Spatial and temporal variation of bacterioplankton in a ... · Daniel Delillea,⁎, Fabien Gleizona, Bruno Delilleb a Observatoire Océanologique de Banyuls, ... (seven stations each).

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s 68 (2007) 366–380www.elsevier.com/locate/jmarsys

Journal of Marine System

Spatial and temporal variation of bacterioplankton in a sub-Antarcticcoastal area (Kerguelen Archipelago)

Daniel Delille a,⁎, Fabien Gleizon a, Bruno Delille b

a Observatoire Océanologique de Banyuls, Université P. et M. Curie, URA CNRS 117, Laboratoire Arago, 66650 Banyuls-sur-mer, Franceb Unité d'Océanographie Chimique, Université de Liège, Allée du 6 Août, 17, 4000 Liège, Belgium

Received 21 June 2006; received in revised form 30 January 2007; accepted 2 February 2007Available online 12 February 2007

Abstract

Bacterial abundance and production were measured monthly for one year along cross-shore transects in 3 sub-Antarctic fjordsof the Kerguelen Archipelago (seven stations each). Mean values of the 3 most coastal (inside) and most offshore (outside) stationswere used to describe the relationship between temperature, phytoplankton biomass, bacterial abundance and bacterial productionover a one year annual cycle. The entire sampling protocol was repeated twice during each cruise: once at noon and once atmidnight. Over the whole sampling period, the temperature ranged from 2.1 to 7.4 °C, while chlorophyll a concentrations variedby a factor of 10, and bacterial abundance and production varied by factors of 12 and 30, respectively. Within one day, all of theseparameters sometimes varied by a factor of 4 between noon and midnight. A clear seasonality was observed for all of theparameters. However, while variations of phytoplankton and bacterial production paralleled those of temperature, bacterialabundance was low in midsummer and maximum in autumn. While no general pattern could be observed from the total data set,spatial gradients could interfere strongly with temporal changes.© 2007 Elsevier B.V. All rights reserved.

Keywords: Phytoplankton; Bacterioplankton; Seasonal changes; Diel changes; Spatial distribution; Kerguelen Archipelago; Sub-Antarctica

1. Introduction

Because the oceans are a significant sink of anthropo-genic CO2, a central objective of many major biologicaloceanographic programs is to quantify, model and predict,at global and annual scales, the flux of biogenic carboninto deepwaters. Bacterial assemblages have the potentialto influence food web and biogeochemical cycles inaquatic systems (Cottrell and Kirchman, 2004; Staroscikand Smith, 2004). In coastal areas, production, degrada-tion and export of organic matter are disproportionate

⁎ Corresponding author.E-mail address: [email protected] (D. Delille).

0924-7963/$ - see front matter © 2007 Elsevier B.V. All rights reserved.doi:10.1016/j.jmarsys.2007.02.007

compared to the open ocean (Wollast, 1998). Further-more, ratios of phytoplankton primary production tocommunity respiration exhibit high spatio-temporalvariability (Gazeau et al., 2004). Indeed, seasonal changesin growth rates and respiratory demands of aerobicheterotrophic bacteria, which dominate total communityrespiration, can induce changes from autotrophy toheterotrophy (Hopkinson, 1985; Cho and Azam, 1988;Fuhrman et al., 1989; Griffith et al., 1990; Wiebe et al.,1993; Delille et al., 1995, 1996; Delille, 2003). Theinformation available concerning the patterns of energyflow through the lower food web in polar regions is stillscarce and is often contradictory (Anderson and Rivkin,2001). Bacteria cannot be included convincingly in

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367D. Delille et al. / Journal of Marine Systems 68 (2007) 366–380

scenarios describing trophic interactions of planktoncommunities.

The upper limit of bacterial abundance in the ocean isset by phytoplankton, but this limit is not always

Fig. 1. Location of the sampling station

realized (Li et al., 2004). Since high nutrient–lowchlorophyll Southern Ocean waters are characterized byhigh concentrations of inorganic nitrogen and phospho-rus, bacterioplankton assemblages seem to be limited by

}

s in the Kerguelen Archipelago.

368 D. Delille et al. / Journal of Marine Systems 68 (2007) 366–380

DOC (Karl et al., 1991; Ducklow et al., 2001). It hasalso been suggested that a low iron concentration couldalso be a limiting factor for bacterial growth (Tortellet al., 1996). Reviewing reports of phytoplankton andbacterial abundance and production, Cole et al. (1988)found significant correlations between bacterial andphytoplankton parameters, suggesting the ubiquity of afunctional relationship between bacteria and phyto-plankton. Since the latter excrete the organic substratesessential for bacterial metabolism, it can be assumed thatbacterial dynamics are essentially controlled by phyto-plankton dynamics (Smith et al., 1995). However, the

Fig. 2. Top: Spatial distribution of surface seawater temperature in Morbihan Bchanges in surface seawater temperature (thin black line: outside stations oftriangles: outside stations of Recques Bay, gray triangles: inside stations ofinside stations of Table Bay).

model of Cole et al. (1988) is not a general rule inAntarctic seas (Billen and Becquevort, 1991; Fiala andDelille, 1992; Delille et al., 1996; Ducklow et al., 2001).Furthermore, even if the model was valid in the oceans,the situation would likely be more complex in coastalareas due to important sources of non-phytoplanktonicsubstrates (Ducklow and Kirchman, 1983; Bouvy et al.,1986; Alber and Valiela, 1994; Smith and Benner, 2005).

High latitude oceans account for about 10 to 20% ofoceanic carbon production (Berhenfeld and Falkowski,1997). Although sub-Antarctic data are necessary for theconstruction of a global carbon budget for the Southern

ay (thin black line: noon, thick gray line: midnight). Bottom: SeasonalMorbihan Bay, thick gray line: inside stations of Morbihan Bay, openRecques Bay, open circles: outside stations of Table Bay, gray circles:


Ocean, studies providing this data in the sub-Antarcticarea have beenmuch less numerous than similar Antarcticstudies (Friedmann, 1993; Bernard and Froneman, 2005).Furthermore most of the previous studies of microbialdistribution focused on short-term observations in alimited period of time (Lochte et al., 1997; Ducklow et al.,2001; Simon et al., 2004 and references herein). Theseasonal variability in plankton biomass is poorlydocumented due to the scarcity of time series observationscarried out over one or several years (Horne et al., 1969;Delille, 1990; Helbling et al., 1995; Moline and Prézelin,1996; Delille, 2003). However, seasonal changes have tobe understood in order to construct accurate carbon

Fig. 3. Spatial distribution of chlorophyll a concentration in surface seawate

budgets (Platt et al., 1992; Priddle et al., 1992; Tréguerand Jacques, 1992). This is particularly true for theSouthernOceanwhich shows intense temporal variability,perhaps the most extreme seasonality observed anywherein the world's oceans (Karl, 1993). Furthermore,variability in plankton biomass at the air–sea interfaceaffects the partial pressure of CO2 and related air–sea CO2

fluxes of the waters surrounding the Kerguelen Archipel-ago (Delille et al., 2000). The purpose of the researchpresented here was to document the spatial and temporaldistribution of bacterioplankton biomass and productionin surface waters of a coastal sub-Antarctic areathroughout an entire year. This study was carried out in

r of Morbihan Bay (thin black line: noon, thick gray line: midnight).


the frame of a project aiming to assess CO2 dynamics inthe surface waters of the Kerguelen Archipelago and toestimate related air–sea CO2 fluxes.

2. Material and methods

This survey was carried out from December 1998 toDecember 1999 in coastal surface waters of theKerguelen Archipelago (Fig. 1). Usually, the KerguelenArchipelago (69°30′E, 49°30′S) is cited in the literatureas a sub-Antarctic island. However, from a strictoceanographic point of view, this archipelago is situatedeither in the Polar Frontal Zone (sub-Antarctica) or inthe Permanently Open Ocean Zone (Antarctica)depending on the position of the Polar Front with

Fig. 4. Spatial distribution of total bacterial abundance in surface seawater

regard to the archipelago (Delille et al., 2000). Watersof the archipelago are always free of ice. Cross-shoretransects were carried out in two fjords and one largebay. Located in the southeast of the archipelago,Morbihan Bay (about 600 km2) opens to the oceanthrough Royal Pass, which is 12 km wide and 40 mdeep. The fjords, Recques Bay and Table Bay, arelocated north and south of the archipelago, respectively.Recques bay is 14.5 km deep and 2 km wide whileTable Bay is 10.5 km deep and 3 km wide and receiveswater from the Cook glacier.

Water samples were collected at 1 m depth using aNiskin bottle. Temperature was measured soon aftersampling using a Hanna thermometer with an accuracyof ±0.2 °C. Other analyses were initiated onboard the

of Morbihan Bay (thin black line: noon, thick gray line: midnight).


R.V. La curieuse within a few minutes of samplecollection.

Water samples for chlorophyll a analysis wereprefiltered through a 200 μm mesh filter to remove largerdetrital material and larger biota. 1000 mL of seawaterwere filtered through aWhatman GF/F glass-fibre filter ata vacuum differential of b20 cm Hg. Pigments wereextracted in 90% acetone in the dark during at least 2 h(Neveux and Panouse, 1987). Chlorophyll a concentra-tions were calculated by measurement of fluorescenceusing a Turner Designs fluorometer which had beencalibrated against purified chlorophyll a (Sigma).

Salinity was measured using a Guildline Portasalinduction salinometer with an accuracy of ±0.003.

Total bacterial abundance was determined byepifluorescence microscopy (Hobbie et al., 1977).

Fig. 5. Spatial distribution of bacterial production in surface seawater of

Direct counts (AODC) were performed using anOlympus BHA microscope with acridine orangestaining on a 0.2 μm pore size black Nuclepore filter.A minimum of 500 fluorescing cells with a clear outlineand a distinct cell shape were counted under oilimmersion (×1000) in a minimum of 10 randomlychosen fields.

Bacterial production was measured via the incorpo-ration of 14C-leucine (Kirchman et al., 1985; Simon andAzam, 1989). Triplicate samples (10 mL) were amendedwith L-[U14C]-Leucine (specific activity 11.5 GBqmmol−1, Amersham, final concentration 80 nmol L−1).The samples and killed controls (10 mL water+0.5 mLof 100% TCA) were incubated for 2 h in the dark inflowing seawater tables. Incubations were terminated bythe addition of TCA to a final concentration of 5%. In

Morbihan Bay (thin black line: noon, thick gray line: midnight).


the same geographic area, during the “Antares” cruise,the saturation level of leucine uptake was reached atslightly over 20 nmol L−1 (Jorma Kuparinen, personalcommunication).

The results obtained were converted to bacterialcarbon production (BCP, g) using the equation:

BCP ¼ leucineinc x ð100=7:3Þ x 131:2 x 0:86

where leucineinc is the number of moles of leucineincorporated, 7.3 is the percentage of moles of leucinein protein, 131.2 is the formula weight of leucine, and0.86 is the conversion factor for converting a gram ofprotein produced to a gram of carbon. Previous studiesshowed that this calculation is appropriate in the South-

Fig. 6. Spatial distribution of “psychrotrophic” heterotrophic bacterial abundgray line: midnight).

ern Ocean (Pedros-Alio et al., 2002; Simon et al.,2004).

After tenfold dilutions in sterile aged seawater, viableheterotrophic platable bacteria were counted using thespread plate method with 2216 E medium (Oppenheimerand ZoBell, 1952, Marine Agar DIFCO). Each dilutionwas plated in triplicate. After inoculation (0.2 mL), theplates were incubated at 18 °C for 10 days (mesophilic/psychrotrophic assemblages) or 4 °C for 20 days(psychrotrophic/psychrophilic assemblages).

Diel changes were compared bymeans of paired t-test.An analysis of variance (ANOVA), conducted in Prism4.00 (GraphPad), was used to analyse the differencesbetween coastal zone versus offshore waters, and dielchanges in specific zones.

ance in surface seawater of Morbihan Bay (thin black line: noon, thick


3. Results

The temperature ranged from 2.1 °C to 7.4 °C over thesampling period (Fig. 2). In Morbihan Bay, salinityusually ranged from 33.42 to 33.68, but in a giventransect, the maximum range of variation was 33.28 to33.68 (February 5).

3.1. Spatial distribution

The spatial distribution of biological parameters ofall transects carried out in Morbihan Bay are presentedin Figs. 3–7.

Chlorophyll a sometimes varied 10 fold along thesame transect (Fig. 3, January 13). The highest values

Fig. 7. Spatial distribution of “psychrophilic” heterotrophic bacterial abundagray line: midnight).

were then observed in the coastal zone (except for thecoastal station that was closest to land). However oppositegradients were also observed (November 18 andDecember 30), and the concentrations were roughly lowand constant during winter.

Within a given transect, total bacterial abundancevaried less than 10 fold (Fig. 4). The maximum range ofvariation was observed in autumn (March 15). Totalbacterial abundance often decreased with distance fromthe coast (February 5, August 17 and November 18) butthis pattern was not consistent overall.

Leucine incorporation showed strong spatial variationduring the warmer periods (Fig. 5). More than tenfoldranges were observed (December 12, January 13,February 5 and November 18). Like for bacterial

nce in surface seawater of Morbihan Bay (thin black line: noon, thick


abundance, there was no clear general pattern. However,the greatest values were often observed in the coastalstation that was closest to land.

Within a given transect, psychrotrophic heterotrophicbacterial abundance sometimes varied more than 10 fold(Fig. 6).Despite the clear increasing gradient from the outerstations to the more coastal ones observed on February 5,like for other bacterial parameters, there were no generalpatterns in the spatial distribution. The spatial distributionsof the psychrophilic heterotrophic bacterial assemblage(Fig. 7) paralleled those of the psychrotrophic assemblage.

Fig. 8. Seasonal changes in chlorophyll a, total bacterial abundance, bacteroutside stations of Morbihan Bay, thick gray line: inside stations of Morbihainside stations of Recques Bay, open circles: outside stations of Table Bay,

3.2. Diel changes

In Morbihan Bay, chlorophyll a varied up to 2 fold(t, p=0.1) between night and day (Fig. 3, January 13and February 5), and phytoplankton biomass waslower during the night than during the day.

A comparison of noon and midnight data showedthat bacterial abundance tended to be higher during thenight than during the day (t, pb0.05) at all stationsduring summer transects (Fig. 4, December to Febru-ary). Bacterial abundance could be 2 times higher

ial production and heterotrophic bacterial abundance (thin black line:n Bay, open triangles: outside stations of Recques Bay, gray triangles:gray circles: inside stations of Table Bay).


(t, pb0.05) at midnight than at noon, as observed inDecember (December 12, 1998).

Except for the two transects conducted in December,leucine incorporation was conspicuously higher atmidnight than at noon (t, pb0.005) and could vary 5fold (t, pb0.05) between night and day (Fig. 5, May 13).

Differences of one order of magnitude between theabundance of the psychrophilic heterotrophic bacteriameasured during the night and the day were observed atsome stations (Fig. 7, December 12). The correspondingrange was only of 5 fold for less psychrophilic bacteria(Fig. 6). Despite this difference, there was a conspicuoussimilarity between the data obtained under the 2 differentincubation temperatures. There was no clear overarchingpattern. Heterotrophic bacterial abundance was some-times higher (t, pb0.01) during the day (April 12) and,at other times, during the night (June 12). The two datasets were merged to compute seasonal averages.

3.3. Seasonal changes

For each transect, we averaged data from the 3 mostcoastal stations (inside) and offshore stations (outside)in order to distinguish clear seasonal trends. Results areshown in Fig. 8.

Chlorophyll a showed clear seasonal variation withmaximal values occurring in the summer (January) andminimal values in winter. Chlorophyll a showed littlecontrast between coastal and offshore stations (ANOVA,p=0.17). In the coastal zone, total annual ranges were0.15±0.03/2.77±1.48 μg L−1 at noon and 0.11±0.08/1.38±0.47 μg L−1 at midnight. Corresponding valuesfor offshore stations were 0.18±0.04/1.15±0.47 μg L−1

at noon and 0.20±0.08/1.19±0.53 μg L−1 at midnight.In the coastal zone, chlorophyll a varied 18 fold at noonand only 6.6 fold at midnight, and was larger at noonthan at midnight (ANOVA, pb0.05). In contrast,chlorophyll a varied less than 6 fold in the offshorezone with no significant diel changes.

The seasonal pattern of bacterial production was rathersimilar to that of chlorophyll a, with maximal valuesoccurring in the summer andminimal values in the winter.In the coastal zone, total annual ranges were 44±17/394±156 ngCL−1 h−1 at noon and 82±29/648±209 ngCL−1

h−1 at midnight. Corresponding values were 27±15/307±30 at noon and 45±14/336±106 ng C L−1 h−1 atmidnight in the offshore zone. In Morbihan Bay,bacterial production was higher in the coastal zonethan offshore (ANOVA, pb0.05), and higher atmidnight than at noon (ANOVA, pb0.005).

The seasonal pattern of total bacterial abundance wasmore complex. A first maximum was observed in

January, and then minimal values were measured inlate summer (late January/February). A first increase wasobserved from February to June, followed by a smalldecrease in July and August. A second peak of abun-dance was observed in November. Total abundance washigher in the coastal zone than in the offshore zone(ANOVA, pb0.05). Total annual abundance ranged from1.8×105±7.3×104 to 2.4×106±2.5×105 cells mL−1 atnoon and from 4.4×105±1.0×105 to 1.7×106±3.1×105

cells mL−1 at midnight. Corresponding values in theoffshore zone ranged from 1.3×105 ±6.2×104 to1.4×106±3.2×105 at noon and from 2.0×105±4.2×104

to 1.8×106±1.0×104 cells mL−1 at midnight. Thus, totalbacterial abundance varied 13 fold at noon in the coastalzone and only 3.9 fold at midnight in the same area. In theoffshore zone, total bacterial abundance varied 11 fold atnoon and 10 fold at midnight.

The seasonal pattern of heterotrophic bacterialabundance differed greatly from that of temperature,chlorophyll a and bacterial production. Several smallgrowth phases could be distinguished. However,minimal values were generally observed in the summer,and maximal values in the winter. At noon, heterotro-phic bacterial abundance varied 16 fold in both coastaland offshore zones, while at midnight it varied 28 fold inthe coastal zone and 14 fold in the more offshore area.

4. Discussion

The highest chlorophyll a values observed during thesurvey (2.77 μg L−1) were lower than the values obtainedpreviously during spring blooms in a coastal station ofMorbihan bay (generally between 7 and 20 μg L−1, with amaximum around 50 μg L−1, Delille et al., 1996, 2000)but were of the samemagnitude as those observed aroundsub-Antarctic and Antarctic islands (Perissinotto et al.,1992; Whitehouse et al., 1993). In contrast, the datacollected from 1990 to 1994 at the Kerfix station locatedin the Indian sector of the Southern Ocean, southwest offKerguelen Archipelago, showed lower concentrations ofphytoplankton with a maximum of 1.2 μg L−1 (Fialaet al., 1998). In the present study, chlorophyll a varied 18fold between winter and summer. This seasonal range isfar below that observed in Antarctica by Anderson andRivkin (2001). They reported a 1000-fold increase ofchlorophyll a in McMurdo Sound between late Augustand early January. Even if our data correspond to meanvalues and thus might underestimate possible extremevariations, this observation highlights the differencesbetween Antarctic and sub-Antarctic conditions. Even ifthe maximum values of chlorophyll a concentrationsreported in McMurdo Sound (4 to 6 μg L−1) are higher


than the values observed around the Kerguelen Islandsduring this study, the major difference lies in the minimalvalues, which were much lower in Antarctica, probablydue to the sea-ice cover that is always absent in Kerguelenregion. Using an average C:chl a ratio of 35, the phyto-planktonic biomass ranges from 4 to 100 μg C L−1.However, C:chl a ratios between 40 (Li et al., 1993) and89 (Eppley et al., 1988) are commonly observed in open-sea environments (Pedros-Alio et al., 1999). If higher C:chl a ratios were used, phytoplankton biomass valueswould increase and bacterial to phytoplankton biomassratios would decrease accordingly.

In studies of carbon dynamics in aquatic microbialcommunities, the ability to convert bacterial abundanceto carbon is needed in order to calculate bacterialbiomass. Considering variability due to differences inbacterial species composition and bacterial growthconditions, it is not surprising to observe a widespectrum of conversion factors. As a consequence ofthe low correlation between carbon per cell and cellvolume, a constant cell mass would seem to be a logicalchoice in estimating bacterial biomass (Berger et al.,1995; Trousselier et al., 1997). Cell mass is, however,also subject to controversy. If, for some specific species,cell mass is quite constant during cell volume decreasesassociated with starvation (Trousselier et al., 1997), cellmass will remain dependent on cell volume for anassemblage of different species (Gazol et al., 1995;Pernthaler et al., 1996; Theil-Nielsen and Søndergaard,1998). Considering all available observations, theextreme values of bacterial cell mass will be in therange of 20 to 120 fg C celL-1. Using a median averagebacterial cell mass of 60 fg C celL-1 (Bjørsen, 1986;Trousselier et al., 1997; Delille, 2003), bacterial biomasswould range from 8 to 15 μg C L-1. This biomass isrelatively high compared to the data available for theopen Southern Ocean (Hodson et al., 1981; Cota et al.,1990; Goeyens et al., 1991; Delille, 1992, 2003), but isconsistent with the values reported in the BransfieldStrait (4 to 28 μg C L-1, Karl et al., 1991, 8 to 34 μg CL-1, Vosjan and Olanczuk-Neyman, 1991), the southernAntarctic Pacific zone (9 to 82 μg C L-1, Sazhin, 1993)and the Terre Adélie coastal area (1 to 30 μg C L-1,Delille, 1993). Despite the uncertainties related to theuse of questionable conversion factors, phytoplanktonicbiomass seems to dominate the bacterial biomass in thesurface coastal waters of the Kerguelen Archipelago.This is in contrast with the situation observed at Kerfixstation in the offshore waters south–west of thearchipelago, where bacterial biomass exceeds photo-trophic biomass (Delille, 2003). These results agree wellwith the review of Gazol et al. (1997) that reports that

open-ocean communities support significantly moreheterotrophic biomass in the upper layers than docoastal communities for a given autotrophic biomass.

Bacterial production is secondary production, or thesynthesis of bacterial biomass, primarily from organicprocessors with some inorganic nutrients. The net effectis to move organic matter from one pool to another(Ducklow, 2000). In the Antarctic polar frontal region,Simon et al. (2004) reported bacterial production valuesranging between 9 and 40 ng C L−1 h−1 during summerand autumn (December to May). The higher valuesobserved in the coastal zone of Kerguelen Archipelagocould be related to both a higher temperature and alarger availability of nutrients.

Salinity changes were too small to explain thedifferences observed in biological parameters. Manyother factors act to control bacterial activity, two of whichare temperature and substrate availability. The relativeimportance of these two factors is not well understood(Hoch and Kirchman, 1993). Substrate concentration andtemperature interact in all bacterial populations at alltemperatures and substrate concentrations (Pomeroy andWiebe, 2001). The majority of the Antarctic microbialcommunities are of psychrotolerant types, which are ableto grow at 0 °C though optimum temperatures are N20 °C(Delille and Perret, 1989); even the small proportion ofobligate psychrophiles have optimum temperaturesgreater than the environmental temperature. Loweredaffinity for substrates will limit growth at low tempera-tures (Nedwell, 1999). However, temperature has beenreported to have only a rather limited influence onAntarctic and sub-Antarctic bacterioplanktonic popula-tions (Delille et al., 1988; Vincent, 1988; Delille andPerret, 1989; Fukunaga and Russell, 1990; Vosjan andOlanczuk-Neyman, 1991; Nedwell and Rutter, 1994).The similarity between the distributions of psychrophilicand psychrotrophic heterotrophic bacteria observed in thepresent data set confirm this assumption. Importantregulating factors of the sub-Antarctic bacterial commu-nities are related to the available trophic sources (Delilleand Bouvy, 1989; Delille and Perret, 1991). The bacterialassemblage in the Kerguelen coastal area showed strongseasonality. Both abundance and production varied withtime but their variations were not parallel. Productionreached amaximum in January, when bacterial abundanceis at its lowest. In a temperate estuary, Coffin and Sharp(1987) observed that while bacterial production remainedhigh over the summer months, bacterial abundance waskept low by microflagellate grazing. In the Arctic Ocean,Anderson and Rivkin (2001) reported that even if grazinglosses of bacteria were insignificant immediately beforeand after the phytoplankton bloom, microzooplankton


could consume 90% of local bacterial production.Seasonal variability could include periods of top-downand periods of bottom-up regulation (Gazol, 1994).Bacterivorous communities were not quantified in thisstudy, but they may have contributed to the low summerbacterial abundance. In addition to grazing, the reducedrates of fall bacterial production may result frombacterioplankton having consumed enough of the avail-able organic carbon to become substrate limited.Heterotrophic bacterial abundance is only representativeof culturable bacteria, though it is a useful bacterialindicator corresponding to a small group of active bacteriathat react immediately to the changes in their nutrientsupply (Delille and Bouvy, 1989; Rheinheimer et al.,1989). The large development of heterotrophic assem-blages during autumn and winter observed in the presentstudy is thus a clear indication of the availability oforganic substrates. Temperature is probably the mostimportant factor regulating bacterial production duringthis period.

In contrast, the diel variations of temperature werecertainly too small to explain the corresponding changesof bacterial biomass and production. Diel verticalmigration of zooplankton has been reported in numer-ous areas of the ocean, and such migration could have animpact on bacterivory. Algal metabolism (phytoplankonor macroalgae) obviously change between day and night(Mague et al., 1980). Variation in DOC excretion ratemust play an important regulating role in the dielvariation of bacterial parameters. Diel variability of thegrowth of heterotrophic planktonic bacteria has beenpreviously related to changes in phytoplankton andzooplankton activity (Riemann and Søndergaard, 1984;Wheeler et al., 1989; Delille et al., 1997). No consistentpattern in the diel bacterial activity, however, wasobserved in these studies. This holds true in the presentstudy. This is presumably due to the fact that relation-ships between diel changes of phytoplankton, zooplank-ton and bacterioplankton activity are intricate and differbetween aquatic environments. Short-term changes inbacterial abundance might be explained by a tightcoupling to photosynthetic processes as well as bychanges of water masses. Advection during diurnalcycles is a possible explanation for bacterial variability(Karner and Rassoulzadegan, 1995; Delille et al., 1997).

Concentrations of particulate and dissolved organiccarbon vary spatially. This variation is driven by theinputs from both plankton and terrestrial sources.Plankton-derived organic matter is enriched in proteinand labile polysaccharides, whereas terrestrial organicmatter contains humic material and structural polysac-charides, such as cellulose and lignin, which are

relatively resistant to mineralization by microbialprocesses (Delille and Perret, 1991; Benner, 2002).Terrestrial material does not play a major role because ofthe complex detrital processing cycle that would largelydissipate the carbon and energy (Peterson et al., 1994)The abundance and composition of POM and DOMcould have short-term impacts on bacterial metabolism.Rates of constitutive enzymes can respond quite rapidly,on the order of minutes to hours, whereas days may berequired for a rare ribotype to increase sufficiently inabundance in order to significantly affect DOMmineralization at the community level (Findlay, 2003).Between these two extremes, the induction andsynthesis of new enzymes occurs within hours (Kirch-man et al., 2004). The response of bacteria tophytoplankton or any other organic matter availabilitychanges is not instantaneous; rather, bacterial activity isdependent upon previous activity of phytoplankton orallochtonous organic inputs. The monthly samplingregime used in the present study would be thereforeinsufficient to capture all the relationships betweenbacteria and their trophic sources. Indeed, even a weeklysampling regime might be insufficient to capture all therelationships between phytoplankton and bacteria (Star-oscik and Smith, 2004).

5. Conclusion

Temperature variations are larger in sub-Antarcticcoastal area than in the surrounding open oceanic zone,with obvious consequences on the microbial loop. Incontrast, the range of seasonal variations of phytoplank-ton is smaller in the sub-Antarctic coastal area than inthe Antarctic one. This is probably related to the absenceof ice cover. In Kerguelen fjords, low winter tempera-ture seems to limit bacterial production and, to a lesserextent, bacterial abundance.

Changes in bacterial abundance are not necessarilyrelated to changes in bacterial growth (Billen et al.,1990). Steady-state abundance is the balance betweengrowth and mortality; hence, the loss rates due tobacterivory and viral lysis must be similar to cellgrowth. Even a small imbalance may result in largeoscillations in bacterial populations (Anderson andRivkin, 2001). Short-term changes could be as large aslong term seasonal changes, and interactive effects oftemperature and substrate supply could occur (Pomeroyand Wiebe, 2001). The data available do not allow us todecipher the main regulating factor. It is therefore likelythat grazing, viral lysis, substrate availability andtemperature adaptation all play a role in the regulationof bacterial communities.


Acknowledgements

We are indebted to the efficient and enthusiastic helpof the captains and crew members of the R.V. LaCurieuse. This research was supported by the “InstitutFrançais pour la Recherche et la Technologie Polaires”and the Belgian Science Policy (contract A4/DD/B14,EV/7/12E, SD/CA/03A). This is MARE contributionno. 108.

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Spatial and temporal variation of bacterioplankton in a ... · Daniel Delillea,⁎, Fabien Gleizona, Bruno Delilleb a Observatoire Océanologique de Banyuls, ... (seven stations each).

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