NOTES. Sources and fate of dissolved free amino acids in epilimnetic Lake Michigan water 1
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1 NOTES Limnol. Oceanog., 32(6), 1987, , by the Ameican Society of Limnology and Oceanogaphy, nc. Souces and fate of dissolved fee amino acids in epilimnetic Lake Michigan wate 1 The impotance of the micobial food web to enegy flow and nutient cycling pocesses in pelagic zones of lakes and othe aquatic systems is widely ecognized (e.g. She et al. 1983; Siebuth 1984; Caon et al. 1985; Fahnenstiel et al. 1986; Stockne and Antia 1986) but details of nutient tansfomations by the vaious components of the food web ae still unclea. Modes of tansfe of photosynthesized nutients fom phytoplankton to fee-living bacteia (Azam and Ammeman 1984; Cole et al. 1982; Coveney 1982) and othe heteotophs and the elative impotance of the vaious heteotophs in making inoganic nutients available to phytoplankton ae only patially undestood. Release ates of specific classes of labile mateials (e.g. amino acids, oganic acids, and cabohydates) must be detemined to assess the impotance of these compounds in the link between autotophic and heteo- GLERL Contibution tophic poduction. Release ates ae difficult to measue because bacteia tend to emove labile compounds at about the ate that they ae nomally supplied (tuiaga and Zsolnay 1983). Thus, although concentations of these compounds may be low o undetectable in natual wates, thei flux may be significant (Fuhman 1987). Fo example, qualitative changes in the C : N atios of dissolved fee amino acids (DFAA) in the Noth Sea duing a phytoplankton bloom indicated a geate DFAA tunove than was suggested fom the examination of tends in DFAA concentation pattens alone (Hamme and Kattne 1986). Diffeentiation of nutient poduction fom uptake pocesses in the micobial food web depends on sepaating the effects of pimay poduction fom those of minealization without substantially affecting community dynamics (tuiaga and Zsolnay 198 1). Diffeential filtation is not completely satisfactoy because the two goups often ovelap in size (Fuhman and Mc- Manus 1984; Rassoulzadegan and Sheldon 1986) some oganisms function as mixotophs (Bid and Kalff 1986), and indiect inteactions between autotophs and heteotophs (e.g. nutient exchange) may be modified by physically sepaating the goups (She et al. 1986). Selective inhibition by antibiotics can cause patial lysis of affected oganisms (She et al. 1986) and may have side effects on nontaget oganisms (Jensen 1983, 1984). These poblems have ecently been avoided in measuements of amino acid uptake and elease in seawate by using isotope dilution techniques in conjunction with high pefomance liquid chomatogaphy (Fuhman 1987). Compaative kinetic studies of natual and added concentations of amino acids and ammonium in lake wate held in dak and light/dak bottles offe anothe ap-
2 1354 Notes Table 1. s of amino acid elease (ng-atoms N lite h-l) by phytoplankton in epilimnetic wate of Lake Michigan sampled duing s of pimay amine elease wee calculated as diffeences in pimay amine concentations between light and dak bottles ove time afte addition of an amino acid mixtue (0.94 PM) to each to satuate micobial uptake sites (except fo the sample of 23 Apil that had a high initial concentation of pimay amines). Amino acid concentations wee assumed to be 1.46 times PA concentations. Numbe of data sets compaed pe egession--n; coelation coefficient--. Data fo the 9 July wate sample (23 C) wee not collected fequently enough fo accuate calculation of PA emoval ates and ae not pesented Temp ( 0 n Unteated 1 /AM NH, addltlon 3-pm filtate 0.8-pm filtate 23 Ap May May Jun Jul Aug oo Sep Nov peach to examine autotophic-heteotophic inteactions with espect to dissolved nitogen compounds. n this pape, we chemically examine poduction and uptake of dissolved nitogen (ammonium and amino acids) ove seveal days in bottles of unfotified and amino acid-fotified epilimnetic Lake Michigan wate and examine the fate (food-web biomass vs. minealization) of DFAA nitogen. Lake Michigan povides an inteesting envionment in which to examine these phenomena, compaed to maine and eutophic lake systems, because it is a elatively oligotophic system whee the phytoplankton ae not unde nitogen limitation. We thank G. Fahnenstiel fo helpful suggestions; J. Malczyk fo technical assistance; W. Buns, J. Gimes, and D. Mose fo help in collecting wate samples; and G. Fahnenstiel, C. Paish, D. Scavia, and H. Vandeploeg fo eviewing the manuscipt. Epilimnetic wate was collected fom a depth of 3-4 m by Niskin bottle at a 45-mdeep station, offshoe fom Gand Haven, Michigan, peiodically between Apil and Novembe The lake wate was placed in clean LPE jugs and stoed at appoximately in situ tempeatues (Table 1). Expeiments wee begun within 24 h of sample collection. Subsamples of lake wate wee peseved with Lugol s solution on most sampling dates fo late pepaation of phytoplankton slides (Dozie and Richeson 1975). Fo the June sample, the contents of the light and dak bottles of unfilteed lake wate (see below) wee also peseved and examined fo phytoplankton content at the end of a 13-d incubation fo compaison with the initial sample. Samples fo bacteial counts wee peseved at the beginning and end of expeiments with - 1% Fomalin. Bacteial abundance was detemined by the acidine oange diect-count method (Hobbie et al. 1977). Fo each lightdak expeiment, eplicate 70-ml potions of lake wate wee subjected to a seies of peteatments, including ammonium addition (1 PM) and filtation though 0.8- and 3-.Ln poe-size filtes, and poued into steile 70-ml tissue cultue bottles (Coning tissue cultue flasks, 25 cm2 size). The 0.8~pm poe-size filtes wee Gelman Meticel membane filtes (Pod. No ) (Apil and May) o Nuclepoe polycabonate filtes (SN ) (June though Novembe). The 3-pm filtes wee Nuclepoe Memba-Fil membane filtes (SN ) (Apil to August) o Nuclepoe polycabonate filtes (SN ) (Septembe to Novembe). Samples wee filteed diectly into the tissue cultue bottles with a clean 60-ml syinge attached to a clean 25- mm-diamete filte holde. The fist 40 ml of sample filtate was discaded to pevent contamination fom the filtation appaatus. Compaison of unteated and pefilteed samples indicated that filtation had no effect on concentations of measuable pimay amines o ammonium in the wate. Two of the fou bottles fom each teatment wee fotified with an amino acid mix-
3 Notes 1355 tue containing 3.75 nmol each of NH,+ and the following amino acids: L-alanine, L-aginine, L-aspatic acid, L-glutamic acid, L-glycine, L-histidine, L-isoleucine, L-leucine, L-lysine, L-methionine, L-phenylalanine, L-poline, L-seine, L-theonine, L-tyosine, L-valine, and 1.87 nmol of L-cystine in 0.1 M HCl (mixtue AA-S-l 8, Sigma Chemical Co.). t esulted in a total addition of 0.94 pmol amino acid (0.64 pmol of measuable pimay amines) pe lite of lake wate. This concentation, chosen to satuate micobial uptake sites, was based on pevious data on Lake Michigan wate (Gadne et al. 1986). One bottle of each teatment was incubated in the dak (dak bottle) at in situ tempeatue; the othe bottle (light bottle) was held unde 12 : 12 L/D conditions. Each teatment bottle was gently mixed at l-3-d intevals and a l-ml sample was emoved (with a peinsed needle and syinge) and analyzed fo ammonium and pimay amines (PA) by a peviously descibed technique fo sampling and disceteinjection liquid Chomatogaphic measuement (Gadne et al. 1986). PA is defined as being amino acids (and possibly othe pimay amines) less basic than ammonium that fom fluoescent deivatives with o-phthalaldehyde. n this technique, a wate sample is filteed (Gadne and Vandeploeg 1982) and injected diectly into a Chomatogaphic analyze that sepaates the PA (as a goup) fom ammonium and quantifies both peaks as fluoescent deivatives of o-phthalaldehyde (OPA; Gadne 1978; Gadne and Mille 198 1). Concentations of total amino acid nitogen wee calculated fom measuements of PA nitogen with a facto of 1.46 to account fo amino acids not measued by the Chomatogaphic technique. This facto was the mola atio of amino acid nitogen in the added mixtue to the nitogen in the OPA-fluoescing amino acid peak that eluted befoe ammonium on the analyze (Gadne et al. 1986). Fo calculations of unknown amino acids eleased by phytoplankton, we abitaily assumed that the atio of PA to DFAA in the samples was the same as in the standad mixtue. Amino acid elease ates wee estimated fom the linea least-squaes slope of (1.46) x (PA, - PA,) vs. time (whee 1.46 is the convesion facto and PA, and PA, ae PA concentations in coesponding light and dak bottles). Dak-bottle concentations wee subtacted fom light-bottle concentations at each sampling point to coect both fo micobial uptake of amino acids and fo possible autolytic elease of amino acids caused by phytoplankton death due to containment. The slopes wee calculated fo the peiod beginning when the light-bottle and dak-bottle cuves began to divege (l- 3 d afte incubations began) and ending eithe when the expeiment was stopped o when PA concentations in one of the bottles eached backgound levels. Phytoplankton composition at the study site befoe expeimentation exhibited typical (Fahnenstiel and Scavia 1987b) seasonal vaiation. The sping phytoplankton assemblage was dominated by diatoms and cyptophytes. Duing themal statification, cyptophytes, blue-geen algae, and smalle unidentified flagellates became moe abundant, while diatom numbes declined. Duing fall isothemal conditions, the assemblage was again dominated by cyptophytes and seveal species of diatoms. Results fom extended bottle expeiments cannot be diectly extapolated to natual conditions because phytoplankton (and othe oganisms) can change in quantity and composition duing containment (Venick et al. 1977). We examined phytoplankton changes in the 9 June expeiment. The contents of the light and dak bottles of unfilteed lake wate wee peseved and examined fo phytoplankton content at the end of the 13-d incubation and compaed to esults fo the initial wate sample. ncubation in the 70-ml tissue-cultue bottles unde dak and light/dak conditions had discenible effects on phytoplankton biomass and composition. Befoe incubation, the lake wate had a typical (Fahnenstiel and Scavia 1987b) sping phytoplankton composition assemblage dominated by cyptomonads (48.2%) and diatoms (39.8%). The total phytoplankton cabon content in the oiginal sample was 9 1 mg C m-3. Afte the 13-d incubation, the phytoplankton biomass in the dak wate sample deceased to 65 mg C m-3 and was dominated by diatoms (56.1 O/o), cyptomonads (24.4%) and
4 1356 Notes 7 May (a) Unteated (b) + AA NH,+, D-w----- // P- 1 (d) + NH; + AA a> E2 8 (e) O.&pm Filteed (f) O.&pm Filteed + AA 0 -*-_ ---_- - _ o p +- =e- 2 NH;, LD,--& a PA, L, D- 1 (g) 3-pm Filteed (h) 3-pm Filteed + AA 1 l- Time (days) FG. 1. Pattens of ammonium and pimay amine concentations vs. time in 12 : 12 L/D and dak bottles of Lake Michigan wate sampled on 7 May 1986 and held in 70-ml tissue cultue bottles at in situ tempeatue of 7 C fo 14 d. Ammonium chloide (1 PM) was added to the bottles labeled + NHq+. Dissolved fee amino acids (0.94 PM) wee added to the + AA teatments. PA-Opeationally defined pimay amines; D-dak conditions: L- 12 : 12 L/D conditions. blue-geen algae (15.5%). n contast, the eotophic potozoans (dak, 26.7 mg C m-3; biomass of the light sample inceased to 264 light, 184 mg C mm3). mg C mm3 with high abundances of chyso- We did not investigate the easons fo the phytes (36.10/o), diatoms (28.9%), and blue- inceases in phytoplankton and potozoan geen algae (13.0%). n addition to phyto- biomass duing the light incubations. nplankton, both dak and light samples had ceased nutient supply seems unlikely beinceased populations of unidentified het- cause geat cae was taken to avoid contam-
5 Notes July (a) Unteated (b) + AA NH$L ---& --a../ -e--+--*----e--.- -e---e- -. *a - x0 NH,+,D,-,B--- a-*---a-.) s -3 G.- $0 2 (c) + NH; l. B NH,+, D /.*.., / *, O---a b, NH,+, L *A- -*- --..@-e- + PA, LJ? =ljh,+, D E a, 22 (e) 0.8~pm Filteed (f) 0.8~pm Filteed + AA s NH,+,D A (g) 3-pm Filteed (h) 3-pm Filteed + AA NH,+,D 9 _e----c Time (days) Fig. 2. As Fig. 1, but sampled on 28 July 1986, at in situ tempeatue of 23 C. ination duing sample handling. A moe samples, but the mesozooplankton that gaze easonable explanation may be the selective o pey on the algae and potozoans wee emoval of the effects of mesozooplankte likely not sampled epesentatively. gaze-pedatos caused by the use of small Bacteial abundances did not diffe sig- (70-ml) incubation vessels. nitial concen- nificantly (paiwise t-test a! = 0.05) between tations of micobial food-web components light- and dak-bottle conditions and vaied would not be affected by the use of small minimally in ou expeiments. nitial abun-
6 1358 Notes dances anged fom 6.7 to 11.4 ( x 105) cells ml- l and esembled numbes peviously epoted fo Lake Michigan (7-10 x 1 O5 cells ml- l: Scavia et al. 1986). Filtation though 3- o 0.8qm poe-size membanes did not affect bacteia concentations. Bacteial abundances did not change significantly duing incubations fo most teatments but did seem to incease slightly (to x lo5 cells ml-l) duing incubations in the 0.8~pm filtates fotified with amino acids. The modest inceases in bacteial numbes in these filtates pobably esulted both fom the emoval of potential bacteial gazes and fom the addition of a new substate (DFAA) fo the bacteia. Net amino acid emoval ates (slopes of PA concentation vs. time) in light bottles fotified with 0.94 PM DFAA wee almost always lowe than in coesponding dak bottles (Figs. 1 and 2). These diffeences can easonably be attibuted to diect, o possibly indiect, amino acid elease by metabolizing phytoplankton. Potozoans may also have been involved in the DFAA elease pocess, but we did not specifically examine thei ole in this study. f bacteial uptake sites ae fist satuated with amino acids (e.g. at concentations of - 1 PM fo Lake Michigan: Gadne et al. 1986) then bacteial uptake ates of amino acids should be simila in both light/dak and dak bottles, and the diffeences in net ates of amino acid emoval between the two should povide a eliable estimate of amino acid elease by phytoplankton. A simila appoach with satuating concentations of inoganic nutients was used to diffeentiate phytoplankton uptake fom zooplankton elease of ammonium and phosphate (Lehman 1980). Estimates of elease of phytoplankton amino acids by this light-dak appoach assume that elease is geate fo photosynthesizing phytoplankton (light/dak conditions) than fo phytoplankton held fo extended peiods in the dak. Ou data suppot this assumption. When we emoved the phytoplankton, no significant diffeences in ates of amino acid uptake wee obseved between light and dak bottles (i.e. net elease in most 0.8~pm poe-size filtates was not significantly diffeent fom zeo: Table 1). f selective autolytic elease of amino acids by phytoplankton occus in the dak, then these estimates would be consevative o negative. Howeve, PA concentations did not incease in any of the dak o light bottles duing ou incubations; micobial uptake ates appaently balanced any autolytic elease of DFAA by old o decaying phytoplankton in the bottles. The lightdak method allows the estimation of DFAA elease, by diect chemical measuement of PA, without emoval o inactivation of bacteia in the sample. Howeve, sufficient incubation time is needed fo the dakened phytoplankton to fist use up stoed enegy eseves so amino acids and poteins ae no longe poduced in the same manne as by the lighted phytoplankton (Piscu and Piscu 1984). Cae must be execised in extapolating such esults to the field because this necessay extended incubation can cause changes in phytoplankton content and composition. Howeve, insights gained fom these expeiments enhance ou undestanding of nutient convesion pocesses in natue. n ou expeiments, the changes in PA concentation in the dak wee usually almost identical to those in the light duing the fist 2-3 d. Aftewad, the net PA levels in unfilteed samples usually deceased moe apidly in the dak than in the light (e.g. Figs. 1 and 2). Positive slopes with significant egessions fo the elationship between amino acid elease [1.46 x (PA, - PA,)] vs. time wee obseved fo all unteated samples and fo all but one of those fotified with 1 PM NH,+ (Table 1). n contast, only one of the 0.8~pm filtates (26 Novembe sample) and thee of the 3-pm filtates (23 Apil, 7 May, and 23 Septembe samples) exhibited significant elease of amino acids. s of amino acid elease anged fom undetectable up to 6.3 ng-atoms N lite- h-l oveall and fom 0.8 to 3.5 in samples that wee not fotified with ammonium o filteed befoe incubations (Table 1). The high value of 6.3 ng-atoms N lite-l h-l fo the NH,+-fotified sample of 28 July esulted fom an unusual patten of PA emoval and may not be typical. n contast to othe teatments, this sample showed a elatively apid, exponential decline in ami-
7 Notes 1359 Table 2. s of ammonium egeneation (nmol NH, lite- h-l) fo epilimnetic Lake Michigan wate held in the dak fo 6-14 d. s wee calculated as the slope of ammonium accumulation vs. time afte l-2 d wee allowed fo the phytoplankton to exhaust biochemically stoed enegy. Numbe of data sets compaed pe egession - n; coelation coefficient - y Unteated 1 FM NH, addition 3-pm filtate 0.8~Fn filtate 23 Ap May May Jun Jul Jul Aug Sep Nov no acids ove time (Fig. 2d). Expessed as cabon, ou measued ates of phytoplankton amino acid elease on unteated samples anged fom 1.1 to 4.8 hg C lite-l d-l. f actual amino acid elease in the lake is consevatively assumed to be about a thid of that obseved in ou bottles (based on the inceases in phytoplank.ton biomass obseved duing containment fo the June expeiment), amino acid elease would be 0.4 to 1.2,ug C lite- d-l. These data suggest that elease of amino acids by phytoplankton could be an impotant pocess supplying oganic substates to bacteia in the lake. Simila conclusions wee eached fo eutophic Danish lakes (Jogensen 1987). Ou uncoected values ae about 10% (vs. - 3% fo containment-coected values) of the seasonal ange in pimay poduction ates obseved at an offshoe station (N pg C lite- 1 d- 1 : Scavia et al. 1986). f ates of pimay poduction at ou station wee appoximately double those at the offshoe station (based on diffeences in chloophyll levels; Mall and Bahce 1986) and if ou ates easonably appoximate actual field ates, this compaison suggests that about 5% (o about 2%, with the above containment coections) of cabon fixed in pimay poduction could be eleased as DFAA. Ou containment-coected ates of amino acid C elease esemble ates of total PDOC elease peviously measued by isotopic techniques in fesh Lake Michigan wate ( pg C lite- d-l: Laid et al. 1986) and in Lake Eie (2.1% of photo- synthetic C) o Lake Ontaio (4.4% of photosynthetic C) (Lee and Nalewajko 1978). The esults fom the isotopic studies may have been consevative because of possible incomplete labeling of the algal excetoy pools duing the elatively shot duation (4-26 h) of the expeiments (Laid et al. 1986). These data indicate that a significant faction of PDOC in Lake Michigan could occu as DFAA. Ammonium accumulation in dak-bottle samples was measued to povide insights about ates of nitogen minealization and to allow examination of potential convesions of DFAA-N to NH,+-N. These esti- mates may be biased eithe by dak-induced decomposition of algae o, at the 24 0 l 0 0 Excluding*, cc 3 0 = '; a = ; $2 0 0 b = 1.55 &= $2 +d 0 -- lcci =6, c -- J Amino Acid Release (ng-atoms N lite-1 h-1) Fig. 3. Compaison of DFAA elease to ates of ammonium egeneation fo epilimnetic Lake Michigan samples collected in Unteated samples - 0; samples teated with 1 PM NH,--0.
8 1360 Notes Table 3. s of ammonium egeneation (nmol NH,+ lite- h-l) fo epilimnetic Lake Michigan wate fotified with 0.94 KM amino acids and held in the dak fo 6-14 d. s calculated as in Table 2. Data fom time points afte the ate of ammonium poduction declined, due to depletion of added amino acids, wee not included in egessions. Numbe of data sets compaed pe egession--n; coelation coefficient--. Unteated pm NH, addition 3-Nm filtate O.&pm filtate 1986 n 7 May 9 22 May 9 9 Jun 10 9 Jul 4 28 Jul 6 20 Aug 6 23 Sep 5 26 Nov oo oo othe exteme, by deceased inputs of new labile oganic nitogen due to discontinued photosynthetic activity in the dak bottles, but they ae useful fo compaison to the amino acid inputs. Except fo some initial l-2-d deceases, ammonium concentations usually inceased in dak bottles. Afte the initial l-3-d peiod, pesumably needed fo phytoplankton to deplete thei enegy eseves, appoximately linea accumulation of ammonium was usually detected ove time in dak-bottle samples (Table 2). n unfilteed samples that wee not fotified with amino acids, significant (P < 0.05) slopes fo ates of dak accumulation of ammonium vs. time wee obseved fo all but the 28 July sample (Table 2). s of dak accumulation of ammonium in the unteated samples anged fom to 4.2 nmol NH,+ lite-l h-l (Table 2). Simila ates wee obseved in the samples that wee fotified with ammonium o passed though 3-pm poe-size filtes, but some slopes wee not significant. n contast, ammonium levels deceased o emained at backgound levels in light bottles (Fig. l), except fo some PA-fotified samples in which NH4+ poduction exceeded emoval by phytoplankton (Fig. 2b, d, f, and h). s of ammonium egeneation wee low (slopes wee often not significantly diffeent fom zeo) in the 0.8~pm filtates except fo the 9 June filtate that yielded a ate compaable to the unfilteed samples (Table 2). These low ates could indicate that micogazes, athe than bacteia, wee the pimay minealizes in the unfilteed wate (e.g. Goldman et al. 1985) o possibly that the ammonium accumulation in the unfilteed wate (o the 3-pm filtates) esulted mainly fom the decomposition of paticles (e.g. dead phytoplankton) in the dak bottles. s of dak ammonium poduction in bottles of unfilteed Lake Michigan wate coelated significantly (P < 0.0 1) with ates of amino acid elease, by the elationship, NH4+-N poduction = (1.55) x (amino-acid-n elease) ( = 0.84; y2 = 14) if two outlies (July and August samples with ammonium additions) wee excluded (Fig. 3). On aveage, the ates of ammonium poduction wee highe than those of amino acid elease, pobably due to the ecycling of dissolved o paticulate labile oganic nitogen occuing in foms othe than DFAA (e.g. poteins o peptides). Addition of amino acids to Lake Michigan wate always enhanced the ates and amounts of ammonium accumulation in the dak (Tables 3 vs. 2). When amino acids wee added, significant egeneation of ammonium was obseved fo all the expeimental teatments except fo two 0.8~pm poe-size filtates (Table 3). s fo unfil- teed samples anged fom 2 to 13 nmol NH,+ lite- h-l and coelation coefficients fo ammonium accumulation vs. time wee all >0.84 (Table 3). By compaing the net diffeences in ammonium poduction in dak bottles caused by addition of amino acids with coesponding deceases in DFAA-N in fotified samples ove the same peiod, we could estimate the pecentage of assimilated amino acid nitogen that was minealized vs. in-
9 Notes 1361 copoated into food-web biomass. f coections wee made fo natual ammonium poduction (i.e. ates in unfotified dak bottles), inceased ammonium poduction in samples fotified with amino acids was elated to amino acid emoval ove the same peiod. The aveage atio of inceased ammonium-n poduced to DFAA-N emoved fo ou samples was 1.Ol (SE = 0.08, n = 29). Thus, on aveage, the amount of DFAA-N emoved fom solution was equal to the amount that appeaed as inceased ammonium in the same bottles. t implies that the added amino acids likely wee quantitatively deaminated and that little of the nitogen in ou bottles was incopoated into food-web biomass. (t also indicates that the ammonium poduced in wate was not nitified in ou expeimental systems.) Although the dynamics of cabon and nitogen ae not stictly compaable, the idea that most DFAA-N is not incopoated into uppe food-web biomass agees in pinciple with the concept that the micobial food web functions pimaily as a sink fo cabon in planktonic food webs and that this ole of minealize is moe impotant than the ole of assimilato of oganic mateial into highe tophic levels (Ducklow et al. 1986) in Lake Michigan. The appaently complete deamination of the added amino acids that wee emoved fom solution was somewhat supising because the use of amino acid cabon fo enegy, with the associated enegy-cost of deamination, seems less efficient than the use of the compounds diectly fo poducing biomass (poteins). Fo example, amino acids ae a less efficient substate fo poduction of aquatic bacteia than is a combination of glucose + ammonium (Wheele and Kichman 1986). Although it is speculation, the appaent quantitative deamination of added amino acids that we obseved may imply a scacity of othe souces of oganic cabon enegy that ae eadily available to heteotophs in epilimnetic Lake Michigan wate. Amino acids may constitute a elatively high pecentage of new, low-molecula-weight oganic cabon eleased by phytoplankton (Mague et al. 1980; Jogensen 1987). This scenaio may be easonable fo epilimnetic Lake Michigan wate whee the phytoplank- ton ae not limited by inoganic nitogen (Batone and Schelske 1982) o light (Fahnenstiel and Scavia 1987~). U.S. Depatment of Commece Geat Lakes Envionmental Reseach Laboatoy 2205 Commonwealth Blvd. Ann Abo, Michigan Refeences Wayne S. Gadne Joann F. Chandle Gwenyth A. Lab-d Hunte J. Caick AZAM, F., AND J. W. AMMERMAN Cycling of oganic matte by bacteioplankton in pelagic maine systems: Micoenvionmental consideations, p Zn Flows of enegy and mateials in maine ecosystems. NATO Conf. Se. 4, Ma. Sci. V. 13. Plenum. BARTONE, C. R., AND C. L. SCHELSKE Lakewide seasonal changes in limnological conditions in Lake Michigan, J. Geat Lakes Res. 8: BRD, D. F., AND J. KALFF Bacteial gazing by planktonic lake algae. Science 231: CARON, D.A.,J.C. GOLDMAN,O.K.ANDERSON,AND M. R. DENNETT Nutient cycling in a micoflagellate food chain: 2. Population dynamics and cabon cycling. Ma. Ecol. Pog. Se. 24: COLE, J. J., G. E. LKENS, AND D. L. STRAYER Photosynthetically poduced dissolved oganic cabon: An impotant cabon souce fo planktonic bacteia. Limnol. Oceanog. 27: 1080-l 090. COVENEY, M. F Bacteial uptake of photosyn- thetic cabon fom fesh wate phytoplankton. Oikos 38: DOZER, B. J., AND P. J. RCHERSON An impoved membane filte method fo the enumeation of phytoplankton. nt. Ve. Theo. Angew. Limnol. Veh. 19: DUCKLOW, H. W., D. A. PURDE, P. J. LEB. WLLAMS, AND J. M. DAVES Bacteioplankton: A sink fo cabon in a coastal maine plankton community. Science 232: FAHNENSTEL, G.L., AND D. SCAVA. 1987a. Dynamics of Lake Michigan phytoplankton: Pimay poduction and gowth. Can. J. Fish. Aquat. Sci. 44: , AND b. Dynamics of Lake Mich- igan phytoplankton: Recent changes in suface and deep communities. Can. J. Fish. Aquat. Sci. 44: , L. SCKO-GOAD, D. SCAVA, AND E. F. STOER- MER mpotance of picoplankton in Lake Supeio. Can. J. Fish. Aquat. Sci. 43: FUHRMAN, J Close coupling between elease and uptake of dissolved fee amino acids in sea-
10 1362 Notes wate studied by an isotope dilution appoach. Ma. Ecol. Pog. Se. 37: , AND G. MCMANUS Do bacteia-sized maine eukayotes consume significant bacteial poduction? Science 224: 1257-l 260. GARDNER, W. S Micofluoometic method to measue ammonium in natual wates. Limnol. Oceanog. 23: , J. F. CHANDLER, G. A. LARD, AND D. SCAVA Micobial esponse to amino acid additions in Lake Michigan: Gaze contol and substate limitation of bacteial populations. J. Geat Lakes Res. 12: , AND W. H. MLLER ntacellula composition and net elease ates of fee amino acids in Daphnia magna. Can. J. Fish. Aquat. Sci. 38: , AND H. A. VANDERPLOEG Mico sample-filteing device fo liquid chomatogaphy o flow injection analysis. Anal. Chem. 54: GOLDMAN, J. C., D. A. CARON, 0. K. ANDERSON, AND M. R. DENNETT Nutient cycling in a micoflagellate food chain: 1. Nitogen dynamics. Ma. Ecol. Pog. Se. 24: HAMMER, K. D., AND G. KATTNER Dissolved fee amino acids in the maine envionment: A cabon to nitogen atio shift duing diatom blooms. Ma. Ecol. Pog. Se. 31: HOBBE, J. E., R. J. DALEY, AND S. JASPER Use of Nuclepoe filtes fo counting bacteia by fluoescence micoscopy. Appl. Envion. Micobial. 33: TURRAGA, R., AND A. ZSOLNAY Diffeentiation between auto- and heteotophic activity: Poblems in the use of size factionation and antibiotics. Bot. Ma. 24: , AND Heteotophic uptake and tansfomation of phytoplankton extacellula poducts. Bot. Ma. 26: JENSEN, L. M Phytoplankton elease of extacellula oganic cabon, molecula weight composition, and bacteial assimilation. Ma. Ecol. Pog. Se. 11: p Antimicobial action of antibiotics on bacteial and algal cabon metabolism: On the use of antibiotics to estimate bacteial uptake of algal extacellula poducts. Ach. Hydobiol. 99: JBRGENSEN, N. 0. G Fee amino acids in lakes: Concentations and assimilation ates in elation to phytoplankton and bacteial poduction. Limnol. Oceanog. 32: 97-l 11. LARD, G. A., D. SCAVLP., AND G. L. FAHNENSTEL Algal oganic cabon excetion in Lake Michigan. J. Geat Lakes Res. 12: LEE, K., AND C. NALEWAJKO Photosynthesis, extacellula elease and glycolic acid uptake by phytoplankton: Factionation studies. nt. Ve. Theo. Angew. Limnol. Veh. 20: LEHMAN, J. T Release and cycling of nutients between planktonic algae and hebivoes. Limnol. Oceanog. 25: MAGUE, T. H., E. FRBERG, D. J. HUGHES, AND. MORRS Extacellula elease of cabon by maine phytoplankton; a physiological appoach. Limnol. Oceanog. 25: MOLL, R., AND M. BRAHCE Seasonal and spatial distibution of bacteia, chloophyll, and nutients in neashoe Lake Michigan. J. Geat Lakes Res. 12: PRSCU, J. C., AND L. R. PRSCU Photosynthate patitioning by phytoplankton in a New Zealand coastal upwelling system. Ma. Biol. 81: RASSOULZADEGAN, F., AND R. W. SHELDON Pedato-pey inteactions of nanozooplankton and bacteia in an oligotophic maine envionment. Limnol. Oceanog. 31: SCAVLA, D., G. A. LARD, AND G. L. FAHNENSTEL Poduction of planktonic bacteia in Lake Michigan. Limnol. Oceanog. 31: SHERR, B. F., E. B. SHERR, T. L. ANDREW, R. D. FALLON, AND S. Y. NEWELL Tophic inteactions between heteotophic potozoa and bacteioplankton in estuaine wate analyzed with selective metabolic inhibitos. Ma. Ecol. Pog. Se. 32: 169-l 79. ~ AND T. BERMAN Gazing, gowth, and ammonium excetion ates of a micoflagellate fed with 4 species of bacteia. Appl. Envion. Micobial. 45: 1196-l SEBURTH, J. McN Potozoan activity in pe- lagic maine wates, p Zn J. E. Hobbie and P. J. LeB. Williams [eds.], Heteotophic activity in the sea. Plenum. STOCKNER, J., AND N. J. ANTA Algal picoplankton fom maine and feshwate ecosystems: A multidisciplinay pespective. Can. J. Fish. Aquat. Sci. 43: VENRCK, E. L., J. R. BEERS, AND J. F. HENBOKEL Possible consequences of containing micoplankton fo physiological ate measuements. J. Exp. Ma. Biol. Ecol. 26: WHEELER, P. A., AND D. L. KRCHMAN Utilization of inoganic and oganic nitogen by bacteia in maine systems. Limnol. Oceanog. 31: Submitted: 17 Apil 1987 Accepted: 6 August 1987
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