The biomass of the deep-sea benthopelagic plankton

Deep-Sea Research,Vol. 27A, pp. 203 to 216 Pergamon Press Ltd 1980. Printed in Great Britain

0011 7471/80/0401-0203 $02.00/0

The biomass of the deep-sea benthopelagic plankton K. F. WISHNER* (Received 2 July 1979; in revised form 6 December 1979: accepted 12 December 1979)

Abstract--Deep-sea benthopelagic plankton samples were collected with a specially designed opening closing net system 10 to I00 m above the bottom in five different oceanic regions at depths from 1000 to 4700 m. Benthopelagic plankton biomasses decrease exponentially with depth. At 1000 m the biomass is about I% that of the surface zooplankton, at 5000 m about 0.1~o. Effects of differences in surface primary productivity on deep-sea plankton biomass are much less than the effect of depth and are detectable only in a few comparisons of extreme oceanic regions. The biomass at 10 m above the bottom is greater than that at 100 m above the bottom (in a three-sample comparison), which could be a consequence of an enriched near-bottom environment. The deep-sea plankton biomass in the Red Sea is anomalously low. This may be due to increased decomposition rates in the warm (22' Ct deep Red Sea water, which prevent much detritus from reaching the deep sea. A model of organic carbon utilization in the benthic boundary layer (bottom 100 m), incorporating results from deep-sea sediment trap and respiration studies, indicates that the benthopelagic plankton use only a small amount of the organic carbon flux. A large fraction of the flux is unaccounted for by present estimates of benthic and benthopelagic respiration.

INTRODUCTION THE QUANTITYOr life in the sea has been s t u d i e d since the earliest d a y s o f o c e a n o g r a p h y . Yet the a m o u n t o r b i o m a s s of p l a n k t o n t h r o u g h o u t the w a t e r c o l u m n r e m a i n s p o o r l y k n o w n , especially in the d e e p sea. The s t a n d i n g stock of o r g a n i s m s at all d e p t h s m u s t be d e t e r m i n e d before an a c c u r a t e analysis o f the cycling o f m a t t e r a n d energy between the surface a n d the b o t t o m can be m a d e . Relatively little w o r k has been d o n e on the b i o m a s s o f deep-sea (below 1000 m) p l a n k t o n because o f the difficulty of collecting samples. A b u n d a n c e s are low a n d closing nets m u s t be used to a v o i d c o n t a m i n a t i o n by near-surface o r g a n i s m s . LEAVITT (1938), GRICE a n d HULSEMANN (1965, 1967), VINOGRADOV (1968), a n d DEEVEY a n d BROOKS (1971) have r e p o r t e d on b i o m a s s e s o f p l a n k t o n s a m p l e s o b t a i n e d with closing nets b e l o w 1000 m. M o s t o t h e r p u b l i s h e d w o r k on d e e p - s e a p l a n k t o n is p r i m a r i l y t a x o n o m i c in n a t u r e a n d does n o t even c o n s i d e r the entire sample. T h e present s t u d y is the first q u a n t i t a t i v e investigation of the deep-sea (1000 to 4700 m) p l a n k t o n living j u s t a b o v e the b o t t o m (10 to 100 m). The n e a r - b o t t o m or b e n t h o p e l a g i c fauna, a link between the b e n t h o s a n d the w a t e r c o l u m n , m a y q u a n t i t a t i v e l y as well as q u a l i t a t i v e l y differ from the rest o f the d e e p - s e a p l a n k t o n a n d m a y be i m p o r t a n t in biological i n t e r a c t i o n s within the b e n t h i c b o u n d a r y layer. These a n i m a l s , because of their p r o x i m i t y to the b o t t o m , i n h a b i t a m o r e h e t e r o g e n e o u s a n d p o s s i b l y richer e n v i r o n m e n t t h a n d e e p p l a n k t o n higher in the w a t e r c o l u m n . M o r e niches m a y be a v a i l a b l e , a n d a specialized b e n t h o p e l a g i c fauna p r o b a b l y exists a l o n g with the r e g u l a r deep-sea * Scripps Institution of Oceanography, La Jolla, CA 92093, U.S.A. 203

204

K. F, WISHNER

zooplankton. GRICEand HULSEMANN(1970) and GRICE (1972), using opening closing nets on the submersible Alvin, found endemic copepods living 20 to 50 cm above the bottom at 1000 to 2000 m, but they did not report biomasses. METHODS

Transects were sampled with a specially designed opening-closing net device attached to the Scripps Institution of Oceanography Marine Physical Laboratory's Deep Tow instrument (Fig. 1). The Deep Tow system has been used for many near-bottom geological and geophysical surveys and routinely collects much information on the physical environment (SPIESSand TYCE, 1973). Its location in the water column, both horizontally and vertically, is continuously known within a few meters by the use of an acoustical transponder navigation network and up- and down-looking sonars. With this system, long horizontal transects close to the bottom of the deep ocean were possible. Two versions of the net system were used during the study. An early model, used on the Cocotow and Natow expeditions (Table 1), was a single net with a rectangular mouth opening 0.38 × 0.39 m (0.15 m2). A later model, used on the other cruises, had three nets. The first and third nets had mouth openings of 0.30 × 0.44 m (0.14 m2); the middle had a Table 1. Deep-sea benthopelagic stations. The underlined letters in the names are initials used to refi?r to the station. Tow depths are rounded to the nearest hundred meters. Abbreviations: ETP, eastern tropical Pac!fic : NEA, northeast Atlantic: EP, eastern Pacific, EqP, equatorial Pacific: RS, Red Sea

Name Sand _Dune _Valley E c u a d o r Trench _Maury _Channel -i-i _Maury _Channel Revisited _Rockall T r o u g h Irish Shelf San _Diego T_ r o u g h III 1 _ ,, III 3 IV-3 -station _2'_0 III 1 III 2 III 3 IV~ 1 _Station _2! V-2 ,, V3 Red Sea South 2 _ _ 3 _Suak]'n _Deep 1 ,, 2 3 _Atlantis -i| Deep 1 . 2 3 _Valdivia _Deep 1 ,, 2 ,, 3

Cruise

Date

Cocotow 3 Cocotow 3 Natow 2 Natow 3 ,,

28 29/10/74 3/11/74 26/'7/75 18/8/75 28 29/8/75

0°33'S 0°18'S 56°19'N 56°19'N 56°16'N

Mel 1 " 7 ~ S C

221,/4/76 3/9/75 21/4/76 21/4/76 3/9,/76 3/9/76 3/9/76 4/9/76 12/9/76

54D21'N 32'33'N 32"33'N 32°32'N 11 °04'N 1 l°05'N 11 °03'N 1 l°03'N 4°01'N

85'33'W 81°08'W 23°42'W 24°29'W 12'~29'W 1TI9'W I17'33'W 117°34'W 117°31'W 140°02'W 140°02'W 140°00'W 140'~02'W 136°01'W

12 13/9/76 14,,'6/78 14/6/78 21/6/78 21/6/78 21/6/78 23/6/78 23 24/6/78 24/6/78 24/6/78 24~25/6/78 25/6/78

4°01'N 1T~28'N 17°24'N 19c37'N 19°40'N 19°41'N 21°23'N 21°19'N 21°21'N 21~21'N 21 ~20'N 21°21'N

135°57'W 40° 15'E 40° 10'E 38°45'E 38°44'E 38 43'E 38 03'E 38°06'E 38°06'E 37°58'E 37°58'E 3T 58'E

,, Pleiades 4

,, Indomed 9 ,, ,, ,, ,, ,, ,, ,, ,, ,, ,,

Lat.

Long.

Ocean region

T o w depth (m)

ETP

2700-2900 2400 3000 2600 3200 2900 3200 2400 2500 1800 2900 1100 a 1200 b 1100 a 4600 4700 4700 4700 4600 4700 4200 4300

NEA ,, ,, EP ,, Eq'P ,, ,, ,, ,, RS ,, ,. ,, ,, ,, ,, ,, ,,

a Entire tow taken at 100 m a b . b Entire tow taken at 10 mab. All other tows included entire interval from 10 to 100 mab.

4200~,300 800 1100 800 1100 2400 2400 2600 2 2 0 0 2600 1800 1700 1800 1700 1800 1200 1300 1100- 1200 1100 1300

Fig. 1.

Photograph of the net system attached to the Deep Tow instrument. All three nets are closed.

[facing p. 204]

205

The b i o m a s s o f the deep-sea b e n t h o p e l a g i c p l a n k t o n

140 °

I00 °

60 °

20 °

0o

20 °

60 °

60 °

40 °

40 °

20 °

20*

0°

0 °

20'

20*

140 °

Fig. 2.

I00 °

60"

20'

0°

20 °

L o c a t i o n s where deep-sea b e n t h o p e l a g i c s a m p l e s were taken. L o c a t i o n s are identified by initials (Table 1).

mouth opening of 0.30 x 0.39 m (0.12 m2). All nets were 1.3 m long, constructed of 183-~tm mesh nylon and fitted with a 0.1-m dia PVC cod end. An outer net of nylon webbing protected the three collecting nets from abrasion. The net frame was attached to skids below the Deep Tow instrument so that the net mouths were unobstructed. The nets were opened and closed by falling horizontal weighted bars, whose release was triggered remotely by electronic command from shipboard through a coaxial cable connected to the Deep Tow instrument. In the multiple net model, closing one net opened the following one. Transects were made from 10 to 100 m above the bottom (abbreviated 'mab') at depths from about 1000 to 4700 m (Table 1). In the San Diego Trough several transects were taken entirely at either i0 or 100 mab. Five different oceanic regions of the world were sampled (Fig. 2). Tows used for biomass estimates lasted 2.3 to 21.8 h and covered 6.6 to 60.6 km (Table 2). Towing speed averaged 1.5 kt (46 m m i n - 1). Plankton samples were preserved in 6~o buffered formalin in filtered seawater immediately after return to the surface. Samples from tows shorter than 120 min were not used for the biomass analysis. The short tows gave highly variable results, which may be a gear artifact or a consequence of patchiness. Longer tows appeared to integrate these small scale effects and therefore permitted the study of large scale geographical and depth patterns of biomass. Other tows were not used because it appeared that excessive towing speed or fast vertical changes had severely damaged the samples. Contamination from shallower water plankton as the net was lowered and raised was negligible, because nets that remained closed during a complete transect contained only an

206

K . F . WISHNER

occasional individual. Some small shallow-water copepods were sometimes present in the samples, probably from having been forced directly through the mesh of the cloth, but their biomass was insignificant. Biomass was determined by wet weight because the sample volumes were too small for accurate volumetric analysis. A container was made from a plastic 35-mm film canister with the bottom cut out and a hole 2.8 cm dia cut in the lid. A piece of net material was attached to the top of the canister by the remainder of the lid. When turned upside down, the canister formed a small lightweight filter and sample holder. The sample was placed in the pre-weighed container, blotted through the netting until slightly damp, and weighed on a Troemer two-pan balance to the nearest 0.01 g. Large animals were removed before weighing, but no attempt was made to sort out detritus, foraminiferan tests, or other nonliving entities. The sample weight was calculated by difference. Sample data and biomasses are presented in Table 2. The volume of water filtered was calculated as (net mouth area) × (tow distance). Tow distance was computed as (average tow speed) × (tow duration). The tow distance calculation agreed well with actual tow

Table 2.

Tow data, biomasses, and surfitee data Jbr each sample

Vol.

Sample SDV ET M C II MCR RT IS S D T III 1 IIl 3 IV 3 Sta. 20 l I I 1 III 2 III 3 IV 1 Sta. 21 V 2 V 3 RSS 2 3 SD 1 2 3 A II 1 2 3 VD 1 2 3

Duration (min)

Distance"

filtered

Wet wt.

(km)

(m 3)

(g)

775 530 1037 245 1309 605 210 221 135 202 383 195 180 209 224 143 142 194 260 156 258 239 506 183 514 210

35.9 24.5 48.0 11.3 60.6 28.0 11.0 10.9 7.9 9.4 17.7 9.0 8.3 9.7 10.4 6.6 6.6 9.0 12.0 7.2 11.9 11.1 23.4 8.5 23.8 9.7

5300 3620 7090 1670 8940 4130 1490 1480 1070 1270 2090 1220 1130 1140 1410 780 890 1220 1420 980 1620 1310 3170 1150 2810 1320

4.94 3.63 3.03 0.72 7.28 2.74 1.91 4.10 1.83 0.13 0.28 0.21 0.15 0.17 0.18 1.00 0.77 0.04 0.31 0.08 0.06 0.11 0.24 0.14 0.35 0.04

Surface Deep-sea biomass biomass as Biomass [cm3(1000m) 3 % surface [g(1000m) -3] or g(1000 m t 3] biomass 0.93 1.00 0.43 0.43 0.81 0.66 1.28 2.77 1.71 0.10 0.13 0.17 0.13 0.15 0.13 1.28 0.86 0.03 0.22 0.08 0.04 0.08 0.08 0.12 0.12 0.03

100 b 200 b 100 c 100 c 100 c 100 c 200 I" 200 b 200 b 75 b 75 b 75 b 75 b 38 b 38 b 250 d 250 d 100 e 100 ~ 100 • 100 e 100 c 100 ° 100 c 100 e 100 ¢

0.93 0.50 0.43 0.43 0.81 0.66 0.64 1.39 0.86 0.13 0.17 0.23 0.17 0.39 0.34 0.51 0.34 0.03 0.22 0.08 0.04 0.08 0.08 0.12 0.12 0.03

Speed assumed to be 46 m min 1 except for S D T I I I - 1 (52 m min 1 ), S D T III 3 (49 m m i n - 1 }, a n d S D T IV 3 (59 m rain 1). b F r o m REID (1962). Closest isopleth value used or, if equidistant from two isopleths, average used. c F r o m Bfset at. (1971). d F r o m PONOMAREVA (1968). • F r o m GORDEYEVA (1970).

207

The biomass of the deep-sea benthopelagic plankton

distances measured from charts of the Deep Tow tracks for several areas. The water filtration efficiency of the nets was assumed to be 100%, because in all areas except the eastern tropical Pacific the nets returned to the surface with no evidence of clogging. This gives a minimum (i.e. conservative) biomass estimate.

RESULTS

Biomass Benthopelagic biomass (Table 2) decreases exponentially with depth for depths greater than 1000 m. When the log10 biomass is plotted against depth (Fig. 3), a significant least squares regression can be fitted to the points (P < 0.001 that the slope = 0). The line is described by the equation: logt0 biomass (g 1000 m - 3 ) = 0.694-0.00034 × depth (m). The mid-point of the depth range of each transect is used in the graph and regression. The Red Sea data are not included in the regression calculation and are also treated separately in the other analyses reported. The Red Sea has unusual hydrographic conditions (see Discussion), and deep-sea biomasses there are anomalously low (Table 2).

Comparison with surface Table 2 shows the benthopelagic biomasses as percentages of the average surface zooplankton biomasses in the same general location. Values for the surface were obtained from REID (1962, Pacific), PONOMAREVA(1968, Red Sea), GORDEYEVA (1970, Red Sea), and I0-X REDSEA • OTHERAREAS \~SOT

~[-3

xx

I

E

SDT "r~- 3 ~ x , . x RSS 2 ~ X ~ ~'"x SDT 3,1T_1J'~ ~ . ~ x . ~ .

I

RSS3j~x

T _i¢~"E

--..~-sov

0

~'-..

3 0 m

~ ~'~

-,,'~..y

xx

0.1

95"1o CL

954. c~'-.e" ~ X

"N

X X

0

I

I000

X

I

2000

i

3000

I

4000

i

5000

DEPTH(m)

Fig. 3. Linearregression of deep-sea benthopelagic biomass as a function of depth. The biomass is plotted on a logarithmic scale. The solid line fits the equation: Ioglo biomass [g(1000 m) -3] = 0.694 - 0.00034 depth (m). The dotted lines are the 95% confidencelimits of the regression. The Red Sea samples (marked by X's) were not included in the regression calculation for reasons mentioned in the text. Initials identifying the samples are given in Table 1.

208

K . F . WISHNER

1.5 F SOT1Tr-3• X RED SEA • OTHER AREAS

O X

IO0:/I

SOT

"fl;:r-~e

0

d~ gg o~-

•

.\ .ss

•

""

.ss

:xx I

•

×x

x x x

tO00

\

I

I

I

I

2000

3000

4000

5000

DEPTH(m)

Fig. 4. "Simple linear regression' of the per cent ratio of the deep-sea benthopelagic biomass to the surface biomass as a function of depth. The Red Sea samples (marked by X's) were not included in the regression calculation for reasons mentioned in the text. Initials identifying samples are given in Table 1.

BL FORNS and ROELS (1971, Atlantic). The studies involved different kinds of nets, mesh sizes, towing methods, and depths so comparisons are only approximate. The percentages (Table 2) are plotted vs depth in Fig. 4 and a significant 'simple linear regression' line (TATE and CLELLAND, 1957) was fitted to the points (excluding Red Sea data) (P < 0.001 that the slope = 0). The negative slope (Fig. 4) shows that, as the depth increases, the relative biomasses decrease. At 1000 m the benthopelagic plankton biomass is about 1~/o of the surface zooplankton, at 5000 m about 0.1~o. The amount of zooplankton decreases most rapidly in the upper water column (by two orders of magnitude in the first 1000 m) and at a slower rate in deeper water (by another order of magnitude from 1000 to 5000 m). DISCUSSION

Biomass and depth The exponential decrease of biomass with depth found in the benthopelagic plankton agrees with deep-sea plankton abundances reported by GRICEand HULSEMANN(1965, 1967) and VINOG~ADOV(1968). Deep-sea plankton biomasses from these authors and the present study are plotted vs depth in Fig. 5. Values for GRtCE and HULSEMANN'S(1965, 1967) samples were determined from their graphs of displacement volume by assuming a conversion factor of I g c m - 3. The other deep-sea plankton studies involved vertical tows, and the depth value in Fig. 5 is the midpoint of the tow. At any one depth, a wide range (1½ to more than 2 orders of magnitude) of biomasses is reported. However, when linear regressions are calculated separately for each author and

209

The biomass of the deep-sea benthopelagic plankton

I00-

iooB

A

!

I0

.

2<

'E 0 0 0

03 co

o 00 OI

*

-+-

- GH( I )

*

x% -~o "~--.~Y

o~

• V(NWP)

~V(I) + V(EqP) oB I I000

I 2000

/ 5000

I 4000

] 5000

0

I I000

I 2000

I 5000

I 4000

I 5000

DEPTH (m)

Fig. 5. Deep-sea plankton biomasses from the literature and this study plotted as a function of depth. The biomasses are plotted on a logarithmic scale. The Red Sea data are not included. Abbreviations: GH(NEA), GRICE and HULSEMANN (1965), northeast Atlantic; GH(I), GRICE and HULSEMANN (1967), Indian ; V(NWP), V]NOGRADOV (1968), northwest Pacific; V(I), VINOGRADOV (1968), Indian; V(EqP), VINOGRADOV (1968), equatorial Pacific; B, benthopelagic. A. Biomasses of individual samples versus depth and linear regressions, calculated separately for each study, of biomass as a function of depth. B. Envelopes of biomasses vs depth from each study. Each envelope includes all the points from a particular study.

sample series (Fig. 5), the resulting slopes are similar (Table 3). There is no difference between the slopes (regression coefficients) of the lines (P > 0.25 that the slopes are equal), except for the GRICE and HULSEMANN (1967) Indian Ocean series, which is significantly different (P < 0.05 that the slopes are equal) from the rest as a group (a posteriori tests for differences among regression coefficients, SOKAL and ROHLF, 1969). This implies that similar processes may be occurring in the water column throughout many of the world's oceans and that the initial input of organic material from primary production at the surface may be utilized in the deep sea at similar efficiencies in different Table 3. Linear regression coefficients for biomass as a function o f depth for each study in Fig. 5 (same abbreviations as Fig. 5). The coefficients fit the equation: logto biomass = log a + ( b ) ( l o g e ) X where biomass is in units o f g(1000 m)- 3 and X is the depth in m. The regression coefficient = (b)(log e); the y-intercept = log a. The equivalent exponential equation is: biomass = a ebx

Study B GH (NEA) GH (I) V (I) V (NWP) V (EqP)

Regression coefficient - 0.00034 -0.00047 -0.00017 -0.00046 -0.00047 -0.00035

95% confidence limits of regression coefficient - 0.00041 -0.00064 -0.00030 -0.00061 -0.00059 -0.00059

- 0.00027 -0.00030 -0.00004 -0.00031 -0.00035 - 0.00011

Y-intercept 0.694 1.361 0.764 0.796 2.065 0.298

210

K.F. WISHNER

oceans. The significant regression of relative biomasses with depth (Fig. 4), consistent over several different regions, also supports this hypothesis. The same kinds of animal groups occur in deep-sea plankton samples from different areas (WIsHNER, 1979); feeding interactions and energy use could also be broadly similar. Only temperate and tropical regions have been sampled to any extent at depth, however, and these relationships might not apply to subarctic, polar, or semi-enclosed seas. The positions with respect to the biomass axis of five of the six regression lines (Fig. 5) are significantly different from each other. The five pairs of adjacent regression lines were tested by an analysis ofcovariance for equality of position. In all but one pair, the two lines showed a significant position difference (P < 0.05 after correcting for multiple testing, benthopelagic and Vinogradov Indian Ocean NS). This large variation in absolute biomasses at any one depth has been attributed to differences in surface productivity (V1NO~RADOV, 1968). However, as discussed later, surface productivity has minimal effects on deep plankton biomasses. The variation is more likely caused by different gear, mesh sizes, and sampling methods used in the different studies. GRICE and HULSEMANN(1965, 1967) and VINOGRADOV(1968) used short (mostly 1 to 2 km) vertical tows with closing nets. The present study used long horizontal transects with an opening-closing net. These transects were hours and kilometers greater (Table 2) than previous deep plankton tows, which might reduce the effect of patchiness on biomass estimates by integrating areas of high and low concentration. This appears to be the case, because the 95~o confidence limits of the regression in Fig. 3 are remarkably small (indicating low variability) considering the number of oceanic regions sampled. Biomasses of deep-sea benthic animals also decrease exponentially with depth (ROWE, 197! ; ROWE,POLLONIand HORNER,1974), and the regression coefficients for the plankton and benthos are very similar. The plankton coefficients range from -0.00017 to -0.00047 (Table 3); the benthic ones from -0.00027 to -0.00054 (Rowe et al., 1974). This implies that the same controlling factors, presumably aspects of the food supply (ROWE et al., 1974), may determine the biomass of both the plankton and benthos. Relationship to primary productivity One would expect deep-sea plankton biomasses to reflect regional surface primary productivity levels, because these represent possible input of food. To test this hypothesis, biomass values from the studies in Fig. 5 (excluding the Red Sea) were sorted into groups, each composed of values for a single 1000-m depth interval from a single study. The biomasses were grouped by depth because of the significant regression of biomass and depth, and each study was treated separately because of the significant differences in position between regression lines (Fig. 5). These biomass values were then assigned to one of three surface primary productivity levels based on their geographical location: (1) < 1 0 0 m g C m - 2 d a y -1, (2) 100 to 2 5 0 m g C m - E d a y -1, and (3) > 250 mg C m -2 day -1. Primary production values were obtained from YENTSCH and WOOD (1960) [cited in HALIM (1969)], KOBLENTZ-MISHKE,VOLKOVINSKYand KABANOVA (1970), FAO (1972) map of phytoplankton production, OWEN (1974), and LOVEand ALLEN (1975). A one-tailed, single classification analysis of variance (SOKALand ROHLE, 1969) was performed on the logxo biomass values within each of the 11 suitable groups of samples (groups of values from the same study and within a single depth interval and including areas of different surface productivity) to test whether areas with lower surface productivity

The biomass of the deep-sea benthopelagic plankton

21 1

had smaller deep-sea plankton biomasses than did areas with higher surface productivity. None of the tests was significant (P > 0.1 for each group that means of different productivity levels were equal). A few individual points did support the hypothesis, however. The two biomass estimates in the present study from the eastern tropical Pacific (Ecuador Trench and Sand Dune Valley), an area of high primary productivity (LovE and ALLEN, 1975), were both above the 95~o confidence limits of the linear regression in Fig. 3. Except for this result, effects of surface productivity variations on deep-sea and benthopelagic plankton biomasses were not statistically detectable with the present data and were much smaller than the effect of depth on biomass. Differences in deep-sea benthic biomasses in different productivity regions of the world have been described by ROWE (1971) and ROWE et al. (1974). However, if their data are grouped by depth interval, assigned to a productivity level, and treated statistically like the plankton data, there is a significant difference between samples from different productivity regions only within the 2000- to 3000-m depth interval (Peru benthic biomasses were greater than northwest Atlantic ones). It is apparent that, except for comparison of extreme world regions, much of the effect of primary productivity differences on deep-sea plankton and benthic biomasses is masked by the variability of the samples. Too few replicate samples (same gear and methods) have been taken at similar depths in areas of different surface productivity to yield many statistically significant comparisons between areas. Primary productivity and benthic processes (as measured by sediment core oxygen uptake) are more closely linked in shallow aquatic ecosystems (HARGRAVE,1973). Near-bottom effect

The near-bottom region of the deep sea appears to be richer in organic material than the water column several hundred meters higher. Using deep-sea sediment traps on the northwest Atlantic continental rise (2800 m), GARDNER(1977) found evidence of sediment resuspension up to at least 100 mab and determined that organic carbon flux increased with closeness to the bottom from 500 to 13 mab. HOLM-HANSEN, STRICKLAND and

Table 4. Comparison of benthopelagic (bottom 100 m) and benthic biomasses. Biomasses being compared are from the same type of area but not the same location

Depth

Benthopelagic a biomass

Benthic b biomass

Benthic ¢ biomass

Benthic b

Benthic c

(m)

( g m -2)

(gin 2)

( g m -2)

Benthopelagic

Benthopelagic

0.043 d 0.013 B

0.653 ~ 0.159 h

0.81 f 0.219 i

15.2 12.2

18.8 16.9

2900 3000 4700 5100

" Calculated benthopelagic biomass in bottom 100 m (g m -3 × 100). b SMITH (1978). c ROWE et al. (1974). d Mean of two M a u r y Channel samples (both taken from 10 to 100 mab). " Station HH. f Mean of six Atlantic continental rise samples (Nos. 14-19). Mean of four Station 20 samples (all taken from 10 to 100 mab). h Mean of samples from Stations J J, K K , and N N . Mean of two Atlantic abyssal plain samples.

212

K.F. WISHNER

WILLIAMS(1966) found that dissolved organic phosphorus and nitrogen increased from 100 to l0 mab off southern California (1300 m), which suggests an increase in biological activity (decomposition or excretion) near the bottom. KARL,LAROCK,MORSEand STURGES (1976) found more ATP at 3 to 5 mab than at about 1000 mab in the abyssal (6000 m) Atlantic, which may indicate a larger microbial biomass close to the bottom. Also, as benthic macrofaunal biomass on the continental rise and abyssal plain (RowE et al., 1974: SMIXH, 1978) is 12 to 19 times the estimated benthopelagic plankton biomass in the bottom 100 m (Table 4), the benthos could be a relatively concentrated food source for the benthopelagic animals. If, as these studies suggest, the near-bottom region of the deep sea is a biologically enriched habitat, then the benthopelagic plankton biomasses should be greater close to the bottom than higher up. A trend in this direction is shown by the San Diego Trough samples; the biomass of the near-bottom (10 mab) transect (SDT III-3) is higher than that of the two 100mab transects (SDT III-1 and IV-3) (Table 1). However, a series of replicated horizontal tows at closely spaced intervals above the sea floor would be necessary to document this hypothesis. Red Sea

All of the Red Sea biomasses are below the lower 95~o confidence limits of the linear regression calculated with data from other locations (Fig. 3). These anomalously low biomasses of the deep zooplankton may be explained by the peculiar hydrography of the Red Sea. Unlike most oceanic regions, where water temperature decreases with increasing depth and is at most a few degrees above freezing at several thousand meters depth, the subsurface Red Sea water is isothermal and warm (22°C) from 200 m to the bottom (2800 m) (SIEDLER, 1969; MORCOS, 1970). At this temperature, nonliving organic material would be expected to decay rapidly. For example, HARDING(1973) found that copepods decomposed in only three days in 22°C water but took 11 days in 4°C water. HoNJo and ROMAN (1978) determined that the surface membrane of copepod fecal pellets degraded in 3 h in 20°C water but stayed intact up to 20 days at 5°C. In the Red Sea much of the organic debris from the surface might decompose too fast to reach the bottom and near-bottom water. The carcass of a surface copepod with a settling rate of 36 to 720 m day- 1 (SMAYDA, 1969 ; TURNER,1977) would travel 108 to 2200 m in the 3 days before having decomposed in the 22°C Red Sea water. A surface copepod's fecal pellet with a settling rate of 15 to 220 m day -1 (SMAYDA,1971; TURNER, 1977; HONJO and ROMAN,1978) would sink 2 to 28 m in the 3 h before the surface membrane disintegrated. These calculations suggest that much less food might reach the deep-sea animals in the Red Sea than in a typical oceanic region with cold deep water. This low food input could lead to the very low biomasses observed in the deep zooplankton community. Hot saline anoxic brines fill several deep basins in the floor of the Red Sea (DEGENSand Ross, 1969; BACKERand SCHOELL, 1972). Planktonic organisms, except some kinds of bacteria (TRI3PER, 1969), would probably not exist in such brines, although the interface between the brines and overlying seawater can be a region of high particle concentration (RYAN, THORNDIKE,EWING and Ross, 1969). Four of the nine northern Red Sea samples (two each from Valdivia Deep and Suakin Deep) did enter the brines and interface region (determined from temperature readings by the Deep Tow instrument) for several minutes during the several hour tow. However, there is no significant difference between the biomasses of these four samples and the five other northern Red Sea samples (t-test on

213

The biomass of the deep-sea benthopelagic plankton

IOglo biomasses, P > 0.1 that means are equal). Therefore, the extremely low biomass values encountered in the Red Sea are not artifacts of sampling the brine environment.

Organic carbon utilization The role of the benthopelagic plankton in the organic carbon cycle in the deep sea can be examined by using data from deep-sea sediment trap and benthic community respiration studies. SMITH (1978) measured the oxygen consumption and biomasses of the benthic communities (the small organisms in the sediment under a bell jar) at a number of deep-sea sites. By assuming that benthic oxygen consumption is proportional to biomass in areas of similar depth and physical properties (SMIXH, 1978) and that the benthopelagic plankton in those areas respire at the same rate per unit weight as the benthos, one can calculate hypothetical values for benthopelagic respiration with the equation: Benthopelagic respiration = (benthopelagic biomass) × (benthic respiration + benthic biomass). The assumption of equal respiration rates for the benthos and benthopelagic plankton at similar locations is legitimate (until actual measurements are made) because many of the physical conditions (e.g. temperature, pressure) and animal types (e.g. polychaetes, small crustaceans) (WISHNER,1979) are the same. The benthic and planktonic animals being compared are similar in size; large animals such as holothurians or fish were not included in the measurements used. The benthic and hypothetical benthopelagic respiration rates, in terms of carbon Table 5. Organic carbon utilization by the benthos and benthopelagic plankton in the benthic boundary layer region (bottom 100 m)

Depth (m)

Location

2800-..3000 Atlantic continental rise 4700 5500 Atlantic and Pacific abyssal plain

2800-3000 Atlantic continental rise 4700-5500 Atlantic and Pacific abyssal plain

Benthopelagic a biomass ( g m -2)

Benthic biomass ~> 297 ~m ( g m 2)

0.043 c

0.653 d

0.80 a

0.053

0.853

0.013r

0.142 g

0.08 g

0.007

0.087

Organic carbon flux (g C m - 2 y - 1)

% of flux respired by benthos

% of flux respired by benthopelagic plankton

Total % of flux respired

Remainder (%)

2.3'

35

2

37

63

0.45 h

18

2

20

80

Benthic respiration ( g C m 2y-1)

Benthopelagic b respiration Total (hypothesized) respiration ( g C m - 2 y 1) ( g C m 2y l t

a Calculated benthopelagic biomass in bottom 100 m (g m - 3 × 100). b Benthopelagic respiration = (benthopelagic biomass)× (benthic respiration-benthic biomass). c Mean of two Maury Channel samples. d SMITH (1978), Station HH. e GARDNER (1977), primary flux, Station K N 58-2. t Mean of four Station 20 samples. B SMITH (1978), Station MM. h HONJO (1978).

214

K . F . WISHNER

(respiratory quotient = 0.85, SMITH, 1974, 1978), are compared to vertical particulate organic carbon fluxes measured with deep-sea sediment traps 100 to 500 mab at comparable locations (GARDNER, 1977; HONJO, 1978) in Table 5. About 20 to 37~o of the organic carbon ftux may be respired, 2~o by the benthopelagic fauna and 18 to 35% by the benthos. As the primary (component from the surface) organic carbon flux at these depths represents 2 to 3~o of the surface primary production (GARDNER, 1977; HONJO, 1978), the benthopelagic plankton of the continental rise and abyssal plain may utilize about 0.04 to 0.06~o of the organic carbon fixed at the surface, the benthic community 0.4 to 1~o. The particulate organic carbon flux in the near-bottom deep-sea region is 43 to 64 times the amount of carbon that the benthopelagic plankton hypothetically use for respiration (Table 5). This apparent organic carbon excess is corroborated by deep-sea sediment trap contents, which include numerous biogenic particles (WIEBE, BOYD and WINGET, 1976; GARDNER, 1977; HONJO, 1978). Fecal pellets are one of the most abundant biogenic categories present in the traps (WlEBE et al., 1976; GARDNER, 1977; HONJO, 1978). 'Red' fecal pellets, the most abundant type, are low in organic carbon content and may in fact be produced by the benthopelagic plankton (HoNJO, 1978). 'Green' fecal pellets, however, contain a high percentage of organic carbon and plant cell remains and are apparently transported directly and rapidly from the surface (HONJO, 1978). This type of fecal pellet would seem to be a good source of food for deep plankton, and phytoplankton remains that could have come from such pellets have been found in the guts of deep-living copepods (HARDING, 1974). In view of their abundance in sediment traps, fecal pellets are incompletely scavenged from the water column. Although their flux may be relatively high, their actual abundance in the water column at any one time may be low. Many fecal pellets might not be caught in transit. The benthopelagic plankton seem able to catch and utilize only a fraction of the total organic carbon passing through their habitat; the benthic animals, given time, can utilize a greater portion of what arrives. However, a large percentage (63 to 80~o) of the organic carbon flux remains unaccounted for by these calculations (Table 5). This remainder may be used by the larger benthic m e g a f a u n a (GRASSLE, SANDERS, HESSLER, ROWE and McLELLAN, 1975), fast benthopelagic animals such as fish or amphipods that escape capture by nets (ISAACSand SCHWARTZLOSE, 1975) or small benthopelagic organisms such as bacteria. The organic carbon may cycle several times between the pelagic and benthic realms of the benthic boundary region before being used; GARDNER(1977) found that a large portion of the total near-bottom organic carbon flux consisted of resuspended material. Some of the organic carbon flux is eventually buried in the sediment, but at these depths that amount is small. For example, in an abyssal plain environment, assuming a sediment density of 2.3 gcm -3 (TUREKIAN, 1976), a sediment organic carbon content of 0.2550 (HESSLER and JUMARS, 1974), and a sedimentation rate of 1 mm (1000 y)-t (MENARD, 1964), only about 0.00575 g C m - 2 y - 1 (1.3~o of the organic carbon flux, 0.03 to 0.04~o of the surface primary production), is incorporated into the top 1 cm of sediment. More research is required to determine how the remaining organic carbon is used or whether the various types of measurements incorporated in these comparisons are themselves in error. Acknowledgements I would like to thank the many people who helped with the design, construction, and shipboard operation of the net system, in particular the members of the Deep Tow group of the Marine Physical Laboratory whose assistance made the sampling a success. I would also like to thank Dr FRED SPIESSfor ship

The biomass of the deep-sea benthopelagic plankton

215

time in the San Diego Trough and the chief scientists, captains, crews, and other shipmates for their help. JOHN McGOWAN, ROBERT HESSLER, MICHAEL MULLIN, ERIC SHULENBERGER, and VALER1E LOEB made many useful suggestions about the manuscript. This work was supported by ERDA (AEC) Contract E(04 3) 34 P.A. 213 7 and Office of Naval Research Contract ONR/USN N00014 75-C 0152.

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