Particulate carbohydrate fluxes in the Bransfield Strait and the Drake Passage

Marine Chemistry, 20 (1987) 255-264

255

Elsevmr Scmnce Pubhshers B.V., Amsterdam --- Printed m T h e Netherlands

P A R T I C U L A T E C A R B O H Y D R A T E F L U X E S IN THE B R A N S F I E L D S T R A I T A N D THE D R A K E P A S S A G E

GERD LIEBEZEIT*

Instttut fur Meereskunde, Dusternbrooker Weg, 2300 Ktel (F R G) (Received M a r c h 3, 1986; revision accepted August 29, 1986)

ABSTRACT Lmbezelt, G , 1987 Particulate carbohydrate fluxes m the Bransfield Strait and the Drake Passage Mar. Chem., 20: 255-264.

Carbohydrate fluxes were determined for five drafting sediment traps ( m a x 30 h) m the Bransfield Strait and one moored trap array (52 days) m the Drake Passage m December/January 1980 In a Phaeocyst,s-dominated zone m the Bransfield Strait the carbohydrate composition was comp a r a b l e to that of water column suspended material with absolute fluxes of 9.0 and 56 7 m g carbohydrate carbon m -2d 1 In Bransfield Strait waters dominated by b a c l l l a r l o p h y c e a e , fluxes were 75 4, 92.6 a n d 276 8 m g carbohydrate carbon m 2 d i w i t h a p r o n o u n c e d d o m i n a n c e of glucose T h i s is attributed to the presence of the reserve p o l y s a c c h a r l d e c h r y s o l a m m a r m m diatom resting spores Drake Passage fluxes were 1 2 orders of magmtude lower w i t h a distract degradation of glucose with depth INTRODUCTION

Large, rapidly settling particles dominate the downward flux of particulate matter in the marine environment (e.g. Honjo, 1980). The organic carbon fr~ctlon of this flux constitutes both labile and refractory compounds which undergo various rearrangement and degradation processes during vertical transport. Whereas a number of reports have appeared on the composition and fate of lipids and amino acids (Lee and Cronin, 1984; Wakeham et al., 1984; Liebezeit, 1985), carbohydrates have received considerably less attention. Wefer et al. (1982) reported total sugar fluxes in the Drake Passage using depth series traps. Here, a pronounced decrease was found from the surface to 965 m water depth. Towards 2540m, no further decrease was observed. Ittekkot et al. (1984a, b) employed time and depth series traps in the Panama Basin and the Sargasso Sea, respectively. In addition to decreases in total fluxes with depth, strong seasonality was found. In the present communication, carbohydrate flux data are presented for five drifting sediment traps deployed in the upper 100 m of the Bransfield Strait and *Present address" Geologmch-Palaontologlsches Instltut, Bundesstrasse 55, 2000 H a m b u r g 13, FRG

0304-4203/87/$03.50

~ 1987 Elsevmr Science Pubhshers B V

256 compared to results from a moored trap array in the Drake Passage. The results are examined in the light of a hypothesis on diatom survival strategies recently put forward by Smetacek (1985). MATERIALAND METHODS Drifting sediment traps (TR 2 6 ) were deployed during crmse 56, leg Ant I of R/V "Meteor" in December 1980 in the Bransfield Strait (Fig. 1) A detailed description of the trap design has been given by Zeitzschel et al. (1978). Background data pertinent to the present experiments are given in Table I. The moored sediment trap array (M 269) was deployed from 2 December 1980 to 25 J a n u a r y 1981 at 60°54.6'S and 57°06.0'W at 3625m water depth close to station 86 (Fig. 1). TR 2 6 samples were homogenised after retrieval m filter-sterilised seawater and ahquots filtered through precombusted (450°C, overmght) GF/C filters. These were stored deep-frozen until final analysis. M 269 samples were split, desalted by repeated washing with distilled water and lyophilised. Samples were hydrolysed with 2 N HC1 at ll0°C for 3 h under nitrogen. After desalting by membrane ion-exchange electrodialysis and lyophilisation in the presence of glycerol, the residue was taken up in 20% aqueous ethanol and an aliquot subjected to automated borate anion exchange chromatography. Details of the chromatographic system have been given by Dawson and Liebezelt (1983). Partmulate organic carbon and phytoplankton data are from Von Bodungen et al. (1986) or from B. von Bodungen (personal commumcation, 1985). RESULTS AND DISCUSSION

Bransfield Strait The hydrographical and biological background mformatmn for the time of trap deployment has been given by Haardt and Maassen (1983), Tilzer et al. (1985) and Von Bodungen et al. (1986). Briefly, three different zones can be dmtinguished in the investigation area (Fig. 1) of which only zones II and III are of interest in the present study. Zone II was hydrographically complex and is thus further subdivided into IIa and IIb. The former was dominated by Phaeocystis and the bacillariophyceae Thallassiosira and Corethron with generally high chlorophyll contents in the surface layers. Zone IIb was somewhat poorer in phytoplankton with a lesser importance of Phaeocystis. Zone III phytoplankton was dominated almost entirely by diatoms (mainly Thallasswsira. but also Biddulphia and Chaetoceros) and showed more homogeneous chlorophyll depth distributions with lower concentrations than zone II. Microscopic examination of trapped particulate matter (Von Bodungen et al., 1986) showed t h a t intact diatoms were dominant in traps 4-6 and also contributed to traps 2 and 3. In the latter two, however, faeces of Euphasia

257 TABLE I Background data for sediment traps m the Bransfield Strait and the Drake Passage Trap

Deployment

2 3 4 5 6 M269 M269

Euphot~c zone

time

depth

depth a

(h)

(m)

(m)

30 17 24 7 10 1248 1248

100 100 100 100 75 965 2540

20 25 100 > 175 > 125 100c 100c

r/b

3 4 2 4 3 1 1

a From a t t e n u a t i o n profiles of Haardt and Maassen (1983) h Number of rephcates analysed c Station 86 (Fig 1)

58 °

56 °

•86 - 61 °

I ELEPHANT ~SLAND

. . . . . . . . .

I_' ""

/ / 62 ° •

I,

o68

coXXi&x'~ 4>@ ~ 9.2

-62 °

7 ~

Z O N E Ha

/I / .23 / o24 o126 / [ o25 /~2v / - "?-3~;77-~l~3ZONE ] T b . - ~ / • * //

L i

I

BRANSFiELD~STRAIT

1

3

-/

102oo107 o33

i /

~.,~

,vv~

ZO N~E m °

~7 -L.O ° 2 8 - 63 °

53 o -

0 580

56 °

Fig 1 Drifting sediment trap locations (v) m the Bransfield Strait m December 1980. Moored trap array (M 269) was deployed close to station 86

superba h a d

the highest contribution to total mass flux. Phytoplankton carbon contributions t o t o t a l c a r b o n f l u x w e r e 23 a n d 4 % f o r t r a p s 2 a n d 3 a n d 47, 6 0 and 48% for traps 4-6, respectively. These values are probably underestimates b y a f a c t o r o f 2 ( V o n B o d u n g e n e t al., 1986).

258

Thalassiosira sp., the dominant phytoplankter in all traps, was present mainly (approx. 65%) in the form of resting spores, tightly packed in large gelatinous clumps of 5(~150 frustules. The presence of a large contribution of 60-100pm sand grains in traps 4 and 6 indicates strong vertical mixing. Absolute fluxes were lowest in trap 2 and increased considerably in zone III (Fig. 2). Generally, a high degree of homogeneity m all parameters measured was found in traps 4-6, quite oppos]te to traps 2 and 3 (Von Bodungen et al., 1986). This is also evident for the carbohydrate composition and absolute fluxes (Fig. 2). In zone III traps, glucose is clearly the dominant sugar with contributions to the total flux well over 80%. In zone II, glucose accounted for 31.5 and 12.2% of the carbohydrate flux only. At stn. 137 (Fig. 1), which was also dominated by Phaeocyst~s, the relative glucose content decreased from 55.8% at the surface to 18.2% at 100 m. Since grazing by krill, i.e. transformation of phytoplankton into faecal material, does not change the relative carbohydrate composition (Tanoue et al., 1982) the spectrum of carbohydrates incorporated into krill faecal pellets and subsequently caught in the sediment traps of zone II will be dependent on feeding depth. In zone III, on the other hand, both absolute and relative carbohydrate fluxes

,o~o,o1°~: d~

2

,oo.

.

,oo%

~-~-,5ol

.ooli o llO0

1

,o

3

~I '°~I

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ill 5o

6

I ZOO

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5

lO0

F]g. 2 Total carbohydrate fluxes and contmbutlons of l n d w l d u a l compounds for traps 2 ~ Bars give m e a n values and r a n g e Note the l o g a m t h m m scale

259 show considerable differences to suspended particulate matter. Whereas in the latter case glucose accounted for 57.3 + 10.0% of total carbohydrates (n 14, Liebezelt, 1984) the corresponding figure for traps 3-6 is 86.0 _+ 5.2% (n 9, Fig. 2). Similarly, total sugar contributions to the orgamc carbon pool are 6.1 + 1.9 and 17.6 _+ 4.0%, respectively. Grazing by k n l l leads to an increase m the relative carbohydrate content at the expense of liplds and proteins (Tanoue et al., 1982). This was, however, not pronounced in zone III (Schnack et al., 1984), which is also supported by the virtual absence of faecal materml in traps 4-6 (Von Bodungen et a l , 1986) Furthermore, amino acids maintain their relative contributions to the orgamc carbon pool both in suspended and sediment trap material (Liebezeit, 1985: Liebeze~t and Bolter, 1986). Hence other processes must be responmble for the observed differences in carbohydrate composition between suspended and sinkmg material in zone III. These can be linked to the dominance of bacillariophycean aggregates with a large proportion of resting spores found m traps 4-6 Due to the small samples available for chemical analysis, an attempt to correlate the high relative glucose contents with individual constituents of the cellular carbohydrate pool can be made only indirectly. Carbohydrates are deposited after silica deposition and serve as a buffer zone between cell and environment (Hecky et al., 1973). This role may be fulfilled with the onset of aggregate formation and mucilage production. The similarity of cell wall and mucilage carbohydrates (O'Colla, 1962; Hecky et al., 1973) indicates that formation of the latter might be achmved by rumply extending the outer cell coating. The question does, however, remain why the sugars making up the mucilage such as xylose, mannose, fucose or galactose are not found m any large quantities in the sediment trap samples. The answer to th~s presumably hes m the sample pretreatment (homogenisation and vacuum filtration) which would tend to destroy such fragile structures. Ittekkot et al. (1984a) report that approximately 18% of total sugars and amino acids are found in the supernatant after centmfugation. This fraction is hkely to be demved from externally attached mucilagenous polymers. Thus, the carbohydrates found in traps 4-6 do not originate from external polysacchandes. Diatom cell walls contain a wide variety of carbohydrates (e.g. Parsons et al., 1961; Hecky et al., 1973; Ittekkot et al., 1982). In addition, fractionatlon of" carbohydrates originating both from laboratory cultures and natural plankton populations dominated by bacillariophyceae into either water or weak acidsoluble reserve polysacchandes and a residual fraction (e.g. Handa and Yanagi, 1969; Haug et al., 1973) showed the latter fraction to consist of various monosaccharides. In no case reported so far has the overwhelming dominance of glucose as found m traps 4-6 been linked to diatom cell-wall polymers. During the fractionation schemes mentioned above, glucose was found m considerable quantities m the water/weak acid extracts. Thus, the dominance of glucose in traps 4 4 .can be hnked to reserve polysacchamdes. The polymer in question is most likely chrysolaminarm, the common carbohydrate storage product of bacillariophyceae (Meeuse, 1962; Handa, 1969). The presence of such large amounts of reserve polymers must also be connec-

260

ted with the fact that the majority of trapped diatom cells contained resting spores (Von Bodungen et al., 1986). It can therefore be assumed that these compounds are of survival value. A successful adaptation to the survival strategy outhned by Smetacek (1985) requires the seeding population to remain m a water mass favourable for later return. According to the above-mentioned hypothesis this is achmved through heterotrophic degradation of mucilage and dissolution of the parent frustule. Since both processes are externally controlled, under unfavourable conditions this strategy might not be successful. Incorporation of an internal control mechamsm such as degradation of reserve polymers wall certainly enhance spore survival chances. This means that resting spores are not m a state, of complete anablosis but maintain at least a reduced metabolism. This ~s supported by the findings of French and Hargraves (1980) who showed that diatom spores can be photosynthetically active. Based on the foregoing discussion the hypothesm is put forward that the production of large amounts of polysaccharides accompanying spore formation and aggregation serves a threefold purpose: (i) the presence of increased amounts of glucose increases the specific weight and hence accelerates stoking, (ii) if the glucan in question is present m the form of a reserve polymer, this might serve as an energy store and hence prolong survival time, and (iii) degradation of this reserve polysacchamde leads to a decrease m specific weight and facilitates return to favourable growth conditions. With the presently available data this hypothesis cannot be extended further and more work is needed to establish the role of chemical compounds in spore formation and survival strategies of Bacillariophyceae.

Drake Passage During the time of trap deployment in December 1980, dinoflagellates dominated the phytoplankton in zone I (Von Bodungen et al., 1986). In J a n u a r y 1981, at the time of trap retrieval, bacdlariophyceae were dominant as is evident from the high biogenic opal contents (> 75%) in the surface and trap samples (Wefer et al., 1982). Microscopic examination also revealed a high content of diatom frustules. Thus, the flagellate population found m December 1980 (Von Bodungen et al., 1986) apparently did not reach the depth of the sediment traps. Total carbohydrate fluxes were 2.6mg m 2d ' at the surface decreasing to 1.1 and 1.2mgm 2d ' at 965 and 2540m, respectively. These figures are considerably lower than zone III fluxes which might be accounted for by the lower pmmary productivity of this region (Von Bodungen et al., 1986) and the high copepod grazing pressure (Schnack et al., 1984). Relative contributions of carbohydrates to total fluxes are 2.9% at the surface increasing to 8.7 and 11.1% with depth. This indicates that other constituents of the organic carbon pool, preferentially nitrogen- and phosphorus-containing substances, are degraded at a much faster rate than car-

261

bohydrates during vertical transport (Wefer et al., 1982). Compared to zone III samples, the relative contmbution of the surface carbohydrate samples to the suspended organic carbon pool is considerably lower (Fig. 4). Again, this might be an effect of sample pretreatment as discussed above. Differences also exist in the relative composition of the surface sample from M 269 and those from the euphotic zone of zone III. In the latter case, glucose was found with 57.3 + 10.0% (Liebezelt, 1984) whereas in the Drake Passage it accounted for 16.3% of the carbohydrate fraction (Fig. 3A). Here fucose was the dominant sugar (35 tool%). Both compounds are prominent in baclllariophyceae: glucose as reserve polymer and cell wall constituent and fucose in the cell walls of some species (Parsons et al., 1961; Hecky et a l , 1973; Ittekkot et al., 1982). The decrease in glucose from 16.3% at the surface to less than 5% with depth indicates that this sugar is predominantly present in an easily degradable form, i.e. as a reserve polymer. Increases of galactose, xylose, arabinose and rhamnose, on the other hand, point to their incorporation into structural compounds (Fig. 3). Although commonly associated with the latter group, fucose shows a m g C m "2 d "~ 3

tj /.0 °k

A

I~-

20

R

F' 2O

0

0

Fig. 3 Total carbohydrate carbon fluxes and contmbutlons of individual sugars for moored sediment trap M 269. Total flux data from Wefer et al (1982) (A) Surface, (B) 965 m, (C) 2540m

262

S

E w u

o o

t~

u_

°/0

rl~ or"

20. S o

(22)

w

.il S

u

u_

:;?.

<°.: •.°

i

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1

i , ° .°• .

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q o

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}

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:.

::...~ .:.:

.

i

•.'i': X"

0

,'.7°

Fig 4. Relative contrzbutlons of carbohydrates to the total particulate o r g a m c carbon pools (M 56 surface) and fluxes (M 269, T R 2 ~ ) m the Bransfield Strait and Drake P a s s a g e D a t a for M 56 are from Llebezelt (1984) For station l o c a t i o n see Fig 1

b e h a v l o u r similar to glucose• Since mucilage will have been removed during sample pretreatment as discussed above, this effect is presumably due to differences in reserve/structural polymer carbohydrates of different diatom specms present in zones I and UI. The observed differences between sediment trap samples from M 269 and zone III can be explained by two mechanisms: (i) the bacillariophyceae follow different survival strategies; and (n) resting spores with a high reserve polysaccharide c o n t e n t do not reach the depth of trap deployment at site M 269. Since data for shallower traps at this szte are not avadable, no clear-cut decision can be made b e t w e e n these two possibihties. CONCLUSIONS

The results presented above demonstrate that chemical analysis provides a means by w h i c h biological observations can be explained and amended on a

263 molecular

basis. They

also point

to our profound

lack

of knowledge

on the

processes involved in diatom spore formation on a cellular level. Thus, more detailed work is necessary to elucidate the role of lipids, carbohydrates, amino acids and other

cellular

constituents

in dmtom

survival

strategies.

ACKNOWLEDGEMENTS The author is indebted to V. Smetacek and B. von Bodungen for supplying the samples and for many valuable discussions. The expert technical assistance of ~Frltz" Bohde is gratefully acknowledged. This work was supported financially by the Deutsche Forschungsgememschaft through the former Sonderforschungsbereich

95 a t K m l U n i v e r s i t y .

REFERENCES Dawson, R and Lmbezelt, G , 1983 Determination of amino acids carbohydrates In K Grasshoff, K Kremhng and M E h r h a r d t (Editors), Methods of Seawater Analysis 2nd edn, Verlag Chemm, Wemhelm, pp 319-340 French, F W and Hargraves, P E , 1980 Physiological characteristics of plankton diatom resting spores Mar Biol. L e t t , 1 185-195 Haardt, H and Maassen, R , 1983 CTD and optmal data from the Antarctic, Meteor 56 Ant I, Part I, CTD and chlorophyll profiles. Rep Sonderforschungsberemh 95, No 57 1 183 Handa, N , 1969 Carbohydrate metabohsm of the marine diatom Skeletonema cobtatum Mar Blol, 4 208 214 Handa, N and Yanagl, K , 1969 Studms on water extractable carbohydrates of the particulate matter from the northwest Pacffic Ocean Mar Blol, 4 197 207 Haug, A , Myklestad, S and Sakshaug, E , 1973 Studms on the phytoplankton ecology of the Trondhelmsfjord I The chemmal composition o f p h y t o p l a n k t o n populations J Exp Mar Blol E c o l , l l 15 26 Hecky, R E , Mopper, K , Kllham, P and Degens, E.T, 1973 The amino acid and sugar compos~tmn of diatom cell-walls Mar Blol, 19 323 331 Honjo, S , 1980 Material flux and modes of sedimentation m the mesopelaglc and bathypelag~c zones J Mar Res., 38 53-97 Ittekkot, V , Degens, E T and Brockmann, U , 1982 Monosaccharlde composition of acld-hydrolyzable carbohydrates m partmulate matter during a plankton bloom Llmnol Oceanogr, 27 77{~776 Ittekkot, V , Deuser, W.G and Degens, E T , 1984a Seasonahty m the fluxes of sugars, amino acids, and amino sugars to the deep ocean Sargasso Sea Deep-Sea Res, 31 1057 1069 Ittekkot, V , Degens, E T and Honjo, S, 1984b Seasonahty m the fluxes of sugars, amino acids, and amino sugars to the deep ocean P a n a m a Basra Deep-Sea Res, 31 1071 1083 Lee, C and Cromm C , 1984 P a r t m u l a t e amino acids m the sea effects of primary productlwty and bmloglcal decomposltmn J. Mar Res, 42 1075-1097 Lmbezelt, G , 1984 Particulate carbohydrates m r e l a t m n to phytoplankton m the euphotm zone of the Bransfield Strmt. Polar B m l , 2 225 228 Lmbezelt, G , 1985 Residual amino amd fluxes m the upper water column of the Bransfield S t r m t Oceanol. Acta, 8 59~5. Lmbezelt, G and Bolter, M , 1986 Dlstrlbutmn of particulate amino acids m the Bransfield Strait Polar B m l , 5 199-206 Meeuse, B J D 1962 Storage products In R A. Lewm (Editor), Physmlogy and Bmchemlstry of Algae Academic Press, London, pp 289-313 O'Colla, P S , 1962 Mumlage In" R A Lewm (Editor), Physmlogy and Bmchemlstry of Algae Academic Press, London, pp 337-356

264 Parsons. T R , Stephens, K. and Strlckland, J.D H , 1961 On the chemical composition of eleven species of phytoplankters J Fish Res Board C a n , 18" 1001-1015 Schnack, S B., Smetacek, V , Von Bodungen, B. and Stegmann, P , 1984 Utlhzatlon of phytoplankton by copepods m Antarctic waters during spring In J.S Gray and E Chrlstlansen (Editors), Marine Biology of Polar Regions and Effects of Stress on Marine Orgamsms. Wiley, Chmhester, pp 6~81 Smetacek, V , 1985 Role of stoking m diatom hfe-hlstory cycles ecologmal, evolutionary and geological slgmficance Mar Blol, 84 239-251 Tanoue, E , Handa, N. and Sakugawa, H , 1982 Difference of the chemical composition of orgamc matter between fecal pellet of Euphasza superba and its feed, Dunahella tertmlecta Trans Tokyo U m v F m h , 5 189-196 Tllzer, M M., Von Bodungen, B and Smetacek, V , 1985 Light dependence of phytoplankton photosynthesis m the A n t a r c t m Ocean. lmphcatlons for regulating photosynthesis In R Smgfrmd, P F Condy and R S Laws (Editors), A n t a r c t m Nutrient Cycles and Food Webs Springer, Heidelberg, pp 60-69 Von Bodungen, B , Smetacek, V S , Tflzer, M M and Zeltzschel, B , 1986 Primary productmn and sedlmentatmn during austral spring m the Antarctic penmsual region Deep-Sea Res, 33 177 194 Wakeham, S G , Lee, C , Farrmgton, J W and Gagoslan, R B . 1984 Bmgeochemlstry ofpartmu[ate orgamc matter m the oceans results from sediment trap experiments Deep-Sea Res, 31 509 528 Wefer, G., Suess, E , Balzer, W., Llebezelt, G , Muller, P . J , Ungerer, C A and Zenk, W , 1982 Fluxes of bmgemc compounds from sediment trap deployment m circumpolar waters of the Drake Passage Nature (London), 299 14~147 Ze~tzscheL B , Uhlmann, L and Dlekmann, P., 1978 A new multi-sample sediment trap Mar B~ol, 45 28~288