Degradation of faecal pellets in Pegea confoederata (Salpidae, Thaliacea) and its implication in the vertical flux of organic matter

Journal

ELSEVIER

of Experimental Marine Biology 203 (1996) 147-177

JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY

and Ecology,

Degradation of faecal pellets in Pegea confoederata (Salpidae, Thaliacea) and its implication in the vertical flux of organic matter W.D. Yoonax*, J.-C. Martyb, D. Sylvain”, P. Nival” “Universitt! Pierre

et Marie

Curie

(UPMC),

mer, Station Zoologique, hiJPMC, ‘Universite’

CNRS-INSU, Nice-Sophia

CNRS-INSU,

Observatoire

Oct!anologique

Chimie Marine,

BP 8, 06230

Antipolis,

Observatoire

BP 28, 06230

Laboratoire

Ockmologique

Villefranche-sur-mer,

de Villefranche-sur-mer, Villefranche-sur-mer,

de Thermodynamique

de Villefranche-sur-

France Laboratoire

Physique

et

France

Expkimentale,

Parr

Valrose,

06108

Nice, France

Received

14 October

1994; revised 29 September

1995; accepted

25 October

1995

Abstract Faecal pellets of P. confoederatu were maintained in suspension for 10 days and changes in their morphological, microbiological and fatty acid characteristics as well as their resulting sinking rates were followed during this period. Among the morphological characteristics measured, the perimeter, the surface area and the longest dimension decreased linearly with time but their form remained unchanged. The weight decreased. Microbiological concentrations showed three stages, a rapid increase was followed by a rapid decrease and then finally a small re-increase for heterotroph populations and stabilization for autotrophs. Total fatty acid concentration followed a similar pattern to that of microbial concentrations with some exceptions for individual fatty acids. These three stages in degradation were attributed to incubation conditions as well as to trophic relationships. The sinking rates, measured in different turbulent conditions, varied from 2706 to 3646 m day - ’ for the fresh faecal pellets and decreased 30% after 10 days incubation whatever the turbulent kinetic energy dissipation rate. For fresh faecal pellets, the observed sinking rates were greater in highly turbulent conditions than in moderately turbulent or in calm conditions. At the beginning of incubation, minima1 sinking rates were observed in moderately turbulent conditions and after four days in calm conditions. This was attributed to the state of degradation of the faecal pellets. Considering the wind induced turbulence for the 0 to 200 m layer, high wind speeds delay sinking rates and increase residence times when compared to moderate or low wind speeds. According to our calculations, the residence times in this superficial layer of faecal pellets of P.

*Corresponding author. Present address: Department Nam-gu, Inchon, 402-751, South Korea. 0022.0981/96/$15.00 0 1996 Elsevier SSDI 0022-0981(95)02521-X

of Oceanography,

Inha University,

Science B.V. All rights reserved

253 Yonghyun

dong,

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confoedeuuru, an oceanic salp species, never exceed from 0 to 24 m SC’). Keywords:

Degradation;

Ed.

203 (1996) 147-177

100 min (calculated for wind speeds varying

Faecal pellets; Salps; Sinking rates; Turbulence

1. Introduction The role of faecal pellets produced by the zooplankton is known to be important in the vertical flux of organic matter from the superficial layer to the sea floor (for review, see Fowler and Knauer, 1986; Alldredge and Silver, 1988; Noji, 1991; Small and Ellis, 1992). General characteristics of the faecal pellets such as high abundance, relatively large size, fast sinking rates and incorporation of organic and inorganic matters allow faecal pellets to mediate organic matter as well as pollutants, metals and radioactive elements (Fowler et al., 1987; Fisher et al., 1991) through the water column. During sinking, faecal pellets are used as a food source by pelagic and benthic organisms (Paffenhiifer and Strickland, 1970; Paffenhiifer and Knowles, 1979; Gonzalez et al., 1994), they undergo microbial remineralization, are fragmented by biological (Lampitt et al., 1990; Noji et al., 1991) or physical processes, and are incorporated into larger aggregates. These different processes can modify the characteristics of faecal pellets such as size, weight, microbiological and biochemical composition and sinking rate. Most of the studies concerning the role of faecal pellets in the vertical flux have focussed on the quantity and quality of the material transported from the euphotic layer to the sea floor. Flux estimations were made from samples taken with sediment traps or pumps (Wiebe et al., 1976; Bishop et al., 1977; Honjo, 1980 U&r-e and Knauer, 1981; Matsueda et al., 1986; Morris et al., 1988; Voss, 1991). The flux was also estimated from the mass and sinking rate of the faecal pellets using the abundance and production rate (Wiebe et al., 1979; Paffenhiifer and Knowles, 1979; Bruland and Silver, 1981; Madin, 1982). Optical methods (Asper, 1987; Hecker, 1990; Gardner and Walsh, 1990) and chemical characteristics of faecal pellets (Marty et al., 1994) were also used for flux estimations. Salps are known to form prodigious swarms which can modify the local ecosystem temporarily (Coale and Bruland, 1985; Morris et al., 1988; Bathmann, 1988). These gelatinous tunicates, capable of filtering I litre of seawater per h (Madin, 1974) and to retain particles as small as 0.7 km (Harbison and Gilmer, 1976 Bone et al., 1991), produce faecal pellets of rectangular form which sink at a rate of 2000 m day- ’ (Bruland and Silver, 1981). Taking into consideration their high faecal pellet production rate (Madin, 1982) and their fast sinking rate, salp faecal pellets must have an important episodic impact on the vertical flux of organic matter. In the present study, we investigate the temporal evolution of morphological, microbiological and fatty acid characteristics and of sinking rates of an oceanic salp species, P. cnnfiederatu, faecal pellets. The experiments presented in this paper had two objectives, to follow the ageing of salp fecal pellets and monitor their consistence as well as organisms interactions with the pellet decay in time and to evaluate the role that such pellets have in vertical particle flux. Both experimental setups operate on different time scales, decaying over days, sinking over hours.

W.D. Yoon et al. I J. Exp. Mar. Biol. Ecol. 203 (1996) 147-177

2. Materials

149

and methods

A chain of P. confoederata collected in April, 1992, in the surface layer in the bay of Villefranche sur mer, France, 43”41 ‘lO”N, 7”19’O”E, was transferred to a 500 1 tank of seawater filtered through a 200 pm mesh filter. No additional food was added. The transport time from sea to laboratory was less than 15 min. As soon as the faecal pellets were produced, they were pipetted intact to a glass Petri dish, rinsed 3 times with 0.22 pm filtered, sterilized seawater and stored in a refrigerator at 1°C for less than 12 h. Faecal pellets having an unusual shape or having no faecal content (pseudofaeces) were discarded. For the incubation of faecal pellets, we used 0.45 pm filtered seawater. Faecal pellets were incubated in a 1 1 acid-rinsed glass bottle. Another bottle without faecal pellets was used as control. The experiment was conducted in a darkroom at a temperature of 14°C (the seawater temperature at the sampling site). The bottles were rotated (45 rpm) along the longest axis to maintain the faecal pellets in suspension. The experiment was divided in two parts. The first lasted 11 days, from D, to D ,,, inclusive (D = day). During this period, the faecal pellets that remained unfragmented were studied. Samples were taken once a day and analysed as described below to follow the changes in morphological, microbiological and fatty acid characteristics and the resulting faecal pellets’ sinking rates. The second part began at D, , and finished at D,, . During this period only faecal pellet fragments were studied. Samples were taken every two days and analysed as described below. 2.1. Morphological

characteristics

of faecal pellets

The following parameters of faecal pellets were obtained using an image analyzer (Gorsky et al., 1989) surface area (S), perimeter (Pe) and longest dimension (Ld) as size parameters and circularity (Ci.F) and convexity (Co.F) factors as form parameters. The lower detection limit of the analyser was 48 pm. 2.2.

Weight

Individual faecal pellets were weighed with a Mettler H54AR micro balance at the beginning (D,) and the end of incubation (D,,). Each faecal pellet was placed on a precombusted and preweighed Whatman GF/F glass fibre filter, dried at 60°C for 72 h then weighed and combusted at 520°C for 4 h. The dry weight and ash dry weight were measured. 2.3. Microbial

concentration

The seawater used in dilution and filtration of samples for microbial counting was prepared as follows: 0.22 pm filtered, autoclaved and stored in a refrigerator at 1°C. seawater were Every day, from D, to D,,, one faecal pellet and the surrounding sampled from the incubation bottle. The particle concentration in the surrounding seawater increased with time. For this reason, we had to increase the dilution ratio with time. The first day we sampled 10 ml of the surrounding seawater, the two following

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days 5 ml and from the D, on, 2 ml. A 10 ml sample was taken from the control bottle. The faecal pellets and surrounding seawater samples were made up to a final volume of 10 ml with prepared seawater. The faecal pellet, once its morphological characteristics had been measured, was fragmented with a mixer (Breda Scientific) and homogenized with a sonicator (DeltaSonic) for 4 min. This procedure was necessary because of the compact nature of the faecal pellets. The use of the sonicator alone for 10 min did not completely homogenize the faecal pellets. To each sample, we added 20 yl of DAPI (4’6-diamino-2 phenylindole, 0.2% of final concentration) and 400 pl of formaldehyde buffered with borax (50% (v/v) of final concentration). The samples were then filtered on a 0.2 pm Nuclepore black membrane and frozen at - 70°C. All counts of microbial populations were carried out using a Zeiss epifluorescence microscope. The epifluorescence equipment and counting procedure employed in this study were described in detail by Rassoulzadegan and Sheldon (1986). The differentiation between small and large bacteria and between heterotrophs and autotrophs was made, respectively, according to their size (cf. Ferguson and Rublee, 1976) and to their fluorescence colour (Table 1). 2.4. Fatty acid analysis Once a day, we extracted the fatty acids of one faecal pellet, of 10 ml of surrounding seawater and of 10 ml of control seawater. Lipids were extracted according to the method of Bligh and Dyer (1959), using sonication (5 min). Solvent was removed from the extract using a Speed-Vat system. Fatty acids from total extracts were transmethylated with 7% BF3 in methanol, in sealed tubes under argon at 70°C for 30 min. Separation of fatty acid methyl esters was carried out with Sep-Pak silica cartridges using solvents of increasing polarity, as described earlier (Viso and Marty, 1993). Fatty acids were then analysed by capillary gas chromatography on both polar (Carbowax) and non-polar (CPsil 5 CB) columns. The non polar column was 25 m long and 0.32 mm (I.D.) and used with a split-splitless injector in splitless mode and He as carrier. The temperature was held at 40°C for 2 min, then increased from 100 to 280°C at a rate of 2 C” mini ‘. The polar column was 25 m long, 0.32 mm (I.D.), used with a solid (Grob) injector and He as carrier. Temperature increased from 100 to 200°C at a rate of 1.5 C” min- ’ . Resolved compounds were identified by comparison of their retention time with those Table I Microbial

population

Group Small bacteria Large bacteria Pica-heterotrophs Nano-heterotrophs Cyanobacteria Pica-autotrophs Nano-autotrophs

groups and their characteristics

used in counting

Size and shape

Fluorescence

SO.5 pm, form cocci

Light blue Light blue Blue Blue Yellow-orange Red Red

from 0.5 to 2 IJ-m, form cocci or rod

52 pm >2 pm 52 pm >2 pm

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of standards run in the same conditions on the two columns, and by GC-MS analysis of selected samples which were then used as standards for identification by GC. Analytical conditions for GC-MS analysis have been described elsewhere (Claustre et al., 1989). Quantification was achieved by integration of peaks with the Nelson Analytical system. Concentrations were calculated with respect to the internal standard (known amount of Cl9 methyl ester) added to the samples prior to extraction, Absolute concentrations are given for each faecal pellet (which are assumed all to be identical, see above). For liquid samples the units are given in millimetres of seawater. 2.5. Sinking rate of faecal pellets The sinking rate measurements of faecal pellets aged from 0 to 10 days were carried out in a turbulent environment. The schematic diagram of the experimental apparatus used is shown in Fig. 1. 2.5.1. Calibration The turbulence in the experimental water column was produced by a motor at 12 rpm connected to and generating the vertical oscillation of a perforated disc. The experimental cylinder was filled with 200 pm filtered natural seawater. The turbulence, in terms of the turbulent kinetic energy dissipation rate (E), was calculated using aluminium paper and transparent vinyl particles’ sinking rates. The particles were rectangular and their volume and density were determined before the beginning of the experiment. The turbulent conditions of the experimental set-up were kept constant for 12 h preceding measurement of sinking rates. The introduction of particles was carried out through a special opening (glass pipe in Fig. 1) under the perforated disc. A series of sinking rate measurements were carried out in still water and another with agitation corresponding to disc oscillation amplitudes of 5, 8.5, 12 and 16 cm. The sinking rates of particles were measured at 6 depths: O-15, 15-30, 30-50, 50-80, 80-l 10 and 1 lo- 140 cm from the particle release spot. After 10 sinking rate measurements, the temperature and salinity were measured at each depth. The sinking rates were used to evaluate the turbulent kinetic energy dissipation rate (E) for each observation depth by the following procedure. The basic equation is F=ma (see Table 2 for abbreviations) When a particle is moving vertically

in a liquid, F =ma becomes

F = F,, - Fd where F,,=(pP-pw)V;g and Fd=Cd.p,,,.A.U2/2 (Granata and Dickey, 1991). But when a particle sinks with a constant speed, the acceleration term, a, is equal to 0. In this case F,,=Fd, then s = (C,P,&‘~/~)~(P,

- P,)V,

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Side view

P -f-

+

motor

1st arm 2nd arm

-f-

plug --+I. ruler

203 (1996) 147-177

-

-

-

-

-

-

*

24 I.

25 I.

-

-

-

L3 L2 Ll Z6

Top view

Fig. 1. Schematic diagram of the cylinder used in sinking rate experiment. The dashed line box on left side enlarged at tight showing the diverse amplitudes of vertical oscillation, All dimension are in cm. Al, 5; A2, 8.5; AX, 12; A4, 16; d, 5; LI, 185; L2, 180; L3, 140; Dl, 20; D2, 19; D3, 0.8; Zl, zone O-15 cm; 22, zone 15-30 cm; 23. Lone X0-50 cm; 24, zone 50-80 cm; Z5, zone 80-I 10 cm; 26, I IO-140 cm.

The acceleration due to gravity, g, is calculated from the sinking rate data in still water in zones of O-140 cm where only gravity acts on the vertical movement of particles, calculated mean g is 980 cm SC* with a standard deviation of 37 cm s-* (n = 54) this is the same as the well known fundamental constant g. When an exterior force(FC) acts on the vertical movement of a particle, this force must be expressed as an acceleration term, according to its intensity and its angle of application on the particle to retard or to accelerate the movement which is already taking its course. In this case where an exterior force exists, the equation F = Fh - Fd is no longer applicable unless one introduces another acceleration term. This acceleration term, g’, changes with the intensity of F, and with observation depth and it will be included in 8, thus

W.D. Yoon et al. I J. Exp. Mar. Biol. Ecol. 203 (1996) 147-177 Table 2 Parameters A a C, d ; Fh F, F, g 8’ H L* L<> L, M Re u U’ v, W Z P,

P, l

Y

153

used in calibration Particle surface area, calculated, mm* Acceleration, mm s-* Drag coefficient Particle nominal diameter, calculated, d=(Ll Lo La/3)“” “‘) Force, mg mm ss* Acceleration of vertical movement of particle due to F Buoyancy force Drag force Exterior force acting on vertical movement of particle, mg mmm2 Fe Acceleration due to gravity, mm sm2 Acceleration due to F,, mm s-’ Particle height, measured, mm Particle width, measured, mm Particle length, measured, mm Longest dimension, calculated, mm Mass, mg Reynolds number (=d.Ulv) Sinking rate of particles (mm s-’ ) Sinking rate difference in absence and presence of turbulence Particle volume, calculated, mm3 Work, mg mm* s-’ Vertical distance, cm Particle density, pp = 1.28817 mg mm-j, n=49 Sea water density Turbulent energy dissipation rate, mm2 s -’ Kinematic viscosity ( I 1 mm2 s ‘)

Equation used to estimate the turbulent energy dissipation speeds: l=u*.3/Kz, where u*=fc.U,,, u* Friction velocity, m s-’ Constant, 0.00123 fc Wind speed 10 m above the sea surface “,,I K von Karman’s constant, 0.4 Depth, m Z

rate at various wind

N.B. the C, was calculated according to Granata and Dickey (199 1). C,=24/Re(l+0.131 Re (’ 82-“‘15’0’ R’), for 0.01
- Pw>V,(g

+ s’>

We supposed that the application angle of Fe on particles is 0 and that the Fe acts on the downward movement of particles and is expressed as an acceleration term, then F, = mg’ = (pp - P,)V, g’. This exterior force may be expressed as work, W (Proudman, 1953). This work depends upon the force applied on an object and upon the resulting speed difference, then

W.D.

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W= F$J’

The dissipation E =

rate of this work per unit of particle

mass is

WIVp(Pp- p, 1

If we integrate

this E for the vertical distance

E = WIAz(p,

(z) of each observation

depth, then

-p,)

Fig. 2 shows the sinking rates of particles and the calculated E for each observation depth. The retardment in sinking rates in the zone 0- 15 cm was considered positively as an acceleration. An exponential equation was best fitted and the E values cited hereafter correspond to those read on this equation for a given observation depth.

2.5.2. Measurement of faecal pellet sinking rate The turbulence was produced by 12 cm of oscillation amplitude during 24 h to obtain a stabilized turbulent regime. The faecal pellets from the incubation bottle were sampled randomly and daily. Their morphological characteristics were measured with the image analyser, and they were then introduced into the cylinder. Their passage times between 0 and 15, 15 and 50, 50 and 80, 80 and 110 and 110 and 140 cm were noted. After this, the temperatures at the same zones were measured to O.Ol”C. Vertical distances between two measurement points (O-15 cm classed hereafter as highly turbulent water, 15-50 cm as moderately, 50-80 cm as weakly, 80-l 10 cm as very weakly and 1 lo-140 cm as calm waters) were used to distinguish different turbulent environments in experimental apparatus, in the results and in the discussion sections.

0

20 40

60

80

100

120

140

D (cm) Fig. 2. Mean sinking rates (U, m day-‘, observation number= 60) of particles and their calculated turbulent kinetic energy dissipation rate (E, mm2 s ‘) in relation with the vertical distance (.!I, cm) in the experimental apparatus. The regression line is l = 9.320 e -” 01147D (r’=O.783). This equation was used to evaluate E for each vertical distance of the cylinder.

W.D. Yom et al. I J. Exp. Mar.

2.6. Particles

originating

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155

from the faecal pellets

At D,,, all faecal pellets from the incubation bottle were sampled and particles originating from faecal pellets were studied from D,, to D,,. Every 2 days, 2 ml of seawater from incubation and control bottles was sampled for enumeration of microbial populations and 5 ml for the description of particles’ morphological characteristics and sinking rate measurements. The experiment methods were identical to those previously described except that the sinking rate measurements were conducted in still water.

3. Results The morphological characteristics of faecal pellets collected within short laps of time are represented in Table 3. For individual faecal pellets, morphological characteristics were measured and the mean as well as the standard deviation were calculated. All calculated coefficients of variation did not exceed 17%.

3.1. Temporal

changes

in the morphological

characteristics

of faecal pellets

The size parameters (Fig. 3a) decreased linearly with time (significant at P =O.Ol, n = 11) but not the form parameters (Fig. 3b, (nonsignificant at P = 0.05, y1= 11). We have observed that the envelope of faecal pellets (probably the mucus net described in Caron et al., 1989) disintegrated rapidly in the incubation bottle and from the second day on, was not observed. The absence of an exterior envelope probably allowed the faecal pellet content to disperse continually in the surrounding water. The result shows that the degradation of faecal pellets in suspension is continuous and decreases particle size but does not modify the original rectangular form.

3.2.

Weight

Faecal pellet weights were measured at the beginning and at the end The dry weight of faecal pellets showed a decrease of 89.3%. The loss of was of 82.5% and that of inorganic matter 93.0% (Table 4). This result faecal pellet maintained in suspension loses its content continually with Table 3 Morphological

Mean SD C.V.

characteristics

of faecal pellets at the time of collection

(at D,‘,

Pe (mm)

S (mm’)

Ld (mm)

Ci.F

Co.F

17.65 3.14 17.78

12.63 I .74 13.74

5.44 0.98 17.98

53.06 10.1 19.03

87.02 4.72 5.42

Pe=perimeter; S =surface area; Ld= longest dimension; S = standard deviation; C.V. =coefficient of variation.

Ci.F=circularity

of incubation. organic matter shows that the time.

n ~25)

factor;

Co.F=convexity

factor;

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l

012345678910 D(day)

(a)

60

0

012345678910 (b)

D(day)

Fig. 3. Changes in size (a; perimeter, surface, longest dimension factors) parameters of faecal pellets of P. cmfoederutu during estimate (observation number of 3 to 5)

3.3. Temporal

evolution

and form) and (b; circularity and convexity IO days incubation. Bars indicate I SE of

in microbial populations

The concentrations of different components of the microbial population were expressed in numbers per mm3 of faecal pellets and in numbers per ml of surrounding seawater and of control. 3.3. I. Faecal pellets The temporal evolution of heterotrophs and of autotrophs detected in faecal pellets (Fig. 4a) seems to follow a similar trend. Increases between D,, and D, and decreases between D, and D,. From D, and on, the heterotrophic population increases and the autotrophic population becomes stabilized. Table 4 Weight change Day

DC, D,,, All values ADW=ash

,I 3

6

in faecal pellets of P. cmfoedrruru DW (mg)

ADW (mg)

OMDW (mg)

OMDWIDW

6.09/1.18 0.6510.42

3.93/0.x3 0.2710.23

2.16/0.35 0.38/0.19

35.61 I 1.27 63.07/l] .52

were expressed as mean/standard deviation. n =number dry weight (=dry weight of inorganic matter); OMDW=dry

(o/)

ADWIDW (%) 64.391 I .?I 36.93/ I I.52

of observations; DW=dry weight of organic matter.

weight;

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small bacteria

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D (day) Fig. 4. Evolution of microbial populations during experiment. (a), in the faecal pellets; (b), in the surrounding seawater (solid line) and in the control (dashed line). At D,,, the faecal pellets not fragmented were exhausted and the experiment was continued with particles of faecal pellets until D2,. The symbols used are identical in (a) and (b).

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(umtinurd)

Surrounding seawater During the first part of the experiment of 11 days, the microbial concentrations varied greatly from day to day. The small and large bacteria appear to undergo similar temporal

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variation and their minima observed at D, are followed by an increase. The cyanobacteria concentration showed an increase at the beginning (from D, to DX) reaching their maximum at D,. After D,, a decrease was noted with a minimum at D,. From D, on, the concentration became stable. Pica- and nano-sized organisms, absent at D,, were observed from D, and on. Pica- and nano-heterotrophs reached maximum concentrations at D, and D,,, respectively. Pica-autotroph concentration, after a small initial increase, shows no further growth, The nanoautotrophs increased from D, to D, and then decreased to a minimum at D,. An oscillation with time was observed for this group. At D,, the stock of faecal pellets in the incubation bottle was exhausted but the remaining fragmented particles of faecal pellets were incubated until the end of the experiment (D,, ). During this second part of the experiment, the small and large bacteria and pica-heterotrophs showed an increase but their concentrations began to decrease from D,,. In nano-heterotrophs we observed a continuous decrease. Cyanobacteria and pica-autotroph concentrations remained stable during this second part of the experiment. The nano-autotrophs showed a large variation with time (Fig. 4b). 3.3.3. Control All microbial populations in the control bottle showed lower concentrations than those in surrounding seawater (from 10 to IO3 times lower) and their variation ranges were relatively narrow, except for the pica-heterotroph population. In the control bottle, the small and large bacteria increased slowly and reached their maxima at D,. Thereafter they showed a continuous and small decrease. In picoheterotrophs, a rapid increase was observed from D, to D,,. After its maximum they seem to decrease slowly. The nano-heterotrophs were absent in the first 10 days and from D,, to D,, they seemed to grow slowly. Cyanobacteria population increased rapidly at the beginning of the experiment, from D, to D, , followed by a slow decrease with a minimum at D,. Picoautotrophs were absent until D,, and after, their concentration remained stable. The nano-autotrophs were observed only once at D,, (Fig. 4b). 3.4. Fatty acid analysis Fatty acids identified and classed in different groups are shown in Table 5. Total fatty acid concentration is depicted in Fig. 5.1 as a typical example in the temporal evolution. In faecal pellets this concentration decreased rapidly at the beginning of the experiment, from D, to D, , and slowly in the following days. In the surrounding seawater, on the contrary it showed a great increase from D, to D, and decreased in the following days. In the controls no temporal variation was observed. It seems that fragmented faecal pellets release their content to the surrounding seawater and that this is the principal cause of temporal variation in the two media. It is noted that, at D,, the concentration of fatty acids is the same for the surrounding seawater and control, certifying the absence or very weak concentration of organic matter in the seawater used to incubate the faecal pellets. The polyunsaturated fatty acids show another trend. In the faecal pellets their concentration remained constant until D, and then decreased rapidly. In surrounding

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l

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iCl5

o aC15 A iC16 A iC17 0 deltaC17

0 0

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D (day) Fig. 5. (1) Temporal change m concentration (ng) of total fatty acids in faecal pellets ( 1 pellet), surrounding seawater (IO ml) and in control (IO ml). (2) Temporal change in concentration (ng) of 7 ‘bacterial’ fatty acids in faecal pellets (1 pellet), (a) and in the surrounding seawater ( IO ml), (b). (3) Temporal change in concentration (ng ml-‘) of C205w3 during experiment in the surrounding seawater. This polyunsaturated fatty acid is known to be absent in bacteria. (4) Temporal change in percentage of ‘bacterial’ fatty acids over total fatty acids in the surrounding seawater.

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8

D (day) Fig. 5. (continued)

seawater their concentration increased rapidly and then stabilized. In the controls, the unsaturated (mono and poly) and ‘bacterial’ fatty acids showed an inverse relationship with time, indicating probably that the unsaturated fatty acids were used in bacterial development. In Fig. 5.2, we show the temporal evolution of 7 fatty acids which were supposed to be of bacterial origin (Table 5). The proportion of branched and cyclic fatty acids in bacteria depends upon the amount of precursors (Kaneda, 1977) and they may be absent in some bacteria (DeLong and Yayanos, 1985). Since heterogenous bacterial communities are present in the marine environment, we use branched and cyclic fatty acids as indicators of bacterial activity as suggested by Wakeham and Canuel (1988) and Reemtsma et al., 1990. All of these ‘bacterial’ fatty acids were not detected in the controls. In the faecal pellets the concentrations decreased rapidly at the beginning and stabilized in the following days. In the surrounding seawater the schema is completely different, showing an increase at the beginning and a decrease followed by a small increase from D, to D,,. This temporal evolution was identical for another fatty acid,

162

W.D. Yom et al. I .I. Exp. Mar. Biol. Ed.

Table 5 Fatty acids analysed

and categorized

Faecal pellet (ng per pellet)

Surrounding

Control

seawater (ng ml ‘)

(ng ml ‘)

according

20.3 (1996)

147-177

to their characteristics

D

SFA

MUFA

PUFA

‘B’FA

Total

D,, D, D, D, D,,, D,, D, D, D? D,,, D,, D,

5056 28.14 39.45 29.84 21.19 21.43 65.15 138.80 43.31 72.4 1 I x.99 19.37

16.93 IO.47 II.21 8.14 2.02 2.79 13.46 59.73 15.95 35.71 2.70 0

2.94 2.26 3.21 1.48 0.34 0.97 I .32 8.16 3.54 7.36 I .5x 0.31

9.77 3.61 3.96 3.28 2.52 2.17 8.85 15.06 6.67 I 1.29 0 1.02

no.20 44.47 57.83 42.74 26.07 27.37 88.78 221.70 69.46 126.80 23.28 20.69

The values are expressed as concentration in ng. D=day; SFA= saturated fatty acids; MUFA= monounsaturated fatty acids; PUFA = poly-unsaturated fatty acids; ‘B’FA = ‘bacterial’ fatty acids (see text) which comprise iCl5, aCl5, iC16, iC17, aC17, AC17 and AC19.

Cl6 l(n-7) (not shown on Fig. 5.2b). The fatty acid aC17 in faecal pellets is an exception and showed an increase followed by a stabilization. AC19 shows a different temporal evolution; rapid decrease in the faecal pellets and absent between D , and D,. In the surrounding seawater we did not detect AC19 from D,, until D, and when a rapid increase was observed after D,, this increase corresponded with a stagnation of the other ‘bacterial’ fatty acids, indicating that AC19 is not an indicator of ‘bacterial’ fatty acids. We suppose that the increase at the beginning of the incubation is due to the enrichment of the surrounding seawater by bacteria of faecal origin. The decrease following the maxima would be a result of consumption on bacteria by heterotrophs. This is shown clearly on Fig. 5.3. Because the C20:5(n - 3) a polyunsaturated fatty acid, is not observed in faecal pellets and in the control and is known to be absent in bacteria, this fatty acid may come from the heterotrophs growing on the expense of the bacteria. In the surrounding seawater, ‘bacterial’ fatty acids, even though we can not supply a definite answer for their nature, seem to stabilize in proportion after D, (Fig. 5.4) which would suggest that a constant ratio between species is attained in bacteria population (we are not sure that this is equivalent to individual bacterial fatty acids).

3.5. Sinking rate In spite of the difference in turbulence intensity at different depths in the experimental cylinder, all faecal pellet sinking rates are negatively and linearly related with time (Fig. 6). 3.5.1. In highly turbulent water The E between 0- 15 cm (0 = the depth of introduction of faecal pellets) varied from 6.333 to 3.018 mm* s I. The mean sinking rates decreased with incubation time from

163

W.D. Yoon et al. I .I. Exp. Mar. Biol. Ecol. 203 (1996) 147- I77

1000 1

1

(4 0 ,

,

,

0

,

,

,

o:,,,

5 6 7 8 9 10

0

,

,

1 2 3 4

,

,

,

,

‘::* % ;ij lOOO-

:

W

, , , , , , , , , , , 0 12 3 4 5 6 7 8 9 10

0

‘q

(b)

,,-,,

1 2

,‘t o

3 4

,,,

,

5 6 7 8 9 10

, , , , , , , , , 1234

5678910

D (day)

(4

: 0

,

,

0

1 2

,

,

,

3 4

,

,

,

,

I

I

5 6 7 8 9 10

D (day) Fig. 6. Temporal change in sinking rate (m day-‘) of faecal pellets of P. confoederafa. (a) in highly turbulent water; (b) in moderately turbulent water; (c) in weakly turbulent water; (d) in very weakly turbulent water; (e) in calm water. Bars indicate I SE of estimate (observation number 3 to 5)

164

W.D. Yoon et al. I J. Exp. Mar.

.

Bid.

Ed.

203 (1996)

0

IIIIl’,‘,,~0

147-177

0

012345678910 (b)

D(dw)

Fig. 7. Temporal change in size (a) and form (b) parameters of faecal sinking rate measurements. Bars indicate I SE of estimate (observation

3646 m day ’ at D,, to 2534 m day-’ 7) decreased with time too.

pellets of P. confoederutu used in the number 3 to 5).

at D,,, (Fig. 6a). The volume of faecal pellets (Fig.

3.5.2. In moderately turbulent water The E between 15-50 cm varied between 3.018 and 0.536 mm’ SC’. The mean sinking rates varied from 2706 m day- ’ at D,, to 1994 m day -’ at D ,(, (Fig. 6b).

33.3.

In weakly

turbulent

water

The E between 50-80 cm was varying from 0.536 to 0.122 mm* s ‘. The mean sinking rates varied between 2928 m day- ’ at D, and 1946 m day- ’ at D,,, (Fig. 6~).

3.5.4. In very weakly turbulent water The E between 80- 110 cm was varying from 0.122 to 0.028 mm’ s- ‘. The mean sinking rates varied from 2910 m day ~-’ at D, and 1932 m day- ’ at D ,() (Fig. 6d).

3.5.5. In calm wuter The E between 1 lo-140 cm was varying from 0.028 to 0.006 mm* SC’. The mean sinking rates lay between 2967 m day- ’ at D, and 1926 m day- ’ at D ,,, (Fig. 6e).

(3) (3) (4) (3) (3) (3)

112.2/_53.6 (6) 89.9/50.0 (6) 123.3/61.7 (16) 121.7/51.1 (17) 100.2/67.3 (16)

_

u (m day-‘)

characteristics

0.4 I /0.27 0.46/0.44 0.43/0.28 0.41/0.23 0.54/0.32 0.46/0.37

(mm)

Pe

(46) (79) (70) (65) (71) (100)

of particles

0.009/0.013 0.013/0.02 0.012/0.014 0.010/0.010 0.019/0.023 0.014/0.026

A (mm’)

The values were expressed as mean/standard deviation (number of observations). Numbers of observations and convexity factors (Co.F) were the same as those of perimeters (Pe); (-)= no observation.

558/213 958/434 637/329 788/278 861/364 1213/647

D,, D,? D,, DIJ D,Y DI,

’)

c (ng ml

sinking rates and morphological

Day

Table 6 Concentration,

(Ci.F)

97.4314.62 98.62/2.61 98.9912.42 98.42/3.38 63.77113.89 98.36/3.90

Co.F

(Ld), circulatory

61.12ll4.47 62.32/ 13.50 67.02/11.16 64.39112.14 60.99112.79 97.1 I 14.76

Ci.F

for surface (A), longest dimension

0.16/0.1 I 20.19/0.18 0.17/0.1 I 0.16/0.09 0.21/0.12 0.18/O. 14

(mm)

Ld

3

3 ; 6’ z 2 g & E ? G

I? P

i

co -+ a ‘-

166

3.6. Particles

W.D. Yom et al. I J. Exp. Mar.

originating

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203 (1996)

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from the faecal pellets

The particle concentration seems to increase with time which suggests that the fragmentation of particles is a continuous process (Table 6). No particle morphological characteristics were in relation with time (Table 6). This result is due to the detection limit of the image analyser which is 48 p,rn for this experiment. This resolution is insufficient to detect small variations in form and size parameters. The sinking rates of particles varied from 90 m day- ’ to 123 m day ‘, but no relationship was found with time (Table 6).

4. Discussion The faecal pellets of f. confoederatu were degraded in a rotating incubation bottle (45 rpm) in total darkness. This incubation condition induced morphological, microbiological and fatty acid changes in the faecal pellets and consequently influenced their sinking rates.

4. I. Morphological

changes

The synergy of the biological and physical conditions (rotation and maintainance in suspension) could enhance the degradation leading to decrease in size as well as in weight of the faecal pellets. Their sinking rates show a negative linear relation with time. This degradation generates an increase in particle concentration in the surrounding seawater. The particles originating from faecal pellets are continuously fragmented into smaller ones. The diminution of size of faecal pellets and the increase in particle concentration in the surrounding seawater needs some comments. According to Jackson (1990) and Jackson and Lochmann (1992), the coagulation of particles results in increase of the particle size if the particle concentration is beyond a certain limit (in general near the stationary plateau) and if the coagulation conditions are satisfied (particle size, stickiness and shear rate of medium). In rotating vessels, Shanks and Edmondson (1989) have observed an aggregate formation from natural unfiltered seawater and attributed it to the shear and differential settling. They noted also that mucus, characteristic of marine snow may act as a ‘glue’ sticking particles together leading to aggregate formation (see also Kiarboe et al., 1990; Riebesell, 1991, 1992). The mucus could be produced by bacteria, some algae or animals. In our experiment bacterial concentrations in faecal pellets and in surrounding seawater were very high (Fig. 4a and Fig. 4b) and they should produce the mucus which are known to play a role in increasing particle stickiness (Kranck and Milligan, 1980; Biddanda, 1985). Nevertheless no aggregate formation was observed. We speculate that either the high rotation speeds of the incubation bottle or the compositional characteristics of faecal pellets of P. confoederutu, being a non-selective filter feeder, caused this no-aggregate formation.

W.D. Yoon et al. I J. Exp. Mar. Biol. Ecol. 203 (1996) 147-177 4.2. Microbiological

and fatty

167

acids ’ evolutions

Numerous authors have studied the temporal evolution of microbial populations. For example, Fenchel(1970) Harrison and Mann (1975) and Robertson et al. (1982) studied seagrass, Linley and Newell (1984) and Biddanda (1985) macroalgae, Hoppe (1981), Fukami et al. (1985) and Biddanda (1985) phytoplankton, Honjo and Roman (1978), Pomeroy and Deibel (1980), Jacobsen and Azam (1984) Peduzzi and Herndl (1986), Caron et al., 1989 and Gonzalez and Biddanda, 1990 faecal pellets, and Davoll and Silver (1986) and Gorsky et al. (1989) appendicularian houses. All of these authors describe the microbial population succession in time as follows, rapid growth in bacterial populations initially followed by a decrease which corresponds to a growth in heterotroph populations (pica- and nano-flagellates and ciliates). The result of this present study is in agreement with this description and can be divided in 3 stages; first stage, increase at the beginning reaching the maximum concentration; second stage, decrease from maximum to generally minimum concentrations and third stage, a new increase of heterotrophs and stabilization of autotrophs. Considering the first stage, the growth rates of microbial populations investigated in this experiment (apart from nano-heterotrophs) from D, to D, in faecal pellets were higher than 0.25 day-‘. In the surrounding seawater it exceeded 0.9 day y’ for small and large bacteria and 0.5 day- ’ for cyanobacteria and pica- and nano-autotrophs. For the second stage, the growth rate from D, to D, in faecal pellets was lower than - 1.5 day-’ for small and large bacteria and for pica- and nano-heterotrophs and lower than - 2.3 day-’ for cyanobacteria and pica- and nano-autotrophs. In the surrounding seawater, it was lower than - 1.4 day- ’ for large and cyanobacteria and lower than -0.5 day-’ for small bacteria and pica- and nano-autotrophs. The pica- and nanoheterotrophs had a positive growth rate. For the third stage, the growth rates from D, and on, in faecal pellets varied from 0.01 day-’ for heterotrophs (bacteria included) to 0.002 day ’ for autotrophs. In surrounding seawater the cyanobacteria and pica- and nano-autotrophs showed a negative growth rate (-0.0005 day-‘). It must be noted that a mixotroph population developed at the end of this experiment in the faecal pellets as well as in the surrounding seawater and this would partly explain the stabilization in autotroph populations. The incubation conditions may influence this succession in microbial populations. Fragmentation of faecal pellets could result from the rapid rotation of the incubation bottle and the maintenance in suspension of faecal pellets. This condition should promote the development of microbial populations, for the following reasons. (1) a rapid rotation allows microbes to evolve in a constantly renewed environment, (2) fragmentation of faecal pellets provides a constant nutrient and microbe supply for the surrounding seawater and (3), surface area increases (due to size decrease in faecal pellets and to concentration increase in particles) produces an increase in microbial substrate (Fenchel, 1970; Harrison and Mann, 1975). These incubation conditions explain why the maximum microbial concentrations in the surrounding seawater were delayed one or two days in comparison with that in the faecal pellets and why the negative growth rates in nanoheterotrophs were observed. These results are in agreement

168

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with the results of Logan and Hunt ( 1987) and Logan and Alldredge (1989) who have found that the bacteria and diatoms in vertically sinking porous aggregates can increase their nutrient uptake up to 60 and 21010, respectively. When considering the trophic relationships, we observed that (1) the increase in nano-heterotrophs in faecal pellets corresponded to the fluctuation in pica-heterotrophs and in bacteria and to the stabilization in autotrophs, (2) in the surrounding seawater, between D, and D,,,, an increase in nano-heterotrophs corresponded to the small increase in bacteria and to the decrease in pica-heterotrophs and (3) after D,,, in the surrounding seawater, in contrast to (2), nanoheterotroph concentration decreased progressively but those of bacteria and picoheterotrophs increased. This indicates the establishment of a trophic relationship between bacteria, pica- and nano-heterotrophs ( 1, 2 and 3) and, less evidently, between pica-heterotrophs and nano-heterotrophs (2 and 3, Pomeroy and Deibel, 1980; Andersen and Fenchel, 1985; Rassoulzadegan and Sheldon, 1986; Gonzalez and Biddanda, 1990). This microbial succession shows also that there exists a close relationship between faecal pellets and surrounding seawater, because at D,,, all faecal pellets were exhausted and at this time the concentration of nanoheterotrophs was lOOO-times higher in faecal pellets than that in surrounding seawater, if we consider the same volume. The trophic relationship and the growth rate of each component of the microbial population should explain why the minimum concentrations were observed at D,. The mean growth rate of microbial populations in faecal pellets at the beginning of incubation (first stage of temporal evolution) was higher than 0.25 day-‘. This indicates that, before D,, populations doubled using the particular and dissolved faecal materials, as shown by the progressive decrease in time of mono and polyunsaturated fatty acids in faecal pellets (Table 5). Once reaching their maximum concentrations, the prey populations decreased and were consumed by predators (second stage of temporal evolution). The new development in bacteria and the stabilization in autotrophs (third stage of temporal evolution) seem to indicate that the particular and dissolved organic materials remaining in the faecal pellets and regenerated by the microbial loop, are high enough to maintain a constant growth in microbial populations in the faecal pellets and in the surrounding seawater. This view is supported by the high concentrations of mono and polyunsaturated fatty acids in faecal pellets and in surrounding seawater (Table 5). 4.3. Futty acids temporul

evolution

The distribution of fatty acids in living organisms is generally dominated by C14, C16, Cl 8 and C20. Polyunsaturated fatty acids are known to be abundant constituents of marine algae and zooplankton (Claustre et al., 1989; Viso and Marty, 1993) but virtually absent from bacteria (Shaw, 1974; Tronczynski et al., 1985). Nevertheless bacteria possess some specific fatty acids; branched chain acids from C I4 to C I9 in the iso and ante-iso position, monosaturated fatty acids (specifically in y1= 7 position), and cyclopropanoic acids such as AC 17 and AC19 (Cranwell, 1973; Matsueda and Koyama, 1977; Volkman and Johns, 1977; Van Vleet and Quinn, 1979; Gillan et al., 1983; Gillan and Johns, 1986; Tronczynski et al., 1985; Ben-Mlih et al., 1992). These fatty acids were used in this study as indicatives of bacteria. Other fatty acids have also been described as

W.D. Yom et al. I .I. Exp. Mar. Bid.

Ed.

169

203 (1996) 147-l 77

I.”

0 faecal pellets

2

0 surrounding 0 control

0.8

r

z01 < I 2 z 2 ’

seawater

0.60.40.2-

0

1

2

3

4 5 6 D (day)

a)

7

8

9

10

0 faecal pellets surrounding seawater q control l

01 0 b)

1

2

3

4 5 6 D (day)

7

8

9

10

Fig. 8. Temporal change in fatty acid ratios in faecal pellets, in the surrounding Unsaturated/saturated; (b) C- I8 unsaturated/C- 18 total.

seawater

and in control.

(a)

bacterial indicators (but were not identified in this study); branched monosaturated (Perry et al., 1979), phytanic acids (Anderson et al., 1977) and some hyroxylated fatty acids (Cranwell, 1981). The temporal changes of the fatty acids resembles that of the microbial populations. This was expected, because both analyses concern living organisms. Only the fact that the fatty acids analysis concern dead materials too, should make a difference. The temporal changes of fatty acids could be simplified in three stages, as for microbial populations. The first stage of increase was not observed in faecal pellets but in the surrounding seawater. This is because fragmentation of faecal pellets increases the fatty acid concentrations in the surrounding seawater but decreases that in faecal pellets due to decrease in volume. The second and third stages of evolution, decrease and new increase, respectively, are in agreement with those of the microbial population. The unsaturated (mono and poly) fatty acids are known to be used more easily by microbial populations than the saturated (Rhead et al., 1971). The ratio between theses two has been considered as an indicator of nutritional value of faecal pellets (Tanoue and Hara, 1986) and of their degradational state (Matsueda et al., 1986). Fig. 8a shows

170

W.D. Yom et al. I .I. Exp. Mu.

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20.3 (1996)

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Table 7 Dimensions and sinking rates of fecal pellets of salps species Species

Length

Width

Surface

Sinking rate

(mm)

(mm)

(mm’)

(m day-‘)

S. ,fu.s~formi.s

2.1-s.0

I .7-3.0

P. so&

I .9

2.85

1070

450-2700

P. so&

agg.

13.0 1.0%6.0

I.5 I .o-3.0 0.3-I .o

P. so&

sol.

Cyclosalpa

pinnatu

3.0-

320-9.50

3.0-4.0

2.0-2.2

179772238

agg.

3.0&7.0

3.0&4.5

1210-1987

S. muxima

agg.

I .o-3.0 I .o-4.0

Pegs

so& 4

P. cmfoederata

S. maxima

0.3

agg

X.63320.29

5.77-12.02

1.0332.74

qg.

38l~lYlO

Morris et al. (1988)

460/ 200

Caron et al.

1.01~1.16

333 I-4037

o present study

2678-2739

P

2766-3138

Y (Y Yoon (1995)

30 I44444 I 240333528

P

2563-3507

Y u Yoon (1995)

3OYYl I61 3066985

P

344-882

Y 01 Yoon (1995)

716-IIXI 241&1020

P

41SSS86

Y

The values were expressed as range, except the sinking rates measured by Caron et al. (1989) mean/standard

( 1989)

217O/lSO

12

3

agg.

S. ,fusiformis

Madin (1982)

588-1642 0.3

Salpa maximu

Bruland and Silver ( 198 I )

S88-1218

S. maxima

S. fusiformi.7

References

which were in

deviation. agg. = aggregates (blastozoids); sol. = solitary (oox~ids). 01, p and y indicate sinking

rates measured in O-15,

IS-SO and SO-140

cm of experimental

cylinder.

the temporal change in this ratio. A progressive decrease in faecal pellets and increase in the surrounding seawater is evident. This evolution indicates that unsaturated fatty acids in faecal pellets are used preferentially by microbes (probably by small and large bacteria growing rapidly at the beginning of incubation, Fig. 4a and that the surrounding seawater is more favorable as a growth site than the faecal pellets as degradation proceeds. The same interpretation is supported by the temporal evolution of biological activity (Fig. 8b) which is a ratio between Cl8 unsaturated and Cl8 total (Goutx and Saliot, 1980). The ratio in faecal pellets shows a small increase, which is in accordance with that of bacteria (Fig. 4a). 4.4.

Changes

in

sinking

rates

with

time

The sinking rates of faecal pellets in a given turbulent condition decreased about 30% over 10 days. We believe that this decrease is due to the decrease in their size (Fig. 7). we had strongly speculated a negative Before the beginning of the experiment, relationship between sinking rates and turbulent kinetic energy dissipation rate. In contrast, we have observed an acceleration of sinking rates in high turbulent waters and a slowing down in others. During the 10 days experiment, the maximum sinking rates

W.D. Yoon et al. I .I. Exp. Mar.

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Ecol. 203 (1996)

147-177

171

were always met in highly turbulent waters, in an observation depth of O-15 cm. The minima were observed in moderately turbulent waters, in 15-50 cm, from D, to D, and in other turbulent waters, in 50-140 cm, after D, (Fig. 6). This indicates that the sinking rates depend on the turbulence intensity and on the decrease in size of the faecal pellets. For fresh faecal pellets, at D,, of P. confoederatu, the mean sinking rates were 3646 mday-‘(n=3)inhigh,2706mday-‘(n=3)inmoderateand2863mday-‘(n=13)in other turbulent waters. These values exceed those reported in the literature (Table 7). The difference between these values can be attributed to acceleration of the sinking rates by turbulence as well as to the size of faecal pellets. The faecal pellets of P. confoederuta in this experiment were much larger than those of other salp species in the literature. Alldredge et al. (1990) supposed that marine snow could be retarded and fragmented as it sank, if the wind speed is higher than 20 m s- ’ (producing energy dissipation rates, E, ranging from 10-l to lo-* cm* s p3 in the upper 25 m of the water column). Other authors have supposed or observed the same process (Pomeroy and Deibel, 1980; Alldredge et al., 1987; Alldredge and Gotschalk, 1989). But we have observed neither retardment nor fragmentation of faecal pellets in this turbulence range which correspond, in our experiment, to that in highly turbulent water (O-15 cm). We suppose that this is because the faecal pellets of P. confoederutu were more compact than marine snow and larger than the euphausiid faecal pellets examined by Alldredge et al. (1987).

4.5. Faecal pellet J%X estimation The sinking rate is one of the most important factors which determines the vertical flux (Bishop et al., 1977; Hofmann et al., 1981). It determines the residence time of particles in a given layer. In our experiments we have observed that as they sank the faecal pellets were not fragmented and their faecal envelope remained intact. We noted also that the faecal content was very compact and that a difference in temperature of 1°C had no effect on the sinking rates. If we suppose that the faecal pellets of P. confoederutu will not undergo physical or biological fragmentation due to turbulence or to microbial activity during the sinking process, then the incorporation or colonization by microbes from the surrounding water will not change the characteristics of faecal pellets significantly and the thermocline will not change their high vertical sinking rate. Caron et al. (1989) report similar results obtained from various salp faecal pellets. Matsueda et al. (1986) and Matsueda and Handa (1986) using optical and chemical analysis have described, from sediment traps recovered at 4240 m, the presence of fatty acids (branched Cl5 and C17) in faecal pellets resembling those of salps living in the superficial layer at the time of study whose envelope was intact or partially degraded. Their data are in agreement with ours. The turbulence in the surface mixed layer is caused mainly by wind and current shear. The depth of the mixed layer depends on daily and seasonal cycles of heating and cooling. It is well known that the surface layer turbulence levels are dominated by the wind speed (MacKenzie and Leggett, 1993). For our interpretation we consider only the

W.D. Yoon et al. I .I. Exp. Mu.

172

sinking rate ( m de’ 2500

3000

3500

Hiol. Ecol. 203 (1996)

147- I77

)

4000

4500

,.-.

a)

270 _,

b””

0

0

6

12

18

wind speed (m s-l

24

)

5 10 15

f-T--

b)

‘:‘“;’

24 wind speed

(m s-l)

0 5 10 15

e)

1’

Fig. 9. Variation in sinking rate of faecal pellets of f. cvnf&dertitu

in relation with depth at various wind

speeds (m s ‘). The extrapolation procedure was described in the text (Section 4.5). (a) Sinking rates vs depth at wind speed of rates of O-200

I m s ‘;

(b) 5 m s-‘: (c) 10 ms-‘:

(d) I5 m s ‘; (e) 20 m s-‘;

m; (g) calculated residence times (=mean

sinking rate/200

(f) calculated mean sinking m) of faecal pellet\ in h or min.

depths of O-200 m in which the turbulence gererated by wind influences the sinking rate of faecal pellets of P. cor$oedevata. Fig. 9 represents the variation of the sinking rate of faecal pellets vs. depth (Fig. 9a-e), their average sinking rates between 0 to 200 m (Fig. 9f) and their residence times (Fig. 9g), in relation to wind speed. The following procedure was employed to extrapolate our results into the natural environment, taking into account the wind speed and resulting turbulence (E) level. From wind speeds varying from 1 to 24 m s- ‘, the turbulence (E) was calculated for every 5 m using the equation given in Table 2, as cited

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in Yamazaki and Kamykowski, 1991. This calculated turbulence varied from 0.000 to 6.431 mmP2 ss3 m . O-200 m depth. Then the corresponding turbulence in experimental cylinder was taken, and consequently the measured sinking rates of faecal pellets. The sinking rates varied directly with the wind speed. The calculated residence time for different wind speed varied but was always lower than 1 h 40 min and increased with increasing wind speed. This indicates that increasing wind speed delays the vertical sinking of the large faecal pellets of P. confoederutu. Short residence times do not allow physical (Alldredge et al., 1990), biological (Lampitt et al., 1990; Noji et al., 1991) or microbiological processes (Caron et al., 1989; this study) in or on the faecal pellets during sinking. Metazoan zooplankton, principally copepods, are reported as a modificator of vertical flux of faecal pellets (Lampitt et al., 1990), being consumer or destructor. The faecal pellets used in this study had a mean surface area of 12.63 mm2 (Table 3) with 3-4 mm of diameter and 3-5 mm of length. It is hardly imaginable that copepods sized l-3 mm attack, consume or destruct these large faecal pellets falling at least 2700 m day- ‘. Then we suppose that the metazoan zooplankton’s influence on the falling faecal pellets of l? confoederatu is not too great to modify their sinking rates and residence times just described, but this needs further studies. Therefore, faecal pellets of P. confoederutu conserve, during sinking, their volume and microbiological and biochemical composition nearly identical to those of the superficial layer and supply organic matter (2.16 mg per pellet) to the deep layers and eventually to the sea floor. In the Ligurian Sea, P. confoederatu is relatively rare, appearing very irregularly (Braconnot, 1971), thus at present we have no idea what its population density may be. Supposing one individual per 1000 me3 at O-50 m depth and 0.05 salp rnm2. This would give by faecal pellet production 0.099 mg C per salp me2 day-’ (calculated with an Eq. given in Madin (1982) for this species of 7.11 mm). This meets about 0.52 and 2.30% of the vertical flux reported by Marty et al. (1994), respectively for 200 and 2000 m depths at the same region. Considering that this species forms episodically great swarms (Braconnot, 1971) in the Ligurian Sea, this faecal pellet flux estimation may be taken as minimal. Taking into account the quantity of faecal pellets produced (82.446 p,g C salp- ’ hP ’ calculated with an Eq. given in Madin (1982) and the high sinking rates whatever the sea state may be, P. confoederuta, as well as other species of salps, in comparison with the copepod faecal pellets (Small et al., 1979), must play an important, if episodic, role in the transport of organic matter to the benthic layer.

Acknowledgments We are grateful to G. Gorsky for his critical reviews of the manuscrit and to Q. Bone for english correction. This paper is a contribution to EROS 2000 program (MAST 11).

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