Bulk-Phase Viscoelastic Properties of Seawater: Relationship with Plankton Components

Journal of Plankton Research Vol.17 no.12 pp.2251-2274. 1995

Bulk-phase viscoelastic properties of seawater: relationship with plankton components

Ian R.Jenkinson and Bopaiah A.Biddanda1 Agence de Conseil et de Recherche Ocianographiques, Lavergne, 19320 La Roche Canillac, France and 'University of Texas at Austin, Marine Science Institute, PO Box 1267, Port Aransas, TX 78373-1267, USA

Abstract The viscous and elastic moduli at different shear rates, together with various biological oceanographic properties, were determined in seawater from different hydrological layers in the southern North Sea in June. The biological oceanographic parameters included Phaeocystis and Noctiluca abundances, chlorophyll a level (Chi), bacteria. HNAN and aggregate volume fraction. The plankton was jointly dominated by Phaeocystis sp. and Noctiluca scintillans. Noctiluca abundance showed no correlation with any other biological or viscoelastic parameter, but Phaeocystis abundance correlated strongly. The other biological parameters correlated with Phaeocystis and with each other positively and mostly significantly. Overall, viscoelasticity correlated more strongly with Chi than with any other biological parameter. For non-microlayer samples, the excess complex (viscoelastic) modulus (jiPa) 1 1 J C*E = 2.0 x Chi - (Chi in mg m ). Viscous and elastic moduli also correlated closely with each other. For a given value of Chi. the microlayer samples were 6.5 or 14 times (depending on the estimation method) more viscoelastic than in bulk-phase samples. Viscoelasticity in samples of settled benthic 'fluff were lower even than bulk-phase samples, but this difference was not significant. Comparison with Mediter- ranean data on viscoelasticity (Jenkinson. Oceanol. Acta, 16,317-334.1993), using published values for phytoplankton biomass (Wiadnyana,/ Rech. Octanogr., 17,1-6,1992), suggests that the relationship between Chi (or phytoplankton biomass) and viscoelasticity might be general. This apparent biomod- lfication of the viscosity and elasticity of seawater is discussed in relation to its likely impact on turbulence and plankton ecology.

Introduction Some microbial cells, both algae and bacteria, produce copious mucus exopoly- mers (Fogg, 1991). Largely as a result, the sea is a solution of polymers, similar to those responsible for the surface rheological properties of the sea surface film (Kattner et al., 1985; Pogorzelski, 1994). Many anecdotal descriptions of the bulk- phase water during phytoplankton blooms (for references, see Jenkinson, 1986; Fonda Umani etal., 1992; Molin etal., 1992) have indicated changes in its rheological properties. The following examples illustrate striking reports of seawater thickening. Firstly, during a 'dinoflagellate' bloom on the French Cdte d'Azur, Dreyfuss (1962) remarked that sampling was difficult with small containers as the seawater resembled fresh white of egg. Secondly, Jenkinson (1989) has argued that small bubbles, previously observed stationary as if trapped in the water column during blooms of Gyrodinium cf. aureolum Hulburt off Ireland and Scotland, constitute evidence for a modification of seawater rheological properties. Thirdly, off the southwest coast of India, during flagellate blooms, the water was so gelatinous that it kept clay in suspension, prevented weighted fishing nets from sinking, made boats difficult to steer and slime clogged fishing nets so that they tore when attempts were made to recover them (Bhimachar and George, 1950). [Although Bhimachar and George considered that Noctiluca scintillans (Macartney) Ehren- berg produced this slime, Subrahmanyan (1954) later presented strong evidence © Oxford University Press 2251 I.RJenkinson and B.A.Biddanda that it had been secreted by the chloromonad flagellate Hornellia marina Subrah- manyan [syn. Chattonella marina (Subrahmanyan) Hara et Chihara; Imai et ai, 1989]. Dramatic manifestations of marine slime, thought to be associated with blooms, have also long been noticed in the northern Adriatic and, although sporadic, appear to be increasing in intensity and extent (Herndl et ai, 1992; Molin et ai, 1992). Off the Shetland Islands (Ewart, 1885), southwestern England (Boalch, 1984), as well as in the Adriatic and the Black Sea (Bodeanu, 1995), bloom-associated mucus events have been associated with mass mortalities of benthic organisms, with difficulty in fishingand/o r with a dislike of the water by holiday-makers. Viscosity is an input parameter in models of exchange dynamics at the surfaces of plankton, other suspended particles (Mitchell et ai, 1985; Csanady, 1986; Jen- kinson, 1986; Lazier and Mann, 1989) and in respiration and excretion in the gills of fish (Jenkinson, 1989,1993a). Phytoplankton produce polymeric substances which increase measured viscosity and elasticity (Jenkinson, 1986, 1993a; Ramus and Kenney, 1989), and damp turbulence at high shear rates (Hoyt and Soli, 1965; Hoyt, 1970; Ramus et ai, 1989). Smetacek and Pollehne (1986) proposed that mucus secretion plays fundamental rdles in the life cycles of phyto- and bac- terioplankton, while Pedros AH6 et ai (1989) suggested that changes to the viscosity of the medium by marine bacteria may be why they do not sink according to Stokes Law. Jenkinson and Wyatt (1992) provided a crude but quantitative framework, based on the Deborah number, within which effects of mucus on flow patterns can be considered. In particular, they suggested that turbulent and high-shear environments are likely to support communities primarily of 'nomads' (Goldman, 1984) and r-strategists. That K-strategists, on the other hand, would be favoured by more highly structured macro- and micro-environments, for instance, suggests evolutionary pressure on phytoplankton to modify flow fields. One way they do this (the evolutionary fitnessha s not been proved, but one might suspect it) is by positioning themselves so as differentially to heat and stratify the water (Grin- dley and Taylor, 1964; Lewis etai, 1983; Sathyendranath et ai, 1991). Another way is to invest energy and materials in extending cell surfaces (Frontier and Pichod- Viale, 1991), mucus polymers or fibres (Jenkinson and Wyatt, 1992; Wyatt et ai, 1993). Furthermore, Malej and Harris (1993) found that carbohydrates of high molecu- lar weight secreted by aggregate-forming diatoms from the Adriatic inhibit grazing by copepods. Part of this inhibition was mechanically mediated, and would thus reduce encounter rate and increase the energy used in swimming. Mucus aggregates represent 'turbulence-free zones' (Jenkinson etai, 1991) and, by enhancing microzones around phytoplankters, affect the oxidation state, distribution and flux of manganese and perhaps other materials (Lubbers et ai, 1990). Mucus can be directly exocytosed by phytoplankton (Chang, 1984), or small molecules secreted by phytoplankton can be polymerized by bacteria (Biddanda and Pomeroy, 1988; Brophy and Carlson, 1989). Organisms selectively disadvantaged by mucus, however, would do well to curdle it into lumps and to live in the surrounding New- tonian liquid (Jenkinson and Wyatt, 1992). By influencing processes such as the sinking of phytoplankton blooms (Smeta- cek and Pollehne, 1987), aggregation of particles (Biddanda and Pomeroy, 1988; 2252 Viscoetesilc properties and phytoplankton

Alldredge and Gotschalk, 1989), transfer of elements through the food chain (Decho, 1990) and sea-surface gas exchange (Goldman et al, 1988), polymeric gelling, adhesion and thickening modulate ocean production and global climate. This thickening of the sea affects and acts through both the bulk phase (Jenkinson and Wyatt, 1992; Jenkinson, 1993b) and the surface film (Goldman et al, 1988). The results of the rheological part of the present study are given by Jenkinson (1993b), as are the results of a similar, but purely rheological investigation in the Rade de Villefranche, Mediterranean Sea. He concluded that in both environments the seawater was a weak but lumpy gel. The lumps may consist of strong gel, not only in terms of yield strength, but also in terms of the definition (Ross-Murphy and Shatwell, 1993) whereby 'strong' gels deform more before yielding (i.e. show higher critical shear) than 'weak' gels. In marine organic aggregates, a positive relationship between yield strength and critical shear has also been found (Jenkin- son et al, 1991). In the present paper, the relationship between rheological properties and the abundance of pelagic micro-organisms during a 1988 spring phytoplankton bloom in the German Bight is described. Excess viscosity and elasticity were closely correlated with the amount of phytoplankton, particularly Phaeocystis, which was dominant in terms of organic carbon. Neither rheology nor any other measured property was correlated with the abundance of Noctiluca, which was subdominant. Published values for phytoplankton biomass in the Rade de Villefranche (Wiad- nyana, 1992) are then used to extend the relationship between viscoelasticity and phytoplankton to lower levels of biomass.

Study area Figure 1 shows the study area: three stations near Helgoland in the German Bight. The phytoplankton succession in the German Bight has been reviewed and discussed by Smetacek et al. (1992), Colijn (1992), Hickel et al. (1992) and Hesse et al. (1992). In this area, phytoplankton biomass has increased 4-fold over the past two decades (Gerlach, 1987), the increase being almost exclusively in the flagellate component. Here and in many other coastal waters worldwide, where similar increases have occurred, increased inputs of nitrogenous and phosphorous nutrients are often (Gerlach, 1987; Smayda, 1989; GESAMP, 1990; Smetacek et al, 1992), but not always (Anderson, 1989; Wyatt and Jenkinson, 1993), considered as the primary cause. The succession of Phaeocystis in the study area was described for the spring bloom during May 1989 and May 1991 by Riebesell (1993). He found that only a minor proportion of the Phaeocystis cell carbon became associated with aggregates in 1989, but that in 1991 half was so associated at depths of 5 and 10 m, but little in the bottom layer. Slimy surface water in the German Bight has been reported by Schaumann et al. (1988) during blooms of Noctiluca. The diatom, Coscinodiscus wailesii, whose slime is thick enough to tear fishing nets with its weight, has recently become a regular, dominant member of the spring phytoplankton in the German Bight 2253 LRJenkinson and B.A.BMdamla

Fig. 1. The study area, showing the three key stations selected for biological and Theological investigation.

(Smetacek et al., 1992). Foam, sufficiently stable to be deposited up to 1 m thick on German Bight beaches during blooms of Phaeocystis (Batje and Michaelis, 1986), further suggests the occurrence of abundant polymeric surfactants.

Selection of stations A preliminary survey of the study area was carried out on 7 June 1988, in which surface readings of temperature, salinity and chlorophyll fluorescence were logged. At several stations, temperature-salinity (TS) profiles were obtained using a pre-calibrated TS meter. For detailed investigation, we chose three stations (Fig- ure 1) which all had well-defined upper and lower mixed layers separated by a distinct pycnocline. The following day the three selected stations were revisited. At each station, after redetermination of the TS profile, samples were taken at five depths: the surface microlayer, the upper mixed layer, the pycnocline [at or near the depth of maximum change in density per unit depth, &a(S,t,d)], the lower mixed layer and the benthic microlayer.

Terminology Rheology is the science of the deformation of materials. In practice, the term is applied to those materials which are neither perfect (Newtonian) liquids nor perfect (Hookean) solids. In general, deformation consists of both shear and elongation, but so far only the effects of shear have been measured on seawater samples. In Newtonian liquids, resistance to deformation, the viscous modulus, G" (Pa), is directly proportional to shear rate, -y (s-1), itself representing d-y/d/ [where 7 is amount of shear (dimensionless) and t is time]; there are no elastic forces. In Hook- ean solids, resistance to shear, the elastic modulus, G' (Pa), is directly proportional to 7 and independent of 7, and there are no viscous effects. Most biological materials, polymer solutions, polymer melts, suspensions, emulsions and colloids 2254 Vbcoelastic properties and phytoplankton fall between the Newtonian and Hookean ideals, and resistance to deformation fall between the Newtonian and Hookean ideals, and resistance to deformation consists of the vector sum of G'+ G" = G*, the complex modulus. To simplify somewhat, phytoplankton cultures (Jenkinson, 1986, 1993a) and seawater (Jenkinson, 1993b) show G" composed of a Newtonian component, independent of -y, to which is added a non-Newtonian component generally related to p 7 by a negative power, such that dynamic viscosity T| = T|MK - J\E, where TIE = ky- , and where the subscript, MK, refers to very high shear rates (in the oceanic context), as used by Miyake and Koizumi (1948) for their classical measurements of seawater viscosity, and r\E represents the 'excess' viscosity contributed by polymers. In seawater and phytoplankton cultures, P has so far been found to lie between ~0 and —1.6. Thus, G" = T\i. In these materials, measured values of G' have so far been found to lie between <,G" E/10 and ~2G"E.

Method Sampling The surface microlayer was sampled from an inflatable boat, without its outboard engine. The boat was paddled well away from the influence of the mother ship to avoid contamination. The microlayer was sampled using a glass plate (Harvey and Burzell, 1972). The volume of the liquid collected divided by the area of the plate gave a nominal thickness of the sampled layer equal to between 66 and 74 n-m, but the degree of mixing with underlying water is unknown. Water from the upper and lower mixed layers and the pycnocline was sampled by Niskin bottle. The sediment was sampled with a Reineck box corer, and the light 'fluff lying on the sediment surface was gently removed with a wide-mouthed pipette.

Analyses Subsamples were preserved in acidified Lugol's iodine (Throndsen, 1978) for counts of Nscintillans (by naked eye using a clear plastic graduated bottle), for microplankton and aggregates (magnification of 100 using a 0.6 cm3 settling cham- ber) and for nanoplankton (magnification of 400). The organic carbon contributed by Noctiluca was estimated by assuming that cell size was 200 |xm diameter, and converting this volume into organic carbon following Eppley el al. (1970). This gave estimated biomass of 3.68 x 10"7 g C cell*1 for Noctiluca. For Phaeocystis, a value of 14 pg C cell"1 was used, following Rousseau et ai's (1990) investigation. Using a Fuchs-Rosenthal haemocytometer, aggregates were sized and their approximate cumulative volume calculated as a preserved aggregate fraction (PAF). Samples preserved in 4% glutaraldehyde were used for the determination of numbers of bacteria and heterotrophic nanoflagellates (HNAN) by epifluorescent microscopy of material stained with 4'6-diamidino-2-phenylindole (DAPI) (Por- ter and Feig, 1980). Biomass of bacteria was calculated using the conversion factor of 20 fg C per bacterium (Fuhrman and Azam, 1982). 2255 I.RJenkinson and B.A.Blddanda

For chlorophyll determination, water was filtered through GF/C filters,an d the chlorophyll a was estimated spectrophotometrically (Jeffrey and Humphrey, 1975). Values for the density of seawater were derived using oceanographic tables (UNESCO, 1987) from salinity (S) and temperature (f), and expressed as the density anomaly, a(S,t,0).

Measurement of viscosity and elasticity Characterization at low shear rates of the weak rheological structure in seawater is slow and is not possible on board ship using current techniques. Even though the properties of most samples were determined only once, it was necessary to keep some samples for up to 7 days. Since the effects of preservatives on the bulk-phase rheology of seawater containing mucus are unknown, and since Carlson (1987) found that the viscosity of unpreserved seawater microlayer samples did not change over 5 days, we stored our material unpreserved at ~4°C. [The dilemma of whether or not to add preservatives to samples for rheometry is similar to that, described by Farrington and Hedges (1993), when sampling for dissolved organic carbon.] Samples were not filtered as our interest was the rheological properties of whole seawater. The samples were measured for viscosity and elasticity at shear rates from 0.0021 to 0.973 s'1 in a Low Shear 30 Sinus rheometer (Contraves AG, Zurich), using a '2T-2T' Couette system (Jenkinson, 1993b).

Results and discussion During the cruise on 7 and 8 June 1988, wind speed did not exceed 2 m s"1 and for much of the time conditions were 'flat calm'. Throughout much of the cruise area, parallel bands characteristic of Noctiluca blooms (cf. Yirbsetai, 1986; Schaumann et ai, 1988) marked the sea surface, and the sea colour was generally brownish yellow, probably due mainly to the large concentrations of Phaeocystis sp. (Table I)- At the three principal stations, 1,2 and 3, the water column presented a slightly stratified upper mixed layer, a well-defined main pycnocline and a homogeneous lower mixed layer (Figure 2). Temperature difference was almost entirely responsible for the stratification at station 3, and also played the major r61e at station 1, but salinity was the dominant stratification parameter at station 2. Station 3 may have been occupied by 'offshore' water from the central German Bight, while at station 1 a slight influence of more dilute coastal water was apparent. The water at station 2 was markedly warmer and fresher than at stations 1 and 3, indicating that this station may have been occupied by the well-defined band of water which moves east then north along the coasts of the Bight, receiving river run-off rich in nutrients (Gerlach, 1987; Hesse et al., 1992). A rather similar surface salinity distribution was shown by Eberlein et al. (1985) during Phaeocystis blooms in June 1981. Taking all hydrological layers together, station 2 was biologically richer than stations 1 and 3 in all measured biological parameters, except for N.scintillans numbers (Table I). 2256 Table I. Summary of the data

Sta- Layer Depth Chlorophyll Bacteria HNAN Phaeocyslis Noctiluca PAF i •"IE G\ G' Gv 3 tion (m) (M-g (M-gC (mm" ) (cells mm •')" (cells dm ')• (xlO-) ( mPa s) (mPa s) (u.Pa) (ixPa) (u-Pa) dm-') dm-')

1 A 0 0.6 4.9 1.0 31.3(438) 250 (920) 590 .217 0.25 3.6 14.1 14.6 B 3 2.4 3.0 0.5 11.8(165) 44(162) 46 .217 0.57 7.6 1.2 7.6 C 12 4.3 4.2 1.5 5.9 (83) 36(132) 7 .218 0.17 13.7 1.9 13.8 D 30 2.1 3.8 144 4.7 (66) 36(132) 55 .218 0.12 7.0 0.01 7.0 E 45 ND 163 1.0 ND ND ND .218 0.02 4.5 0.0 4.5 2 A 0 4.6 48.1 9.7 53.7 (752) 40(147) 636 .207 2.79 19.3 9.9 27.2 B 3 6.1 21.6 2.5 20.0 (280) 200 (736) 2400 .207 2.26 24.3 0.8 24.3 C 8 5.9 30.4 3.6 27.8 (389) 91 (335) 389 .210 0.97 9.0 1.4 5.8 D 14 25.6 30.6 20.6 45.3 (634) 20 (74) 10 600 .213 35.21 263d 196.5" 328 E 15 ND ND ND ND ND ND .213 0.62 7.6 0.2 7.6 3 A 0 3.9 8.2 2.6 27.5 (385) 467(1718) 137 .218 23.8 107 92.4 141 B 3 2.3 5.4 1.0 15.3(214) 40(147) 0.2 .218 0.37 3.0 0.1 3.0 C 10 2.4 8.2 0.5 3.4 (48) 0"(0) .218 0.12 5.9 0.0 5.9 D 30 0.4 5.6 2.6 5.9 (83) 100(368) 0= .218 0.04 1.0 Off 1.0 E 41 ND 28.1 3.1 ND ND ND .218 -0.04 11.9 0.0 ll.9« Means (excluding layer E) Arithmetic mean 5.0 14.5 5.0 21.1 (295) 110(406) 1238 .22 5.5 38.7 26.5 48.6 Logarithmic mean 3.0 9.4 2.5 14.9(209) 49(162) 40 .22 0.71 11.5 1.71 13.9 3 Hydrological layer A = surface microlayer, B = upper mixed layer, C = density discontinuity, D = lower mixed layer; E = benthic microlayer of organic 'fluff "8 HNAN, heterotrophic nanoflagellates; PAF - preserved aggregate volume fraction; t\uk - viscosity according to Miyake and Koizumi (1948) for salinity in silu and temperature of measurement (l^C);-^, viscosity, measured at a shear rate of 0.00716 s~', in excess of that due to the aquatic phase; G"E, excess viscous modulus (mean of values measured at shear rates 7 from 0.0021 to 0.973 s '); C, elastic modulus (mean of values measured at shear rates-y from 0.0021 to 0 286 s '); C*E, overall excess complex modulus denved from the mean values of G\ and of C given in Table I: [(IC"E IC",) + (IC'I-G'))"; ND, no data. " Values in parentheses are expressed as estimated equivalent in organic carbon (mgorg. C m '), denved according to Eppleyr/o/. (1970), assuming cell size equivalent to a diameter of 200 (LITI for Noctituca. Estimates for Phaeocyslis are based on a value of 14 pg org. C cell' and do not include extracellular mucus (Rousseau el al, 1990). ' Value of 20 assigned for logarithmic transformations. ' Value of 0.1 assigned for logarithmic transformations. * Arithmetic mean of two series of measurements. • Shear thickening indicated for this sample (viscosity positively related to shear rate). 1 Value of +0.1 assigned for log transformations. I.R Jenkinson and B.A.Biddanda

2US 25-0 245 250 —I i i | i i i 1 1 ' - Dept h 11 -A -0 • ~A ris.toi -B • • 3 -10 c'-#

• 1 Stn 3 j Stn -20 T S T S -12-5 32-6 surface 12-4 321 surface 9-3 32 B bottom • 1 m 92 32-8 bottom • 1 in 'D- -Hi : •

-40 • E""777

20--«• * Oepf h b 2W 215 22-0 225 230 i i i I i i i i l i i i i i i i i i A -B Stn 2 • -c . 10 T S — 1S1 279 surface • 307 bottom + 1 m

Fig. 1 Density stratification at the three key stations. Also shown are the depths of samples representing the hydrological layers A (surface microlayer), B (upper mixed layer), C (pycnocline), D (lower mixed layer) and E (benthic 'fluff microlayer). Inserts show surface and near-bottom temperature and salinity.

In places, when the ship was stopped, golden-brown chunk-shaped aggregates up to 2 or 3 cm across could be seen beneath the sea surface. These aggregates were so weak that attempts to sample them using a ~5 dm3 bucket resulted in their complete disaggregation. When the bucket containing sampled water was left to stand for about an hour on deck, however, similar aggregates up to 2 cm across re-formed, but showed no tendency to sink in the bucket. Some re-formed aggregates were sampled gently by wide-mouth pipette and were examined fresh on board. They consisted largely of Phaeocystis colonies and swarmers. In these aggregates Noctiluca was also present, many specimens of which contained boluses of what appeared to be Phaeocystis cells. Diatoms, dinoflagellates and cili- ates were also present in low numbers in these re-formed aggregates. Aggregates sampled by Riebesell (1993) in the same area, however, were either poor in Phaeo- cystis (in May 1989) or had Phaeocystis colonies associated mainly with the aggregates' outer surfaces (in May 1991). The type and degree of association between Phaeocystis and aggregates in the German Bight thus vary considerably. Such 2258 Viscoelastk properties and pbytoplankton aggregates may sink, rise or be neutrally buoyant (Skreslet, 1988; Riebesell, 1992; present results).

Biological and Theological parameters In terms of organic carbon, dominance of the plankton samples overall was shared by Phaeocystis sp., a haptophycean flagellate, and N.scintillans, a large heterotrophic dinoflagellate. Both Phaeocystis (Chang, 1984; Lancelot, 1984) and Nocti- luca (Uhlig and Sahling, 1982; P6res et al., 1986; Schaumann et al., 1988) secrete much dissolved organic matter (DOM), including large amounts of gel and slime. The surface microlayer was enriched in Phaeocystis cells relative to the rest of the water column (not measured in the 'fluff) by a factor of 2.9 (P < 0.001), perhaps reflecting the buoyancy found at times in this species (Skreslet, 1988). No significant difference was found between layers, however, for any other simple biological parameter. The chlorophyll/P/iaeocysfw ratio in the surface microlayer, 19-140 fg chlorophyll cell-', was correspondingly lower than that in the subsurface water, 68-730 fg cell-1 (P < 0.02), by a factor of 4.6. This difference may indicate bleaching at the surface, as found by Moreth and Yentsch (1970), whether or not the cells were viable.

The Theological parameters T|E and G' are presented in full, at all the shear rates -yfor which they were measured, in Jenkinson's (1993b) Appendix Table 3. From tests on log-transformed data, and expressed as logarithmic (i.e. geo- metric) means, in the seawater from the surface microlayer the elastic modulus, G', was 32 times as great (P < 0.05) as that from the bulk-phase layers (52 times if the 'fluff layer is included in the bulk phase), and the excess complex modulus, G*E, was 7 times as great (0.05 < P < 0.1). The viscous parameters measured, the 1 excess viscosity at -y = 0.716 s* , r\e, and the mean excess viscous modulus, G"E, however, were not significantly enhanced in the surface microlayer relative to the rest of the water column. Figure 3, however, indicates that the higher G '/G"E ratio may simply reflect an overall positive relationship between G'/G"E and G"E. This relationship may indicate that the samples the most thickened in terms of G"e were in general those the most dominated by 'strong' gels rather than 'weak' gels. In the terminology of Ross-Murphy and Shatwell (1993), who worked on algal and bacterial polysaccharide gels, 'strong' gels show strain-independent rheological properties even at strains >0.25 (above which they yield), whereas any strain inde- pendence in the properties of 'weak' gels breaks down at strains <0.05. Measure- ments made in the present study imposed an oscillating strain of—1.5. That in most of the more thickened samples the rheograms (Jenkinson, 1993b) indicated that structure breakdown was occurring (in the less thickened samples, the rheograms had too little resolution to resolve such breakdown in the bulk phase), is consistent with Ross-Murphy and Shatwell's idea. For comparison, using non-oscillatory, incremental-strain rheometry, Jenkinson etal. (1991) found that in three classes of marine organic aggregate yield took place on average at strains of from 0.7 to 2.7. Neither the benthic microlayer of 'fluff nor any of the non-microlayer layers was significantly different in its rheological properties from the rest of the layers. In the 'fluff layer, rheological properties may have been reduced by adsorption of polymers onto the particle surfaces. 2259 I.RJenkinson and B.A.Biddanda

Fig. 3. Elastic modulus (means of all measurements, except at 7 = 0.973 s"1) versus excess viscous modulus. [•], surface microlayer sample; [o], all the other samples. The straight line (C' + 0.1 = C 'J is just to help the reader.

Relationships between plankton abundance, chlorophyll a concentration, viscosity and elasticity Cross-correlation tables are shown for biological and rheological parameters in Table Ila for all samples (except the 'fluff layer) and in Table lib for the non- microlayer samples. In any sufficiently large (n>~ 20) set of statistical tests, a subset of them is likely to appear statistically significant (P > 0.95) by chance alone. It is more appropriate to consider a plot of the ranks of the probabilities against the P values themselves (a P-value plot) as this provides insight into significance in the context of the whole set of tests, rather than only of individual tests (Schweder and Spj0tvoll, 1982). In P-value plots, the 'non-significant' P values tend to lie close to a straight line, while the higher, significant P values follow an upward curving line. Figure 4a and b shows P value plots for P-tests associated with the correlations in Table Ila and b, respectively. Since the different parameters of the rheological measurements are likely contributed in part by the same mechanical structures, however, they have been considered as not mutually independent, so correlations with only one rheological parameter, the mean excess complex modulus, G*E, have been included in these P-value plots. Among the biological parameters, chlorophyll, bacteria and HNAN correlated positively. In the whole sample set (Table Ila), rheological properties correlated in 2260 Viscoelastic properties and phytoptankton

Table II. For log-transformed variables, correlation coefficients (r x 100) (upper value in each pair of values) and probability, P (lower value in each pair) (a) Including air-sea surface microlayer, but excluding benthic 'fluff microlayer (n = 12)

Bac HNAN Pha Noc PAF C G\ +63 +47 +44 -31 +59 +78 +85 +50 +75 Chi 7x10- 0.02 0.05 0.3 3x10- 1x10"' lxlO-10 0.006 7x10"' +55 +67 -03 +56 +61 +51 +42 +49 Bac 0.001 lxlO"5 0.99 8x10-5 1x10- 0.005 0.05 0.03 +38 -14 +55 +40 +50 +36 +45 HNAN 0.1 0.85 8x10- 0.04 0.008 0.2 0.03 +33 +78 +77 +54 +77 +62 Pha 0.2 3x10^ 4x10-" 0.002 4xlO-« 1x10- +24 +20 +02 +29 +12 Noc 0.5 0.7 0.99 0.4 0.9 +73 +70 +74 +75 PAF 4x10-' 3xlfr^ 3x10"' 2x10-'

+92 +83 +90 T|B <10-'u 6x10-'°

+78 +96 G'B 8x10-' <10-'° +98 c <10-'°

(b) Excluding both air-sea surface microlayer and benthic 'fluff microlayer (n = 9)

Bac HNAN Pha Noc PAF G\ C G\ +67 +41 +71 -24 +81 +90 +95 +84 +92 Chi 0.007 0.2 2x10- 0.7 4x10"* 1x10-* <10-'° 8x10-" 2x10-' +44 +73 +24 +70 +72 +60 +57 +55 Bac 0.1 8xlO-5 0.6 2x10-4 1x10- 0.006 0.01 0.08 +39 -03 +62 +45 +52 +47 +51 HNAN 0.2 0.99 0.003 0.1 0.04 0.09 0.04 +39 +77 +89 +63 +73 +59 Pha 0.2 2xl0-J 4x10-" 0.002 1x10- 0.007 + 18 -08 -28 -22 -31 Noc 0.8 0.97 0.6 0.7 0.5 +87 +84 +77 +81 PAF 1x10-' 6x10-' 2x10-' 3x10^

+90 +87 +88 •HE lxlO"1 4x10"* 4x110-*

+90 +99 G"E lxlO"1 <10-'° +89 C 3x110-*

Chi, chlorophyll concentration; Bac, bacterial biomass; HNAN, biomass of heterotrophic nanoflagellates; Pha, concentration of Phaeocyslis; Noc, concentration of Noctiluar, PAF, preserved aggregate volume fraction; T|E, excess viscosity at a shear rate of 0.00716 s-'; G"E, excess viscous modulus; C, elastic modulus; G*E, overall excess complex modulus. 2261 I.RJenkinson and B.A.Biddaoda

0 0.2 0.4 _ 0.6 0.8 1

20-

0.8 1

Fig. 4. Values of P for each cross-correlation of the parameters shown in Table II, except that correlations for only one rheological parameter, G*E, are shown. Rank of probability is plotted against probability (/*). Data involving Nochluca are circled. Rank-/1 distributions for random data would be expected to lie close to a straight line (Schweder and Spj0tvoll, 1982). The vertical and horizontal lines represent our suggestion for the value of (/>, rank) above and to the right of which the data appear significant in the context of the overall data set. (a) All depth layers; (b) data for surface film layer excluded. general with Phaeocystis numbers about as well as with chlorophyll. In the subsurface samples alone (Table lib), however, rheological properties correlated much better with chlorophyll than with Phaeocystis. This difference reflects the lower ratios in the surface microlayer of both ch\oxo^hy\\l Phaeocystis and chlorophyll/rheological properties (Table I). While these lower ratios in the surface layer are consistent with a strong functional relationship between the secretion of rheologically active material by Phaeocystis irrespective of its physiological state, it seems likely that they result at least partly from two independent phenomena: first, rising of some Phaeocystis to the surface and its possible trapping by surface tension in the calm conditions; secondly, a tendency for rheologically active organic matter to adsorb at the surface (Frew and Nelson, 1992) and to exist in the bulk phase immediately below this surface (Goldman et al, 1988). The relationship between the excess complex modulus (representing overall thickening) and chlorophyll a over all hydrological layers (Figure 5) is:

G*E = 4.3[2.1-5.5]-Chl' (n = 12) (1) where Chi is chlorophyll a concentration in p,g dm"3 and values in square brackets are 95% confidence limits. A similar positive relationship can be discerned in Fig- ure 4 for each of the microlayer and the bulk-phase sample sets. For the non- microlayer samples, the relationship was:

= 2.0[1.3-3.1]-Chl1J(0J>-"i (2) 2262 Viscoelastic properties and phytoptankton

To test whether the microlayer showed G*B higher, for a given level of chlorophyll, than the bulk phase, the distances from the regression lines [equations (1) and (2)] of the microlayer points were compared (independent /-test) with those of the bulk-phase points (Figure 4). Using equation (1), G*e in the surface microlayer was higher than that in the bulk phase (P < 0.005) by a most probable factor of 14 (95% confidence that the factor exceeded 2.1). The corresponding estimate obtained using equation (2) was 6.5 (95% confidence that the factor exceeded 2.3).

Comparison with the Mediterranean Calculated from 50 measurements on 32 samples of bulk-phase seawater sampled over a year (1986/1987) in the Rade de Villefranche, Mediterranean, Jenkinson (1993b) found the complex modulus, G*E, to average 4.0 jiPa. From a 15 month investigation of plankton biomass at the same station in 1989/1990, Wiadnyana (1992) showed a mean value for the biomass of total pico-, nano- and microplankton of 25.7 u.g C dm-3, of which autotrophic biomass constituted 38.3% (9.8 jig C dm3). Estimated from a typical ratio of chlorophyll a:phytoplankton carbon of 2% (Raymont, 1980; Butterwick etai, 1982), this represents an estimated mean of 0.2 \ig chlorophyll a dm3. The estimated 'average' co-ordinate for the Mediterranean is shown in Figure 5. A circle of radius log(5) centred on this point suggests an intuitively estimated uncertainty zone cumulating sampling errors, systematic errors in estimating chlorophyll level and those due to mismatch because the values to be compared were determined at different seasons and in different years. To compare like with like, an equivalent point (co-ordinate of arithmetic means of G*E and chlorophyll for all bulk-phase samples) is shown for the North Sea cruise. (In a log plot, any arithmetic mean falls above and to the right of the centre of the cloud of its elements.) 0 7 The bold, dashed line joining these points represents G*E = 13-Chl - . Although confidence limits cannot be estimated, the positions of these two points suggest both that a close relationship between thickening and phytoplankton abundance might be general across different scales, but that, for a given chlorophyll level, bulk-phase water in the Rade de Villefranche (over the year) may have been more thickened than that in the North Sea Phaeocystis bloom.

The benthic microlayer of organic 'fluff Samples from the benthic microlayer of 'fluff were greyish and appeared thickly cloudy to the eye. Even though some of the clearly enclosed particulate load may have settled in the Couette system of the rheometer, it is nevertheless remarkable that the particles did not render the 'fluff microlayer significantly more viscous and elastic than the other layers. Any tendency they may have had to do this by increasing the particle volume fraction may have been offset by adsorption of colloidal material onto the exposed surfaces of these particles. Such adsorption might make the colloidal matter more available to biological consumers. 2263 I.RJenkinson and B.A.Biddanda

-1 -0.5 0 0.5 1 tog chlorophyll a [mg.m-3]

Fig. 5. Excess complex modulus (C*e) versus chlorophyll a concentration. [•], bulk-phase samples from North Sea cruise; [•], surface microlayer samples. The middle and lower dashed lines represent the respective regressions in equations (1) (all samples) and (2) (bulk-phase samples only). •, log co-ordi- nates of arithmetic averages for the Mediterranean (lower left) and the present study (upper right). Dashed circle, estimated error zone (factor of 5) around Mediterranean co-ordinate.

'Dissolved' organic material and Phaeocystis abundance 'Dissolved' and colloidal material (DOM) was not measured in the present study. During a previous Phaeocystis bloom also in the German Bight, however, Eberlein et al. (1985) found that the concentrations of 'dissolved' organic nitrogen (DON), free amino acids (DFAA) and 'dissolved' carbohydrates (DCH) were positively and strongly correlated with Phaeocystis cell numbers. Much of the carbohydrate in the water column during Phaeocystis blooms may have consisted of the mucopolysaccharide chrysolaminarin, which Phaeocystis excretes directly in large quantities to form its mucus envelope (Chang, 1984). The amount of any substance present at equilibrium equals (production rate x residence time), and Eberlein et al. (1985) suggest that the high levels of DOM associated with high Phaeocystis numbers might represent long residence by the DOM because bacterial utilization of DOM is inhibited by acrylic acid, an antibac- terial agent which Phaeocystis secretes (Sieburth, 1964). Grossel and Delesmont (1986) showed that acrylic acid concentration was related to Phaeocystis density in a bloom of up to 170 x 106 Phaeocystis cells dm"3, but that the maximum concentration of acrylic acid in situ was only 13 u-g dm"3, while 50 u.g dm 3 was found necessary to inhibit bacterial growth. If this acrylic acid is preferentially concen- trated in mucus-reinforced microzones (i.e. colonies), however, as the findingso f Davidson and Marchant (1987) suggest, its local concentration may be sufficient to 2264 Viscoelastic properties and phjioplankton protect the mucus from bacterial attack and hence the microzones from turbulent dispersion. That Phaeocystis can catabolize its own mucus in the dark (Lancelot and Mathot, 1985) suggests that this mucus is not biologically refractory. Solutions in water of polymerized acrylic acid are non-Newtonian, and their rheological properties have been much studied in relation to the types of co-polymer present (Yemelyanov et al., 1990). If the acrylic acid is polymerized, or complexed with the mucopolysaccharide of Phaeocystis colonies, it may modify the strength and other rheological properties of the mucus.

Further relationships among plankton abundance, PA F and rheological properties The shape of the aggregates in the preserved samples was irregular and variable, and their maximum volume was equivalent to that of a sphere of diameter 1 mm. Some aggregates were whole or broken Phaeocystis colonies, containing numer- ous cells, while others contained no Phaeocystis cells, and may have been either former Phaeocystis colonies which the cells had left, as described by Verity et al. (1988), mucus from Noctiluca, or marine snow formed by bacterial adhesion (Bid- danda, 1986) and aggregation (Biddanda, 1985) of secreted organic matter. Even gentle sampling by bucket disrupted the large fragile aggregates visible in the water, the samples taken for preservation were subject to high shear in the taps of the water bottles and Lugol's preservative dissolves much phytoplankton mucus, including that of Phaeocystis colonies (Chang, 1984). Thus, the aggregates finally visible in the preserved samples are likely to represent only the tougher, more highly flocculated part of the aggregate population in situ. Nevertheless the PAF was large, between 0 and 1.06% (mean 0.12%). PAF was not significantly associated with any hydrological layer, but it showed significant correlation with all rheological and biological parameters except Nocti- luca (Table Ila and b). We were concerned lest the aggregates or the large diameter (up to 0.35 mm) Noctiluca cells in the (fresh) samples might artificially increase our viscosity or elasticity values by bridging the measuring gap in the Couette system. That none of the rheological parameters were significantly correlated with Noctiluca suggests that direct bridging of the measuring gap by large particles did not contribute appreciably to the measured rheological properties, and that the excess viscosity and elasticity measured were contributed principally by non-aggregated colloids. Bridging between small marine organic aggregates (Jenkinson, 1991) and between aggregates more generally (Otsubo, 1994) deter- mines rheological properties at length scales larger than that of aggregate size. Phytoplankton-produced transparent exopolymeric particles (TEPs) show huge differences in stickiness, both to different surfaces and as a function of taxonomic and physiological differences in the secreting organisms (Ki0rboe and Hansen, 1993; Ki0rboe etal., 1994). Variation in abundance, stickiness and bridging mechanisms in TEPs may thus sometimes be related to rheological properties at scales larger than that of TEP size. Mucus probably tends to be more evident to the casual observer when it remains around its producer organism than when it is dispersed and diluted into the 2265 I.R Jenklnson and B.A.Biddanda surrounding medium (Jenkinson, 1986; Smetacek and Pollehne, 1986). Scavenging of colloidal material by floes,however , is likely to reduce viscosity measured either between floes or at length scales much greater than floesize , but disaggregation of floes by increased turbulence in situ could increase viscosity again. This may be of particular importance in strong winds during or just after Phaeocystis blooms, when the aggregate polymers may disperse, thus reducing lumpiness (rheological heterogeneity), and perhaps increasing inter-aggregate viscosity enough to trap bubbles either mixed down by waves or produced by near-surface out-gassing due to high oxygen concentrations. Such trapped bubbles might be the origin of the foam produced after blooms, and if the remaining lumps are strong enough they may be brought up to the surface by bubble-induced buoyancy, as suggested for mucus diatom colonies (Stunzhas et al., 1994), and shown in mucus events in the North Sea (Riebesell, 1992) and the Adriatic (Herndl et al., 1992). As well as mucus, Phaeocystis also secretes small molecules which escape from the colony (Lancelot and Mathot, 1985), and outside Phaeocystis colonies, as mentioned above, the acrylic acid concentration is likely to be too small to inhibit bacterial activity. The mucus of healthy Phaeocystis colonies was obviously fairly free of bacteria, which indicates that coupling between primary production and bacterial secondary production was drastically inhibited in these microenvironments. The high correlation of bacterial biomass both with Phaeocystis numbers and with chlorophyll (Table Ila and b) in the water as a whole nevertheless indicates that bacterial growth is not prevented in the surrounding water, where current ideas about the close coupling between the activities of phytoplankton and bacteria (Biddanda, 1988; Michaels and Silver, 1988) were confirmed. Such ideas can also explain the significant correlation among metabolite secretors (here represented by chlorophyll and Phaeocystis), metabolite consumers and polymerizers (bacteria), new available colloids (responsible for enhanced rheological properties), and consumers of bacteria and polymer disrupters (HN AN) (Table II). Noctiluca mucus and any aged Phaeocystis mucus no longer poisoned by acrylic acid secretion (Lubbers et al., 1990) may constitute mid-water, turbulence-free microenvironments (Paerl, 1985) suitable for enhanced bacterial (Biddanda, 1988) and protozoan (Biddanda and Pomeroy, 1988) activity.

The rdle of Noctiluca That Noctiluca appeared well distributed through the water column indicates that the population was young and vigorous: mass floating is associated with dying individuals and with ageing populations (Uhlig and Sahling, 1982; P6res et al., 1986) and develops in the German Bight only from late July (Uhlig and Sahling, 1982). Table Ila and b, as well as Figure 4a and b (in which data points involving Nocti- luca are circled) show the remarkable absence of a correlation between Noctiluca abundance and all other parameters. This concurs with the conclusions of an extensive study by Uhlig and Sahling (1982). They also found that Noctiluca 2266 Vbcoelastk properties and phyioplanklon showed no correlation with other variables, and that its annual cycle in the German Bight is apparently influenced little by variation in external factors.

Estimated shear rates in situ during the cruise The intensity of small-scale turbulence is conventionally represented as root mean square (r.m.s.) shear rate. Often this has to be calculated from published values of turbulent energy dissipation, e. Since values of e have been calculated using assumed values of Newtonian viscosity (e.g. Miyake and Koizumi, 1948), it is appropriate to use the Miyake and Koizumi viscosity T\MK to derive shear rate from the literature:

r.m.s.-y=1.93-(e/TiMK)«(s-') (3) where e is energy dissipation (W m~3). Currently, measurement of r.m.s. y poses technical difficulties in water of low turbulence. Measurement of in situ rheological properties has yet to be made in conjunction with measurements of oceanic turbulence. From conversions of published values of e made using equation (3), r.m.s. y of 5-36 s"1 occur in waves breaking at sea (Kitaigorodskii, 1984), and as low as 3 x 10~* s"1 have been observed by divers in deep thermoclines (Van Leer and Rooth, 1975), lower than the approximate lower cut-off for present instrumentation. Oakey and Elliott (1982, Figure 16) plotted turbulence dissipation per square metre against the cube of Uw (wind speed at a height of 10 m) in a mixed layer —20 m deep. Their Figure 16 predicts r.m.s. -y equal to 1 s~' when Ul0 is 12.6 m s~' and 0.06 s"1 at 2.7 m s~' , the lowest co-ordinate for which they expressed confi- 1 dence. Extrapolation of Oakey and Elliott's relationship to L/10 of 1 m s" give r.m.s. -y equal to 0.028 s~'. Values of r.m.s. y < 0.0052 s-', however, accounted for half the sampling periods during a calm-weather project (Osborn and Lueck, 1985; Fig- ure 14), while Farmer et al. (1987) reported values of only 0.01 S"1 in the upper 1 mixed layer (but higher nearer fish) when Uw was 1.5 m s" . In addition, as pointed out by Bowen et al. (1993), because of the skewness of the distribution, the most frequently occurring shear rate may be an order of magnitude below mean -y (and thus nearer two orders of magnitude below r.m.s. y). In the samples comprising the present study, excess viscosity was negatively related to shear rate by a negative exponent of 1.1 (Jenkinson, 1993b; Table II). Given the probable shear rates in the practically flatcal m conditions in the present study, we thus conclude that values of % for -y of 0.00716 s1 (Table I) are likely to represent conservatively high in situ modal values for the surface mixed layer. R.m.s. -y is difficult to estimate, however, for the other hydrographic layers.

The oceanographic context for further measurements of viscoelasticity in relation to plankton Most processes involving pelagic organisms, such as secretion and uptake in microzones, plankton feeding (Jenkinson and Wyatt, 1992; MacKenzie et al., 1994; Jen- kinson, 1995; Ki0rboe and Saiz, 1995) and bacterial clustering (Bowen et al., 1993) 2267 I.RJenkinson and B.A.Biddanda involve characteristic length scales. This length scale is frequently closely related to that across which the deformation rate acts on the particular process. For each length scale (and thus for each process), a distribution of shear rates will be present, and each shear rate in this distribution is subject to viscoelasticity over the same length scale. In a homogeneous medium, viscosity and elasticity would be independent of length scale. In natural waters, however, the importance of length scale on viscoelastic properties is in part due to the presence of particles which can be classified as: (i) hard (functionally undeformable by ambient forces); (ii) soft (functionally deformable, but not destructible by ambient forces); and (iii) fragile (readily destroyed by ambient forces). Re-aggregation is then a function of turbulence and stickiness (Jackson, 1990; Ki0rboe and Hansen, 1993). Fragile particles may generally be in dynamic equilibrium between agglomeration and mechanical destruction. The even more tenuous part of the continuum represents the liquid phase. Such distinctions may be equivalent to the differences, already mentioned, between 'strong' and 'weak' gels. Since pelagic processes take place both within and outside particles, the deformation rates right through a parcel of sea ('particles' and 'liquid') may act on such processes. Furthermore, because elastic effects, together with those of buoyancy, tend to restore deformed shapes by 'remembering' previous configuration, they will act to decouple mixing parameters from those of the spectrum of deformation rate, particularly where deformation forces are sporadic (Jenkinson, 1990; Jenkinson et ai, 1991). Some phytoplankton may have evolved the ability to use slime secretion to decouple mixing parameters and to change and manage the physicochemical environment (Jenkinson and Wyatt, 1995). The respective contributions of polymers and other particles to both viscosity and elasticity, particularly under different conditions of turbulence, require further modelling and observation. One of the major goals of research on deformation, including turbulence, in natural waters should be to quantify the spectrum of deformation rates (shear and elongation) at scales pertinent to different processes, and to determine the time of deformation (for instance the components of simple shearing and elongation). This should be done bearing in mind the rheological properties of the materials present and the biologically active substances bound or otherwise associated with them (e.g. stimulators, inhibitors, toxins, sex attractors, 'scent' trails of prey and preda- tors). Further development of methods to observe such shape restoration in situ, combined with rheological measurement of mechanical resistance to deformation, will be necessary to understand turbulence, dispersion and flocculation in the sea, particularly as altered by both buoyancy and biorheological secretions. The geometry of the particles, any physical links (i.e. bridging percolation) between them and their size spectrum all determine interaction in rheological properties among different length scales, as well as spectra of rheological variance both in batches of randomly taken subsamples and in series of successive measurements on the same subsample. It is therefore important to be aware of the scale and the geometry addressed in rheological measurements: from measurements by Jenkin- son (1993b), it can be deduced that those reported here concerned a volume of water sheared within a measurement gap 0.5 mm wide and 1.4-3.6 cm2 in area (i.e. 0.07-0.18 ml), although during measurement some exchange must have occurred

2268 Viseoelastic properties and pbytoplankton between the material in the measurement gap and that in the rest of the apparatus (total volume 1-3 ml). The generally positive relationship between Theological and biological parameters may be explained by several possible mechanisms: (i) active migration into or out of floes or zones of increased viscosity (Goldman, 1984); (ii) reduction of speed through the water by sinking, rising or swimming organisms when passing through either viscous zones or zones richi n sticky particles or networks; (iii) scavenging of organisms by sinking or rising floes or by those in turbulent motion; (iv) production of thickening polymers by the planktonic organisms themselves. Mechanism (i) might produce either positive or negative correlations, and mechanisms (ii) and (iii) mostly positive correlations, but at scales probably not greater than of dispersal over a few generations (days and centimetres to tens of kilometres). It is hard to see how correlations over larger scales (e.g. between the North Sea and the Mediterranean, as in the present study) could be explained other than by mechanism (iv). Evidence from both investigations on cultures (Jen- kinson, 1986, 1993a; Ki0rboe and Hansen, 1993) and casual observations of blooms (see Introduction) suggests that the amount and nature of the thickening compounds present are likely to depend not only on the biomass and primary production of the plankton, but also on its taxonomic and physiological state, as well as on degradation and dispersion. Apart from in isolated patches, turbulence is generally much less marked in the middle of both lake-sized (Spigel and Imberger, 1987) and ocean-sized (Toole et ai, 1994) basins than near their horizontal and vertical margins. Jenkinson (1986), who found excess viscosity inversely related to shear rate in phytoplankton cultures by a power of 0 to -1.3, suggested that the effects of polymers on deformation may be relatively just as important in low-productivity deep waters as in areas of high biomass inshore. That excess viscosity in the sea has been found related to shear rate to a power of -1 to -1.4 (Jenkinson, 1993b), but also related to chlorophyll levels to a power of +1.1 to +1.3 (this study), adds further weight to the idea. Measurements of spectra of both turbulence and Theological properties will no doubt prove easier in productive, inshore zones, but both are necessary in practically all waters. Non-Newtonian properties in natural waters will have to be measured and taken into account to refine estimates of deformational forces and energy dissipation, and to re-assess their relationships with Kolmogorov parameters, which are themselves inputs to models of turbulent processes and mixing. Without this fundamental work, the chemical, ecological and evolutionary implications (Jenkinson and Wyatt, 1992,1995) of this biophysical modification of the ocean continuum will remain largely inaccessible.

Acknowledgements For hospitality and help we thank V.Smetacek, P.Abreu, S.Elken, K.Hesse, K.Muller, M.Pamatmat, R.Plugge, U.Riebesell, F.Rieman, K.Schaumann, C.Turley, E.Wahl, H.von Westernhagen, C.Wiencke, and the master and CTew of the 'Victor Hensen'. We also thank D.H.Cushing, J.L.S.Hansen and T.Wyatt for improvements. This is AW1 Publication no. 937]. Both authors were supported 2269 I.RJenkinson and B.A.BkJdanda

primarily by Alfred-Wegener-Institute Research Fellowships, while I.R.J. has also been helped by the clients of ACRO, by the French Interministerial Mission for the Sea within the French National Programme on Harmful Algal Blooms and by Danish Science Research Council grant no. 9401060 to Thomas Ki0rboe. Alfred- Wegener-Institut filr Polar- und Meeres-Forschung, Am Handelshafen, 27570 Bremerhaven, FRG, is the institute having primarily supported this work.

References

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