and ostracods, including some which are bioluminescent, undertake diel vertical migration (Roe 1972a, Roe 1972b, Angel 1979, Roe 1984, Roe etal. 1984, Ambler and Miller 1987). Migration of zooplankton, since they are relatively bright flashers, could potentially alter both the number of flashes and the mean intensity or the flash intensity distribution in near- surface waters at night.

In our studies in the Sargasso Sea there were significant diel changes in the number of flashes, the number of bioluminescent organisms (due to vertical migration), and the depth distribution of bioluminescent organisms and flashes. We observed a significantly (2 to 5 x ) higher flash density at night as compared to daytime in paired day and night vertical profiles in August 1987. There was a corresponding, but less marked (2 to 3 x ) increase in BPOT. However, the mean light output per flash (photons flash -1) did not differ between day [10.9 to 14.5 x 101~ (CV= _+40%)] and night [9.5 to 11.3 x 101~ (CV = _+ 30%)] profiles, nor was there a statistically significant (Chi-square test) difference day to night in the frequency distribution of photons produced per flash. The number of flashes of all intensities (brightness as photons per flash) increased at night.

The amplitude of the diurnal cycle of bioluminescence potential we observed in the Sargasso Sea (2 to 3 x ) is less than has been reported for some other regions. Biolu- minescence at night increased by 1 000 x in Great Harbor, Woods Hole, Massachusetts (Backus et al. 1961), by ca. 15 x in the northwestern Atlantic (Yentsch et al. 1964), by 40 to 70 x in the California Current (Greenblatt et al. 1984), and by approximately 30 x in the Oyashio subarc- tic current (Utyushev et al. 1984), compared to at midday. It is also somewhat less than has been observed previously in the Sargasso Sea (Lapota and Losee 1981, Neidhardt 1989).

Our observations of the percentage of the day-to- night increase in BPOT and FD occurring during two hours at dusk yielded variable results. Our data from August, which are most complete, indicate that ca. 34 and 50% of the day-to-night increase in FD and BPOT, respectively, occurred during the time when sunlight intensity decreases most rapidly. Conversely, more of the day-to- night increases in March-May appeared to occur during this interval; in one case all of the nightly increase appar- ently occurred between two samples. FD and BPOT increases during dusk, if caused by the liberation of di- noflageUates from photoinhibition, should be relatively monotonic (see for example Hamman et al. 1981) and once increased should remain high if variations due to patchiness in numbers of types of bioluminescent organisms is minimal. BPOT and FD changes caused by migrating zooplankton, on the other hand, may create inter- mittent increases and decreases in time series observations of BPOT and FD: increases as they first arrive to the sampled depth, and decreases if they continue to migrate

to even shallower depths. As in the midday to midnight comparison, the dusk series of samples provided no evidence for a change in the mean flash photon output or in the frequency distribution of flash photon output (Chi- squared test).

From May and August MOCNESS samples we calculated a nighttime mesoplankton contribution of 4 to 14 x 1014 photons m -2 integrated over the upper 150 m of the water column. This compares to 0-150 m integrated estimates of 80 to 120 x 1014 photons m -2 from nighttime bathyphotometer profiles in August and to the 90 140x 1014 photons m -2 (seasonally invariant) reported earlier for the Sargasso Sea (Batchelder et al. 1990). Given the likelihood that the/n situ bathyphotometer and the MOCNESS (nets) are sampling two almost non-overlapping suites of bioluminescent taxa (Batchelder and Swift 1989), a better estimate of total BPOT due to large and small, motile and non-motile, and abundant and scarce types, might be made by summing together the estimates from the direct and indirect methods taking into consideration the possibility that Pyro- cyst& spp. might be adequately sampled by both tech- niques. The conclusion emerging from this exercise is that photoinhibition played a more important role than vertical migration in creating the diel pattern of bioluminescence that we observed in the Sargasso Sea. Evidence supporting this conclusion is of two types. First, while the day/night comparisons of both the in situ bathyphotometer data and the MOCNESS-derived light budget indicate roughly comparable percentage declines (40 to 65%) in bioluminescence potential during the daytime, the decline measured by the bathyphotometer, because of its order of magnitude greater bioluminescence during day

Day to Night BPOT Change (1013photons ~3 )

-10 -5 0 5 10 15 20 0

25 FDBp':, J /

50 \ " ' " \ " ,

s 75 FO~oo !

100

.<L.. ,

125 ;i Y 1'

150 ; o 40o 80o 12oo

Day to Night FD Change (flashes m "3)

Fig. 8. Net increases (nighttime minus daytime values) in bathyphotometer estimated bioluminescence potential (BPOTap, continuous line) and flash density (FDBp , dashed line), and in MOCNESS light budged bioluminescence potential (BPOTuoc, solid line) and bioluminescent organism abundance (FDMoc, dashed line), from August 1987

338

and night , overwhe lms the day /n igh t change seen in the M O C N E S S l ight budge t (Fig. 8). Since the b a t h y p h o t o - mete r ra re ly cap tures s t rongly mot i le p l ank ton , it is l ikely tha t few ver t ical m ig ra to r s are represen ted in the ba thy- p h o t o m e t e r signals.

Second, the increase in b io luminescence at n ight due to large o rgan i sms , no t all o f which mig ra t e diel ly, can be at mos t only 1 4 x 1014 p h o t o n s m -2 when in teg ra ted over the uppe r 150 m (light budge t es t imate f rom M O C - N E S S o rgan i sm abundances ) . This represents less than 15% o f the to ta l ( M O C N E S S es t ima ted plus b a t h y p h o - tometer ) BPOT (ca. 94 to 134 x 1014 p h o t o n s m -1) over tha t d e p t h in terval . I f all o f the b io luminescen t z o o p l a n k - ton c a p t u r e d in the n igh t t ime M O C N E S S samples va- ca ted the u p p e r 150 m dur ing the day , then BPOT w o u l d decrease by 15% at most ; in fact , the d a y t i m e r educ t ion in measu red BPOT rela t ive to n ight t ime is much grea ter (33 to 65% lower in day than at night) . Thus, while we have cer ta in ly no t answered all the ques t ions a b o u t the mechan i sms respons ib le for the genera l ly h igher b io luminescence in surface waters du r ing the n ight t han in the day , our results for the no r the rn Sargasso Sea s t rong ly suggest tha t p h o t o i n h i b i t i o n o f b io luminescen t f lashing in the d inof lagel la tes dur ing the day is the p r inc ipa l m e c h a n i s m respons ib le for the diel pa t t e rn in b io luminescence.

Acknowledgements. The authors thank the captains and crews of the R. V. "Endeavor" and USNS "Bartlett" on which these data were collected, C. Mann and J. Sullivan for assistance at sea, J. Sullivan, D. Van Keuren, and S. Northby for sample processing, Dr. M. J. Perry for providing a LICOR PAR continuous integrator in May 1987, and Dr. D. Ondercin of the Applied Physics Lab of Johns Hopkins University for inviting us to participate in the March- April 1988 cruise. This work was supported by Office of Naval Research Contracts N00014-89-J-1455 (HPB) and N00014-81-C- 0062 (ES). This is contribution number 049 of the ONR sponsored BIOWATT program.

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diel patterns of planktonic bioluminescence in the northern sargasso sea

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