AQUATIC MICROBIAL ECOLOGY Vol. 12: 263-273, 1997 1 Published May 29 Aquat Microb Ecol l
Trophic interactions between picophytoplankton and micro- and nanozooplankton in the western Arabian Sea during the NE monsoon 1993
Marcus Reckermannl,*, Marcel J. W. veldhuis2
'Institut fur Ostseeforschung. Seestr. 15, D-18119 Warnemunde, Germany '~nstituut voor Onderzoek der Zee. Postbus 59,1790 AB Den Burg. The Netherlands
ABSTRACT: The grazing pressure of micro- and nanozooplankton on phytoplankton was estimated in serial dilution experiments in the northwestern Arabian Sea and its adjacent areas (the Somali Current, the Somali Basin, the Gulf of Aden and the southern Red Sea) during the NE monsoon 1992-1993. Microzooplankton grazing rates @) on total phytoplankton (analyzed as chl a)were generally exceeded by phytoplankton growth rates (g = 0.2 to 1.19 d-l, mean 0.48 d-'; p = 0.52 to 1.12 d-', mean 0.72 d-'1, resulting in an average daily consumption of 38% of the phytoplankton standing stock and 67% of the primary production. Microzooplankton grazing on 4 picophytoplankton groups (Prochlorococcus spp., Synechococcus spp., and 2 picoeukaryotes) analyzed by flow cytonletry showed growth (p = 0.27 to 0.92 d-l, mean 0.68 d") and grazing mortality rates @= 0.26 to 0.73 d-l, mean 0.67 d-l) well in balance, with an average of 49% of the standing stock and 102% of the primary production grazed per day. Pico- phytoplankton growth and grazing mortality rates increased dramatically when grazers >l0 pm were removed. These results suggest a control of the small grazers by larger ones (trophic cascade) and a close coupling between picoautotrophic prey and small grazers. The trophic cascade within the micro- bial food web of the nanoplankton encompasses 3 trophic levels: picoplankton - small HNF - larger flagellates and ciliates.
KEY WORDS: Grazing . Picophytoplankton . Prochlorococcus . Synechococcus . Picoeukaryotes Flow cytometry . Arabian Sea . Trophic cascade
INTRODUCTION rates is essential. Knowledge of the size of the principal predators of picoplankton is important as well, as size Photoautotrophic picoplankton (size 0.2 to 2 pm) largely determines the fraction of carbon which is often dominates the phytoplankton community within passed on to higher trophic levels (Sherr et al. 1986). the euphotic zone of oligotrophic oceans (Campbell & Grazing can be assumed to be the most significant loss Vaulot 1993, Fogg 1995), and particularly so during the factor for these organisms, as direct sedimentation is inter-monsoon periods in the Arabian Sea (Burkill et al. unlikely due to their small size, although they may 1993, Jochem 1995). The prokaryotic species Pro- form a significant component in sinking aggregates chlorococcusmarina (Chisholm et al. 1992) and Syne- (Lochte & Turley 1988). Prochlorococcus,reaching chococcusspp. (Johnson & Sieburth 1979, Waterbury abundances of up to 350 000 cm-3 in the euphotic zone et al. 1979), as well as eukaryotic algae of various tax- of oligotrophic regions (Olson et al. 1990, Veldhuis & onomic groups (Johnson & Sieburth 1982, Simon et al. Kraay 1993, Lindell & Post 1995, Buck et al. 1996), can- 1994) are the predominant autotrophs within this size not be discriminated reliably from heterotrophic bacte- class. In order to assess their role in oceanic carbon ria by epifluorescence microscopy, due to their dim flux, information on their growth and grazing mortality and fast-fading autofluorescence (Monger & Landry 1993), and many have been mistakenly counted as 'Present address: Forschungs- und Technologiezentrum West- heterotrophic bacteria for that reason (Campbell et al. kiiste, Hafentorn, D-25761 Biisum, Germany. 1994, Sieracki et al. 1995). Although the occurrence of E-mail: [email protected] Prochlorococcuswas shown in the NW Indian Ocean
O Inter-Research 1997 Aquat Microb Ecol 12: 263-273, 1997
(Pollehne et al. 1993, Veldhuis & Kraay 1993, Jochem 60 E 1995), information on the dynamics of these tiny pri- N mary producers has been scarce. To date, information on Prochlorococcus growth rates is available only from the Sargasso Sea (Goericke & Welschmeyer 1993) and ,, the equatorial Pacific (Vaulot et al. 1995); grazing esti- mates have been reported only from the equatorial Pacific (Landry et al. 1995a, b). Information on eukary- otic picoplankton dynamics is also rare. For Syne- chococcus, Burkill et al. (1993) reported high bio- masses and turnover rates in the Arabian Sea during the autumn inter-monsoon period. 10 We report here specific phytoplankton growth and grazing mortality rates by microzooplankton (measured as bulk chl a and as separate picoautotrophic groups by iivw cyiu111et1y: Pruciiiur-ucuccus, Syr~ec'i~ucocc~ls,2 picoeukaryotes, and occasionally 2 sub-populations of Prochlorococcus and Synechococcus) at different loca- SOMALI BA~~~ tions in the Somali Current, the Gulf of Aden, and the o southern Red Sea during the NE monsoon period (January-February 1993). The standard dilution proto- col of Landry & Hassett (1982) was modified in order to S
account for the respective grazing impact of different 40 W 60 E grazer size within the microzoo~lankton Fig, 1, Investigation area with in the Somali Current, munity (grazers c 20, < 10, c 3 and < 2 pm). the Gulf of Aden and the southern Red Sea. Arrows indicate the direction of the Somali Current during the NE rnonsoon
MATERIAL AND METHODS water (prepared by sterile, preflushed 0.2 pm filter Micro- and nanozooplankton grazing experiments capsules; Nalgene) to give 4 dilution steps (100, 75, (Landry & Hassett 1982) were carried out aboard RV 50 and 25% original water) and incubated on board 'Tyro' on cruise B2 of the Netherlands Indlan Ocean in 5 1 glass bottles for 24 h, starting at sunrise. In situ Programme 1992-1993 (Baars et al. 1994) at 8 stations condltlons were simulated in a light-screened flow- in the Arabian Sea off Somalia, in the Gulf of Aden through bath which ensured mixed layer tempera- and the Red Sea (Fig. 1) during the NE monsoon tures and irradiances corresponding to the sampling (January-February 1993). Water samples were taken depths (Table 1).For chl a analyses, samples (1 to from the upper mixed layer (10 to 30 m) on the 2.5 1) were filtered over a GF/F glass fibre filter uphaul with a Seabird CTD rosette water sampler (47 mm; Whatman) at the beginning and at the end of equipped with 10.5 1 NoEx bottles. Water samples each respective experiment. Filters were stored at were prescreened through a 200 pm mesh (to remove -80°C until fluorometric analysis according to Veld- mesozooplankton) and diluted with particle-free sea- huis et al. (1993).
Table 1 Locations, dates and ambient environmental conditions for the experiments in the Somali Basin (SB2 to SI), the Gulf of Aden (GA1, GA2) and the southern Red Sea (RS1, RS2) during the NE rnonsoon 1993. FC: flow cytometry
Expt Phytoplankton Stn Date Simulated incubation Temperature NO, Chl a analyzed by (1993) depth (m) ("c) (l.lM) (pgdm 'I
1 chl a, FC SB2 (809-1) Jan 15 20 26 9 0 13 0 35 2 chl a, FC US1 (813-1) Jan 18 20 26.7 0.23 0.28 3 chl a, FC US2 (818-5) Jan 21 20 26.0 0.80 0.30 4 chl a, FC S1 (820-1) Jan 24 20 26.0 0.93 0.25 5 chl a GA1 (826-4) Jan 26 20 25 9 0.30 0 50 6 chl a, FC GA2 (832-11) Jan 30 20 25.4 1.53 0 46 7 chl a RSI (840-4) Feb 02 10 25.7 0.02 0.95 8 chl a, FC RS2 (842-14) Feb 04 10 25.8 0.40 1.04 Reckermann & Veldhuis: Trophic interact~onsarnong plankton
In parallel treatments, the standard serial dilution of the respective picophytoplankton group (filters in protocol was modified to the effect that in addition to the range of 8 to 0.45 pm pore size were used). Using a grazers > 200 pm, also grazers > 20, > 10, >3 and > 2 pm volume-to-carbon factor of 220 fg C pm-"Booth et al. were removed by prescreening in order to determine 1988),and depending on the variation in scatter signals, the respective grazing pressure of smaller grazer size a carbon content of 975 (Stn SB2), 1880 (Stn US1) classes on the picoautotroph community. The experi- and 2500 fg C cell-' (other stations) was assumed for mental water was siphoned from the CTD bottle into a the small picoeukaryotes, and 5090 fg C cell.' for the light-screened 2 l plastic beaker by means of a sub- large plcoeukaryotes. merged silicon tube. The water was prescreened by gravity through meshes (for the size fractions c20 and
Table 2 Cell concentrations (cells cm-3) of photosynthetic picoplankton at the beginning of the experiments analyzed by flow cytometry. ' Prochlorococcusnot analyzed, -: not detected
I Expt Stn ProchlorococcusDim Bright SynechococcusDim Br~ght Small euks Ldryeeuks
Table 3. Results of chl a-based dilution grazing experiments (representing phytoplankton growth rates in the micro- the total phytoplankton population). Growth and grazing coefficients zooplankton grazing treatments also derived from dilution plots (apparent growth rate vs dllution factor) accord- showed 1 division d-l on average (p= 0.67); ing to Landry & Hassett (1982). Consumption rates calculated according to Frost (1972).ns: linear regressions of dilution plots not significant (p > U.ir5) h~l~~ller,picoph ytoplankton qrazing mor- tality rates caused by microzooplankton were in the same range, resulting in a quasi- Stn Growth Grazlng Consumption of (l) g (d-l) Chl a Carbon steady-state system with grazing losses (mg m-3 d-l) (mg m-3 d-l) compensated by growth (filled circles in Fig. 2, Table 5). SB2 0.653 0.192 0.07 14.16 0.442 12 ns Total phytoplankton carbon consump- US1 0.595 0.042 0.02 3.22 0.076 12 ns US2 0.520 0 201 0.08 15.33 0.630 12 <0.05 tion rates by microzooplankton increased S1 0.928 0.503 0.18 34.69 0.729 12 <0.01 from the Somali Basin (US2 and SI) towards the Gulf of Aden (GA2) and the 12 <0.01 12 <0.01 southern Red Sea (RSI and RS2; Table 3). 12 <0.01 There, carbon consumption by microzoo- plankton was highest (148 mg m-3 d-' at I RS1). Picophytoplankton carbon con- the southern Red Sea (RS2), a highly diverse phyto- sumption was relatively conservative throughout the plankton community was found, consisting of large cruise and made up total phytoplankton consumption diatoms (Chaetoceros, Nitzschia, Coscinodiscus, Bid- in the Somali Basin (Fig. 3A; US2 and SI). However, in dulph~a),dinoflagellates (Gymnodinium and Amphi-
dinium) and cryptophytes, as well as Phaeocystis-type Sedy Slate Lire colonies. / / Ir=g 2.0 ' Gr- SueClasses F- - X / e~m(~.a)1 Phytoplankton growth and grazing mortality by '0 - am microzooplankton m / / /a 81.5 - *(+ / O <2$m ++ + Table 4. As Table 3, but for picophytoplankton andlyzed by flow cytometry in slze-fractionation experiments. Results of exper- iments involving grazers c2 pm not shown (ns) Stn Growth Grazing Consumption of r n v (d '1 g (d '1 Cells (no,cm-.' d.') Carbon [mym-:' d.') Grazers c200 pm P~O~J/OI'OCOCC~/~ IJS2 GA2 Synechococcus SB2 us1 US2 GA2 RS2 Small picoeukaryotes SB2 US1 US2 GA2 Large picoeukaryotes GA2 RS2 Grazers c20 pm Prochlorococcus us2 GA2 Synechococcus US2 GA2 Small picoeukaryotes US2 GA2 Large picoeukaryotes GA2 Grazers c10 pm Prochlorococcus US2 S I GA 2 Synechococcus us2 S1 GA2 Small picoeukaryotes us2 SI GA2 Large picoeukaryotes S1 Grazers c3 pm Proch1orococcus US2 S1 GA2 Synechococcus US2 S1 GA2 Small picoeukaryotes US2 S1 GA2 Large picoeukaryotes S1 Reckermann & Veldhuls: Trophic interactions among plankton 269 Picophytoplankton growth and grazing mortality by Steady State Lne nanozooplankton / /)1=9 eclo~m/ Removal of the microzooplankton and larger nanozooplankton (10 to 200 pm) from the incubation water resulted in a considerable increase of grazing pressure on the autotrophic picoplankton (Figs. 2 & 4, Table 4). In the samples containing the entire nano- (c20 pm) and microzooplankton (c200 pm), rates for all picoplankton groups were much lower and in the similar range as for chl a (Fig 2). Hence, the larger microzooplankton obviously exerted a strong control over first-order consumers of the picoplankton, there- by relieving the picoplankton from being grazed. As an average over all stations and picophytoplankton % groups, grazers cl0 and c3 pm consumed 78 and 73 0.0 0.5 1.O 1.5 2.0 2.5 of the picoautotrophic standing stock d-l, and 131 and Specific Grawth Rate p (d .l) 115% of picoautotrophic production d-l, respectively (Table 5). The prokaryotic genera Proch1orococcusand Fig. 5. As Fig. 2, for 2 Prochlorococcus and Synechococcus sub-populations ('dim' and 'bright' types). Respective grazer Synechococcus,as well as the small eukaryotic picoau- size classes are indicated for each data point (only data at totrophs, experienced the highest growth and grazing p 5 0.05 plotted) mortality rates in the small size fractions observations demonstrating Prochlorococcus to be a dances typical for oligotrophic conditions (up to true open-ocean organism, largely restricted to oligo- 350000 cm-3; e.g. Campbell & Vaulot 1993, More1 et trophic warm stratified waters (Lindell & Post 1995, al. 1993, Lindell & Post 1995, Buck et al. 1996), the Suzuki et al. 1995, Buck et al. 1996). However, hardly nutritional importance of Prochlorococcus lliigllt be any rate estimates have been published for Prochloro- equal to, or even higher than, that of Synechococcus coccus. Goericke & Welschmeyer (1993) found rela- or the picoeukaryotes. tively low growth rates in the Sargasso Sea (below 1 The sue-fractionation experiments suggest that division d-l), while Vaulot et al. (1995) report on divi- small heterotrophic nanoflagellates (HNF) are the sion rates of 1 d-' in the surface layer of the equatorial main consumers of Prochlorococcus, Synechococcus Pacific. Growth and grazing estimates from the same and picoeukaryotes in the Arabian Sea. Epifluores- region are presented by Landry et al. (1995a, b): in cence analysis revealed that the vast majority of HNF their experiments, Prochlorococcus grazing mortality (>go%) was smaller than 3 pm, with the biomass peak considerably exceeded specific growth rates, which still within the <5 pm size range (data not shown). were extraordinarily low (mostly p = 0 to 0.26 d-l). The Small HNF are known to be mainly responsible for existence of 2 different strains of Prochlorococcus had the removal of heterotrophic bacteria (e.g. Fenchel vccll demons:ratcd zzrr!iz: in the subtropical r\lort.h. 1986): h~~tare also able to consume coccoid cyanobac- Atlantic on the basis of pigment types (Goericke & teria in sitv (Caron et al. 1991). Parslow et al. (1986) Repeta 1993) and different chlorophyll and DNA con- reported that the small HNF Pseudobodo (2 X 4 pm) is tents at the HOT site (Hawaii, subtropical North capable of rapidly reproducing on the picoeukaryotic Pacific; Campbell & Vaulot 1993). The data presented alga Micromonas pusilla (1 to 2 pm) as sole food here suggest that the 2 sub-populations also may ex- source. Calculations assuming HNF to be the only perience different growth characteristics, with an consumers of picoautotroph carbon imply that they apparently healthy growing population ('dim') and a could well be able to satisfy their daily carbon hardly active one ('bright'; Fig. 5). demand exclusively from this source (up to 1200% of Phytoplankton grazing estimates from the Arabian their own body carbon consumed d-'; Table 6: daily Sea have been reported so far only by Burkill et al. ration). Although this assumption is a simplification (1993). During the autumn inter-monsoon period, (larger protozoa will probably contribute to the they found Synechococcus to be a highly abundant removal of picoautotroph carbon to a certain extent, and dynamic component of the food web, with and heterotrophic bacteria will still be a major diet for growth and grazing mortality well in balance. Syne- HNF), it nevertheless shows that c3 pm HNF may chococcus was the dominant picoautotroph during apply a vigorous grazing pressure on picophytoplank- our investigations in terms of cell numbers, but the ton. There is also direct microscopical evidence for picoeukaryotes, due to their larger size, dominated in the ingestion of autotrophic picoplankton by HNF: a terms of carbon biomass. They were the most impor- large number of HNF <3 pm contained 1 or 2 whole tant picoautotrophic carbon source for the microzoo- or partly digested Synechococcus cells, which can be plankton (Fig. 3B). Prochlorococcus was less abun- identified reliably by their bright yellow autofluores- dant by a factor of 4 during the NE monsoon (up to cence under blue excitation. Although some dino- 66000 cm-" than during the spring inter-monsoon flagellates also contained Synechococcus cells, their (up to 276000 cm-3; Veldhuis & Kraay 1993), so its frequency was much lower than the Synechococcus- contribution to micro- and nanozooplankton diet was containing HNF. Ciliates containing Synechococcus rath.er low during this season. However, at abun- cells were not detected. Table 6. Absolute picophytoplankton carbon consumption rates as the sum of all picophytoplankton groups in the <200 pm fractions (SI: Stn P~cophytoplankton HNF Total protozoa consumption C biomass Daily ration C biomass Daily ration (mg m- ' d.') (mg m--') of HNF (%) (mgm-?) of protozoa ('X,) US2 12.68 2.98 4 26 4.84 262 S1 25.08 2.12 1183 4.59 546 GA2 26.33 2.92 902 4 61 571 RS2 5.63 1.90 296 7.18 78 Keckermann & Veldhuis: Trophic interactions among plankton Multiple trophic interactions within the microbial assume that the increased grazing rates are sympto- food web matic of an increased grazer biomass, it is possible to roughly estimate grazer growth and predation mortal- The number of trophic levels within the micro- ity rates from the size-fractionated experiments. It can zooplankton comnlunity and the size of the pr~ncipal then be estimated that grazers c10 pm more than grazers of picoplankton are important variables when doubled their biomass within 1 d when predators estimating carbon flux in picoplankton-dominated sys- >l0 pm were removed (increase of 124'%,;Table 5), tems. Eukaryotic and prokaryotic bacterivores have which is a realistic figure (see above). When these been found in the bacterial size class, i.e. 0.2 to 2 pm results are extrapolated to field conditions, this means (Fuhrman & McManus 1984, Guerrero et al. 1986). that small HNF, like their prey, divide once a day, and Wikner & Hagstrom (1988) presented experimental are removed by their predators at a similar rate. This is evidence for the existence of 4 trophic levels in the size a strong indication for the presence of a trophic cas- class 112 pm, with the primary bacterivores being cade encompassing at least 3 trophic levels within the smaller than 3 pm and controlled by the larger proto- nanoplankton: picoautotrophs - small HNF - larger zoa. Glibert et al. (1992) found a similar effect in size- protozoa. fractionated grazing and NH,' regeneration ex- In our experiments, the picophytoplankton also periments in Chesapeake Bay (USA) waters. When increased their specific growth rates when they were organisms >l0 pm were removed from their incuba- exposed to an increased grazing pressure (on average tion~,ammonium regeneration rates increased signifi- by 75 %, in the of these first-order consumers indicate that this amount web of the northwest Indian Ocean. Deep Sea Res I1 40: of picoplanktonic primary production reaching higher 773-782 Campbell L, Nolla HA, Vaulot D (1994) The importance of trophic levels will be smaller than in systems with Prochlorococcrr.~to community structure In the central larger herbivores. In such a system, where tiny primary North Pacific Ocean. Limnol Oceanogr 39(4):954-961 producers (closely coupled to their grazers) represent Campbell L, Vaulot D (1993) Photosynthet~cpicoplankton the major fraction of primary production, recycling of community structure in the subtropical North Pacific nutrients and respiration within the euphot~czone will Ocean near Hawaii (station ALOHA). 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