Benthic algae control sediment water column fluxes of organic and inorganic nitrogen compounds in a temperate lagoon

Transcription

1 Limnol. Ocenogr., 48(6), 200, , y the Americn Society of Limnology nd Ocenogrphy, Inc. Benthic lge control sediment wter column fluxes of orgnic nd inorgnic nitrogen compounds in temperte lgoon Ann Christin Tyler 1 nd Kren J. McGlthery Deprtment of Environmentl Sciences, P.O. Box 400, University of Virgini, Chrlottesville, Virgini Iris C. Anderson School of Mrine Science, Virgini Institute of Mrine Science, College of Willim nd Mry, Gloucester Point, Virgini 2602 Astrct Costl lgoons re common lnd-mrgin feture worldwide nd function s n importnt filter for nutrients entering from the wtershed. The shllow nture of lgoons leds to dominnce y enthic utotrophs, which cn regulte enthic pelgic coupling. Here we demonstrte tht oth microlge nd mcrolge re importnt in controlling dissolved inorgnic s well s orgnic nitrogen (DIN nd DON) fluxes etween the sediments nd the wter column. Fluxes of nitrogen (NH 4, NO, DON, ure, nd dissolved free nd comined mino cids [DFAA, DCAA]) nd O 2 were mesured from Octoer 1998 through August 1999 in sediment cores collected from Hog Islnd By, Virgini. Cores were collected from four s representing the rnge of environmentl conditions cross this shllow lgoon: muddy, high-nutrient nd sndy, low-nutrient s tht were oth dominted y enthic microlge, nd mid-lgoon with fine snds covered y dense mcrolgl mts. Sediment wter column DON fluxes were highly vrile nd comprle in mgnitude to DIN fluxes; fluxes of individul compounds (ure, DFAA, DCAA) often proceeded simultneously in different directions. Where sediment metolism ws net utotrophic ecuse of microlgl ctivity, TDN (totl dissolved nitrogen) fluxes, mostly comprised of DIN, ure, nd DFAA, were directed into the sediments. Heterotrophic sediments, including those underlying mcrolgl mts, were net source of TDN, mostly s DIN. Mcrolge intercepted sediment wter column fluxes of DIN, ure, nd DFAA, which ccounted for 27 75% of clculted N demnd. DON uptke ws importnt in stisfying mcrolgl N demnd sesonlly nd where DIN concentrtions were low. Up to 22% of totl N uptke ws relesed to the wter column s DCAA. Overll, mcrolge ssimilted, trnsformed, nd rerelesed to the wter column oth orgnic nd inorgnic N on short (minutes hours) nd long (months) time scles. Microlge nd mcrolge clerly regulte enthic pelgic coupling nd therey influence trnsformtions nd retention of N moving cross the lnd se interfce. Costl lgoons, like deep esturies, process nutrients trveling from costl wtersheds cross the lnd mrgin to the open ocen. The shllow nture of lgoonl esturies leds to high rtio of surfce re to wter volume nd the enthos is usully within the photic zone. As result, enthic primry production is often more importnt thn pelgic production, nd sediment minerliztion of nutrients my drive overll iogeochemicl cycling (Mrtens 1982; Snd- Jensen nd Borum 1991; Anderson et l. 200). Segrsses, 1 To whom correspondence should e ddressed. Present ddress: Deprtment of Environmentl Science nd Policy, University of Cliforni t Dvis, One Shields Avenue, Dvis, Cliforni (tyler@lumni.virgini.edu). Acknowledgments We re grteful to T. Mstronicol, J. Burton, I. Buffm, J. Spitler, J. Rosinski, M. Thomsen, L. Skne, K. Russell, A. Moore, nd J. Men for their ssistnce with field nd lortory work, to J. Gllowy for the use of his HPLC system, nd to J. Porter for ssistnce with sttistics nd figures. Two nonymous reviewers provided comments tht gretly improved the mnuscript. This mteril is sed upon work supported y the Ntionl Science Foundtion under grnt DEB (Virgini Cost Reserve LTER) nd DEB (K.J.M.) nd the U.S. Environmentl Protection Agency under grnt U-952 (STAR Grdute Fellowship to A.C.T.). 25 mcrolge, nd microlge re the dominnt enthic primry producers in these shllow systems (Snd-Jensen nd Borum 1991). As humn inputs of nitrogen (N) to shllow costl systems increse, there is often shift in the dominnt group of producers, from segrsses to mcrolge, nd perhps eventully to phytoplnkton where nutrient loding nd wter residence time re oth sufficiently high (Vliel et l. 1997). Becuse microlge nd mcrolge re cple of rpid nutrient uptke, prticulrly in comprison to segrsses, their presence t the sediment surfce influences the movement of dissolved nutrients cross the sediment wter interfce. Although the influence of enthic lge on enthic pelgic coupling of dissolved inorgnic N (DIN) hs een well studied (Sundck nd Grneli 1988; Rizzo 1990; Kruse-Jensen et l. 1996; McGlthery et l. 1997), the impct of these importnt primry producers on dissolved orgnic N (DON) fluxes is not well understood. DON, which enters costl systems vi freshwter input nd tmospheric deposition, often mkes up lrge proportion of the dissolved N in sewter (Shrp 198). Sediment fluxes of recycled N lso re potentilly importnt source of DON to the wter column, lthough the mgnitude of DON fluxes in shllow esturies cn vry widely (Hopkinson 1987; Dollr et l. 1991; Tyler et l. 2001). Mesurements of ulk DON, however, msk the dynmics of individul compounds, which vry widely in moleculr weight

2 26 Tyler et l. Tle 1. Chrcteristics of the four s in Hog Islnd By. Wter column concentrtions re the nnul men, rnge, nd percent of the totl dissolved nitrogen (TDN) pool mde up y ech compound from smples collected t the time of core collection for flux experiments. Mcrolgl iomss, enthic microlgl Chl, sediment % N, nd sediment C : N were mesured within week of ech flux experiment nd lso represent the nnul men nd rnge. TDN NH 4 NO DON* Ure DFAA* DCAA* Biomss Chl %N C:N Sediment type mol L 1 mol L 1 % TDN mol L 1 % TDN mol L 1 % TDN mol L 1 % TDN nmol L 1 % TDN nmol L 1 % TDN gdwm 2 mg m 2 Willis Whrf Men Rnge Mud Men Creek Rnge Mud Men Shol * DON, dissolved orgnic nitrogen; DFAA, dissolved free mino cids; DCAA, dissolved comined mino cids. McGlthery et l. unpul. dt. Rnge Fine snd Men Hog Rnge Snd nd iovilility (Burdige nd Zheng 1998). For exmple, ioville compounds such s mino cids nd ure my mke up significnt portion of the DON pool nd contriute to the enthic flux of DON (Boucher nd Boucher-Rodoni 1988; Lomstein et l. 1989; Burdige nd Zheng 1998). In ddition, these smll, lile orgnic compounds my represent n importnt source of N for oth heterotrophic nd utotrophic microorgnisms, s well s for enthic plnts (Jorgensen 1982; Admirl et l. 1984; Lomstein et l. 1989; Keil nd Kirchmn 199; Nilsson nd Sundck 1996; Rondell et l. 2000). In the work presented here, we investigted the role of the two dominnt groups of enthic primry producers, mcrolge nd microlge, in regulting sediment wter column exchnges of DIN, ulk DON, nd specific lile DON compounds (dissolved free nd comined mino cids [DFAA, DCAA], ure) in Hog Islnd By, shllow lgoon on the Virgini cost. Methods Site description Hog Islnd By, locted within the Virgini Cost Reserve LTER, is typicl ck-rrier lgoonl estury extending westwrd from the Delmrv Peninsul, Virgini (Fig. 1). Of the totl enthic surfce re of the lgoon (,085 h), 7% is intertidl mrshes nd flts nd 46% is less thn 2 m deep t men low wter (MLW) (Oertel 2001). Recent numericl model results indicte tht residence times of individul wter prcels within the lgoon re sptilly highly vrile nd rnge from 1 to 21 d, with n verge of 16 d (D. Fugte pers. comm.). The smll creeks tht drin the griculturl wtershed contin high concentrtions of dissolved N, primrily s DIN, resulting lrgely from nutrient-enriched groundwter nd to lesser extent from overlnd flow fter rin events (Neikirk 1996; J. Wu unpul. dt). Atmospheric deposition is lso potentilly importnt source of DIN nd DON to the system. There is grdient of nutrient inputs nd sediment orgnic mtter cross Hog Islnd By from the minlnd to the islnds, with the highest concentrtions of dissolved N nd sediment orgnic mtter found closest to the minlnd (McGlthery et l. 2001). Segrsses hve een loclly extinct since the 190s, so tht enthic mcrolge nd microlge re the dominnt primry producers. The dominnce of ech of these functionl groups of primry producers vries cross the lgoon nd shifts throughout the yer (McGlthery et l. 2001). Mcrolgl iomss, which is dominted y Grcilri tikvhie, Bryopsis plumos, nd Ulv lctuc, peks in July. Phytoplnkton my exhiit pek in productivity following the decline in mcrolgl iomss (McGlthery et l. 2001). Benthic microlgl productivity hs een shown to rnge from 4% to 99% of totl enthic productivity, with highest rtes in the lte summer (McGlthery et l. 2001). Smples were collected from four shllow sutidl s (1 m t MLW) tht represent the rnge of environmentl conditions within Hog Islnd By (Fig. 1). Descriptive chrcteristics of ech re given in Tle 1. Closest to the minlnd, the Willis Whrf (WW) ws locted ner the hed of Prting Creek, smll triutry of Mchipongo Chnnel. Historiclly, shellfish processing plnts were locted here nd more recently, quculture fcilities dischrge wter into the creek. The Creek ws locted on the mr-

3 Algl control of nitrogen fluxes 27 gin of smll secondry tidl creek (5 m cross) flowing through well-developed Sprtin lterniflor mrsh. Mcrolgl iomss ws generlly low t oth of these s (10 g dry weight [dw] m 2, McGlthery et l. 2001; McGlthery et l. unpul. dt). The Shol ws locted mid-lgoon in proximity to series of relict oyster reefs, which provide n ttchment for mcrolge nd serve s rrier, trpping floting mcrolge. All smpling took plce in the fine-grined sndy sediments just to the est of the reefs. Mcrolgl iomss t Shol ws n order of mgnitude higher thn t the other s, with ptchy mts 650 gdwm 2 (McGlthery et l. 2001). A ck-rrier locted t the southern end of Hog Islnd (Hog) ws chrcterized y corse-grined, low-orgnic-content snds nd mcrolgl iomss similr to Creek, ut microlgl chlorophyll [Chl ] tht ws often 2 higher thn elsewhere in the lgoon (McGlthery et l. 2001). N flux mesurements Sediment wter column fluxes of dissolved nitrogen were mesured in polycronte core tues (8 cm i.d.; cm sediment, 18 cm wter column) in Octoer 1998 nd Jnury, Mrch, My, June, nd August In July of 1999, n dditionl experiment ws conducted t Shol only, in n ttempt to cpture the high fluxes previously oserved following the crsh of the mcrolgl mts. The mcrolge did not exhiit the mssive die-off s in previous yers, however, nd iomss declined more slowly. Mesurements from this month re included in figures, ut were not included in sttisticl nlyses to mintin n equl numer of smples etween s. Sediment cores, wter, nd U. lctuc were collected from ech y hnd, trnsported to the lortory in Chrlottesville, Virgini, nd held overnight in Conviron environmentl growth chmer t mient tempertures. Stoppers were removed from the cores overnight to llow gs exchnge with the ir. At the initition of the experiment, the overlying wter ws siphoned from ech core nd crefully replced with unfiltered sewter tken from ech. Experimentl tretments (sediment only, sediment lge, nd wter lnks) were run in triplicte. U. lctuc iomss in the cores, equivlent to g dw m 2, pproximted the men monthly iomss in the lgoon ( g dw m 2, McGlthery et l. unpul. dt). To simulte conditions in the field, mcrolge were positioned t the sediment surfce nd held in plce y smll disk of cler plstic netting (1 mm mesh). A smll mgnetic stir r ws then suspended from flexile metl holster in ech core nd the core ws cpped with n crylic top. All ir ules were relesed through smll hole in the top nd ruer stopper ws inserted to sel the chmer. Cores were plced in rndom sequence in filled quri in the environmentl chmer. The wter column of ech core ws gently stirred (60 rpm) throughout the experiment to prevent the uild-up of concentrtion grdients t the sediment wter column interfce. Fluxes were mesured over -h period (6 h light [550 mol photons m 2 s 1 ], 6 h drk) t mient field tempertures. Dissolved oxygen (DO) nd temperture were mesured nd smples for mmonium (NH 4) nd nitrte nitrite (NO NO 2) were collected t -h intervls; smples for ure, mino cids, nd totl dissolved nitrogen (TDN) were collected t 6-h intervls. DO ws mesured using n Orion Model 842 meter with self-stirring proe. Wter smples were collected with syringe nd cores were refilled with n equl volume of wter efore recpping. The cores were drkened y covering quri with luminum foil immeditely fter the 6-h smpling. All nutrient smples were filtered immeditely (Gelmn Supor, 0.45 m) nd frozen with the exception of NH4 nd ure smples, which were nlyzed within h of collection. Smples for mino cid nlysis (20 ml) were filtered through mixed cellulose ester filters using gentle vcuum pressure nd frozen. Mcrolgl thlli from sediment lge cores were removed fter the experiment, rinsed riefly with deionized wter, ptted dry, nd frozen. Smples were lyophilized, ground to homogeneity, nd C nd N contents were mesured using Crlo Er NA 2500 Elementl Anlyzer. Nutrient nlyses Ammonium ws mesured using the phenol hypochlorite method (Solorzno 1969). Nitrte nitrite ws mesured using n Alpkem Flow Solution Autonlyzer (Perstorp 1992). Ure ws mesured using the method descried y Goeyens et l. (1998) nd TDN ws mesured s NO fter lkline persulfte digestion in precomusted seled mpoules s descried in Tyler et l. (2001). DFAA concentrtions were determined y precolumn derivtiztion with o-phthldildehyde, seprtion y high-performnce liquid chromtogrphy (HPLC) using two-eluent grdient (eluent 1: 80% NAc uffer, 19% HPLC-grde methnol, 1% tetrhydrofurn; eluent 2: 80% HPLC-grde methnol, 20% NAc uffer; Alltech Gurd Column nd Adsorosphere OPA HR Seprtor Column), nd detection y fluorescence (Jones et l. 1981). Totl dissolved mino cids were mesured fter hydrolysis of 1-ml wter smples in pre-shed mpoules. One milliliter of N HCl ws dded, the mpoule ws seled nd heted to 100C for 24 h (Pedersen et l. 1999). The mpoules were then opened nd dried in vcuum desicctor. After redissolution in 2 ml of nnopure wter, smples were nlyzed s descried ove. DCAA were clculted s the difference etween totl nd free mino cids. Nnopure wter lnks were run through the entire filtrtion, storge, nd nlysis procedures for oth DFAA nd DCAA to evlute nd llow correction for contmintion. Stndrd revitions re used for ll mino cids. Pro ws not detected using this method nd ecuse of co-elution with n unidentified compound, Vl ws not stisfctorily resolved. Asn nd Gln re converted to Asp nd Glu, respectively, y the hydrolysis procedure nd re reported together. Amino cid concentrtions re expressed s mol L 1 N. Flux clcultions Fluxes were estimted on the sis of the chnge in wter column concentrtion over time s descried in Tyler et l. (2001). Wter lnks were used to correct sediment nd sediment lge tretments for wter column ctivity. Likewise, U. lctuc uptke nd relese were clculted y sutrcting the verge sediment flux from the nd then dividing y the iomss of mcrolge in ech core. Dily fluxes were clculted using the numer of hours of light or drk on the dy of the experiment. Annul sediment fluxes were clculted for ech y mul-

4 28 Tyler et l. tiplying ech individul replicte y the numer of dys in the seson tht it represents. One rndomly selected replicte from ech seson ws chosen nd these six estimtes were summed, yielding n nnul flux rte. This ws repeted for the two remining replictes, nd the resulting three nnul estimtes were verged to give single nnul flux rte nd error estimte. Although these clcultions ssume tht the vrince cross smpling times ws equl, which my not e true, it llows for n estimte of the potentil vriility in the nnul flux rtes. Annul mcrolgl uptke ws clculted similrly, y multiplying the mesured uptke rte for ech seson (s mmol g dw 1 d 1 ) y the corresponding locl iomss (g dw m 2 ; McGlthery et l. unpul. dt). This clcultion ssumes tht the reltion etween mesured uptke nd iomss is liner, which is likely true t low iomss (equl to or less thn iomss used in experiment). However, t the higher iomss occsionlly found in the field, ll sediment relese of NO, NH 4, nd ure would e consumed y the lower portion of the mt (McGlthery et l. 1997). Thus multiplying our clculted uptke rte y the iomss found in dense mts would gretly overestimte in situ mcrolgl uptke. To compenste for this, the extrpoltion of mesured uptke rtes to field conditions ws modified when field iomss ws greter thn tht used in our experiments (Shol, Jnury 1999 through August 1999) nd oth rtes re presented in the text. In our incution cores, N ville for mcrolgl uptke ws derived from two sources, sediment nd wter column. We ssumed tht the sediment contriution to mcrolgl N demnd ws equl to the mesured dily sediment efflux, regrdless of mcrolgl iomss. The wter column contriution ws clculted s the difference etween mesured uptke nd the sediment flux (totl uptke sediment flux wter column N uptke). To otin the totl rel uptke of N y mcrolge in situ, the wter column N uptke rte ws multiplied y the field iomss nd this vlue then dded to the rel sediment flux (totl rel uptke [wter column N uptke iomss] sediment flux). Our closed experimentl system my underestimte the wter column N vilility found in the field where tides continully ring in new nutrients. Sttisticl nlyses The influence of mcrolge on dily sediment fluxes ws nlyzed cross ll s nd dtes using one-wy nlysis of vrince (ANOVA). Light drk differences in hourly flux rtes nd hourly uptke rtes were nlyzed similrly. Differences etween s nd dtes were nlyzed using two-wy ANOVA (three s six dtes), nd significnt differences etween s or dtes were determined using Tukey s HSD post hoc test. Person correltion nlysis ws used to identify significnt reltions etween sediment flux rtes nd wter temperture mesured in this experiment, nd mcrolgl iomss, enthic Chl, nd sediment N nd C : N content (Tle 1). Reltions etween lgl uptke rtes nd wter temperture nd lgl tissue N were lso nlyzed using this method. Results Site chrcteristics Wter column dissolved N concentrtions clerly show the pttern of decresing N vilility Fig. 1. Mp showing the loction of Hog Islnd By on the Delmrv Peninsul, Virgini nd the four s used in this study. cross the lgoon (Tle 1), with highest concentrtions t WW nd lowest t Hog. Overll, DON ws 55 97% of the N pool, nd ws proportiontely greter t Hog nd Shol thn t Creek nd WW. DCAA concentrtions were comprle with NH4 nd NO ; ure concentrtions were slight- ly lower nd DFAA very low reltive to the other components. The most common DFAA (4 mole %) in the wter column were Ser (11%), His (20%), Gly (14%), Arg (1%), Asp (7%), Glu (6%), nd Al (4%) (Fig. 2A). Becuse these percentges re sed on concentrtions of mino cid N, the reltive importnce of N-rich mino cids, such s His nd Arg, increses. The most undnt DCAA (Fig. 2B) were Gly (26%), Al (14%), His (%), Thr (9%), Asp (9%), Ser (8%), Glu (7%), nd Arg (5%). Temporlly, TDN concentrtions were highest in lte summer nd lowest in winter nd spring. U. lctuc tissue N generlly reflected the sptil nd temporl vriility in wter column nutrients; highest tissue N ws found t the minlnd s nd there ws uniform decrese during spring, followed y n increse in summer t ll s except Hog (Fig. ). Sediment fluxes Differences in sediment fluxes generlly divided the s into two groups: WW nd Hog; Creek nd Shol. On n nnul sis, sediments t Hog nd WW were net utotrophic ( nd mol O 2 m 2 yr 1, respectively); Creek ws pproximtely in metolic lnce ( ), nd Shol ws net heterotrophic ( mol O 2 m 2 yr 1 ; Tle 2). WW nd Hog sediments were net utotrophic throughout the yer; Creek sediments were utotrophic only in Octoer nd August, nd Shol sediments only in Octoer (Fig. 4). Mximum net heterotrophy of Shol sediments underlying mcrolgl mts coincided

5 Algl control of nitrogen fluxes 29 Fig.. Tissue N content of Ulv lctuc used in experiments (%N SE). Fig. 2. Mol % N for (A) wter column stnding stock, sediment, nd mcrolgl uptke of dissolved free mino cids nd (B) sediment nd mcrolgl of dissolved comined mino cids. A zero vlue indictes tht no relese or uptke of this mino cid ws mesured except where noted s nd ; these mino cids re not recovered fter hydrolysis s descried in the Methods. with mximum mcrolgl iomss. Overll, the sediment DO flux correlted negtively with mcrolgl iomss nd positively with enthic Chl nd temperture (Tle ). The verge dily TDN fluxes (ll smpling periods weighted eqully) showed similr grouping of s; Creek nd Shol sediments produced net efflux (220 nd 276 mol m 2 d 1, respectively) nd utotrophic WW nd Hog sediments net influx (816 nd 24 mol m 2 d 1, respectively; Tle 2). Overll fluxes were highest during the summer months (Fig. 4). Annul fluxes (smpling periods time-weighted) lso divided the s into two groups: TDN efflux t Creek nd Shol (82 21 nd mmol m 2 yr 1, respectively) nd influx t WW nd Hog (299 9 nd mmol m 2 yr 1, respectively; Fig. 5). However, the individul components of the flux often ehved differently from the net TDN flux, with uptke nd relese of different compounds occurring simultneously. On n nnul sis, Creek nd Shol sediments consumed DON nd relesed DIN. The NH4 relesed from the Creek sediments ws 94% of the totl N efflux ( mmol m 2 yr 1 ). Similrly, t Shol, NH 4 (65%) ws lso the primry component of the N efflux (247 mmol m 2 yr 1 ), with ure (2%) nd DCAA (2%) exhiiting only short-term importnce. Of the totl DON influx, 2% ws identified t the Creek (ure 4%, DFAA 7%, DCAA 11%) nd only 1% t the Shol (s DFAA). At WW nd Hog, DIN ws the dominnt component of the influx (NH4 9%, NO % t WW; NH 25%, NO 1% t Hog); unknown 4 DON compounds were lso importnt (49% nd 4% t WW nd Hog, respectively), ut DFAA were not (1%). The smll efflux of N from the sediments t these s (efflux 4 nd 4 mmol m 2 yr 1, for WW nd Hog, respectively) ws mde up of ure (100% t WW; 9% t Hog) nd DCAA (61% t Hog). There were sustntil sesonl differences t ll s, resulting in high vrince of the men dily fluxes (Tle 2; Fig. 4). The highest NH4 effluxes were in summer t Creek nd Shol, while there ws still net influx of oth NH 4 nd NO t WW nd Hog. Totl DON fluxes were generlly directed into the sediments during the wrmer months t ll s except WW in June. DON relese occurred in Octoer nd Jnury t Hog nd in Octoer t Shol nd ws predominntly mde up of ure. The dily DIN, totl DON, nd TDN fluxes were ll highly negtively correlted with the sediment DO flux (Tle ). The dily NH4 flux ws lso negtively correlted with sediment Chl nd positively with mcrolgl iomss in the field (Tle ). Overll, no significnt sesonl trends in sediment ure uptke or relese were oserved nd it ws only sustntil component of the flux t Hog nd Shol. However, the relese of ure nd DON were oth proportionl to the C : N of the sediments (Tle ). DFAA fluxes were generlly smll reltive to the totl DON flux, with little vriility etween s. The only lrge relese of DFAA ws oserved t Shol nd Hog in Jnury; t ll other s nd times the fluxes of ll DFAA, except Arg, Tyr, nd -minoutyric cid (GABA), were directed into the sediments (Fig. 2A). DCAA fluxes exhiited high vriility cross the lgoon, nd differences etween s were seen only etween WW nd Hog; there ws no interpretle pttern of DCAA relese reltive to seson. Overll, only GABA nd Ile were tken up s DCAA y the sediments (men DCAA uptke 1.9 mol m 2 d 1 ) nd ll other mino cids were relesed (men DCAA relese 27. mol m 2 d 1 ; Fig. 2B). Sediment NH4 relese nd DFAA uptke were much greter in the drk (Fig. 6). Individul DFAA lso showed distinct light drk differences, with significntly greter drk uptke of the most undnt DFAA (dt not shown).

6 210 Tyler et l. Tle 2. Anlysis of vrince results nd verge dily flux rte for ech (mol m 2 d 1 N SE; n for mino cids nd 18 for ll other vlues). A positive numer denotes flux out of the sediment; negtive numer indictes flux into the sediment. Significntly different susets (Tukey s HSD post hoc test) for the comprison re denoted y the different letters given eneth the overll mens. DO NH 4 NO DON Ure DFAA DCAA TDN dte dte dte dte dte dte dte dte dte dte dte dte dte dte dte dte F df Willis Whrf Creek Shol Hog.**** 10.8*** 5.6*** 9.7*** *** 10.5***.6*** 6.*** ***.5***.6* ** 2.4*.1* *** 19.1*** 8.2***.6*** c c * P0.05; ** P0.01; *** P DO, dissolved oxygen; DON, dissolved orgnic nitrogen; DFAA, dissolved free mino cids; DCAA, dissolved comined mino cids; TDN, totl dissolved nitrogen. Influence of mcrolge on sediment fluxes Where mcrolgl iomss ws high t Shol, the nnul enthic (sediment mcrolge) TDN fluxes were controlled y mcrolgl uptke nd relese of N (Fig. 5). At Shol, net TDN fluxes decresed y mmol m 2 yr 1 (first numer djusted for high iomss) ecuse of mcrolgl uptke. In contrst, t WW, Creek, nd Hog, low mcrolgl iomss hd little impct on the net enthic TDN flux (dditionl uptke 17, 19, nd 8 mmol m 2 yr 1, respectively). On n nnul sis t Shol, the enthos (including mcrolge) imported DIN nd DFAA nd exported DCAA nd ulk DON (Fig. 5). The sme trend ws seen in the dily mesurements, s shown in Fig. 4. Mcrolge intercepted DIN nd ure fluxes to the wter column, nd enthic uptke of DFAA nd relese of DCAA were greter in the presence of mcrolge. Averged over ll s nd dtes, the sediment mcrolge tretment resulted in 500 mol m 2 d 1 chnge in the NH4 flux nd 100 mol m 2 d 1 chnge in the ure flux (Fig. 7). Uptke of NO nd DFAA from the wter column incresed two- to threefold in cores with mcrolge (Fig. 7). All DFAA were tken up y U. lctuc, except His (Fig. 2A). Totl enthic DON uptke ws less in sediment lge cores, ut not significntly so ecuse of high vriility. However, the DCAA flux, which ws insignificnt in sediment-only cores, verged mol m 2 d 1 in cores with mcrolge. Mcrolgl uptke nd relese, corrected for the sediment fluxes, lso vried etween drk nd light; uptke of NH 4 nd NO were higher in the light, wheres uptke of ure nd DFAA were higher in the drk (Fig. 6). The uptke of ll individul mino cids ws greter in the drk, ut only significntly so for Glu, Asn, Thr, Arg, Tyr, GABA, nd Phe. DCAA were relesed only in the light; lthough ll DCAA were relesed, Gly (18%), Glu (14%), Al (11%), His (11%), nd Ser (5%) were the most undnt (Fig. 2B). The verge dily mcrolgl uptke (s DIN, ure, nd DFAA) t ech vried significntly cross the lgoon, from 24.6 mol gdw 1 d 1 t Creek, to.8 nd 1.4 t WW nd Shol, nd.2 t Hog (Tle 4). NH 4, NO, nd ure uptke were ll correlted with the N content of lge (Tle ). The reltive importnce of DON for mcrolge incresed s DIN vilility decresed: DIN ws the mjority of the uptke t WW nd Creek; DIN uptke lso ws dominnt t Shol, ut ure contriuted greter percentge; t Hog, DIN ws only one-third of totl uptke nd DON contriuted the reminder (Tle 4). There ws generl trend of incresing DCAA relese from the mcrolge s the N content of the lge decresed (Tles, 4). Averged cross ll s, this relese ws equivlent to 22% of the totl uptke of N y the mcrolge. NH4 uptke ws greter during the wrmer months nd DFAA uptke ws greter during the colder months (Tle ). Discussion The oserved ptterns of enthic uptke nd relese of nitrogen show clerly tht within Hog Islnd By the dom-

7 Algl control of nitrogen fluxes 211 Fig. 4. Dily sediment nd sediment lge fluxes (mmol m 2 d 1 N SE) of dissolved oxygen, mmonium, nitrte nitrite, dissolved orgnic nitrogen, ure, dissolved free mino cids, nd dissolved comined mino cids cross Hog Islnd By. Fluxes mesured in sediment lge cores re shown for the Shol only. Positive vlues indicte flux from the enthos to the wter column; negtive vlues indicte flux from the wter column to the enthos. innt primry producers, either enthic microlge or mcrolge, control enthic pelgic coupling. Where sediments were net utotrophic (WW nd Hog) the sediments were TDN sink nd microlge were likely to e the most importnt fctor controlling TDN fluxes. Where sediments were net heterotrophic (Creek nd Shol) the sediments were TDN source. At Shol, dense mcrolge overlying the sediment surfce cused the totl enthos (sediments mcrolge) to e TDN sink, in spite of reltively high sediment N relese. Sediment fluxes nd the influence of enthic microlge The dily sediment NH4 nd NO flux rtes in Hog Islnd By were low ( mmol m 2 d 1 NH nd mmol m 2 d 1 NO ) compred to those oserved in similr shllow esturies (8.1.6 mmol m 2 d 1 NH 4, mmol m 2 d 1 NO, Nowicki nd Nixon 1985; Rizzo 1990; Rysgrd et l. 1996; Anderson et l. 200). The high vriility we oserved in dily DON fluxes in Hog Islnd By ppers to e typicl of costl sediments. Smll vlues of DON uptke y sediments lso hve een oserved in some modertely shllow esturies (0. mmol m 2 d 1 ; Dollr et l. 1991), ut others hve found DON fluxes directed out of the sediments (0.2.9 mmol m 2 d 1 ; Hopkinson 1987; Lomstein et l. 1998). The sme vriility hs een found in deeper esturies, where in some cses DON ws n importnt component of the TDN efflux (Lomstein et l. 1989; Blckurn et l. 1996) nd in others it ws smll or insig-

8 2 Tyler et l. Tle. Results of Person correltion nlysis. Vlues re the Person correltion coefficient (r). n 60 for AA nd 72 for ll other components. DO NH 4 NO DON Ure DFAA DCAA TDN Sediment flux Biomss Chl Temperture Sediment C : N DO flux 0.5** 0.47*** ** 0.** * ** *** * 0.2* *** 0.42*** 0.0** *** Mcrolgl uptke/relese Temperture 0.59*** * *** Tissue % N 0.60*** 0.0* 0.41** 0.28* * 0.67*** * P0.05; ** P0.01; *** P DO, dissolved oxygen; DON, dissolved orgnic nitrogen; DFAA, dissolved free mino cids; DCAA, dissolved comined mino cids; TON, totl dissolved nitrogen. nificnt (Burdige nd Zheng 1998). The reltively low fluxes of oth DIN nd DON tht we oserved were consistent with previous work in Hog Islnd By, which demonstrted tht cteril immoiliztion nd microlgl uptke were cple of removing ll minerlized N, in spite of high minerliztion rtes (Anderson et l. 200). Becuse sediment DIN fluxes were negligile or directed into the sediments in the previous study, phytoplnkton in the wter column hd greter effect on wter column nutrients thn the enthos (Anderson et l. 200). It is likely tht in the erlier study, when the sediments were utotrophic t ll s (Mc- Glthery et l. 2001), microlge were more importnt in consuming sediment-derived DIN thn in the present study when the sediments t Creek nd Shol were net heterotro- Fig. 5. Clculted nnul sediment wter column fluxes, rel mcrolgl uptke/relese (corrected for high iomss s descried in the text), nd net enthic flux (sum sediment flux mcrolgl uptke/relese) cross Hog Islnd By. Positive numers represent relese from the enthos to the wter column. All vlues re in mmol m 2 yr 1 N SE. Fig. 6. Comprison etween light nd drk (A) sediment fluxes nd (B) mcrolgl uptke/relese of dissolved nitrogen. Error rs SE; n 72 ech for light nd drk for ll mesurements except mino cids, where n 60. *, significnt difference etween tretments t P 0.05; **, significnt difference t P A positive vlue indictes flux from the enthos/lge to the wter column; negtive vlue indictes flux into the enthos/lge from the wter column.

9 Algl control of nitrogen fluxes 21 Fig. 7. Comprison etween sediment nd sediment lge tretments. All units re in mol m 2 d 1 N SE. n 72 for ech tretment for ll components except mino cids, where n 60. *, significnt difference etween tretments t P 0.05; **, significnt difference t P A positive vlue indictes flux from the enthos to the wter column; negtive vlue indictes flux into the enthos from the wter column. phic nd we oserved more significnt relese of DIN from these sediments. The lck of cler reltion etween DIN nd DON fluxes nd either sediment type or orgnic content (Fisher et l. 1982; Nowicki nd Nixon 1985) in Hog Islnd By is likely due to the strong influence of the primry producers. Benthic microlgl medition of DIN fluxes is evident in the significntly lower light fluxes t ll four s nd the correltion etween NH4 nd NO influxes (t Hog nd WW) nd oth DO production nd enthic Chl (NH4 only). NH4 my e removed from the wter column directly y microlge nd lso y nitrifiers stimulted y microlgl DO production (An nd Joye 2001). Microlge lso prevent NH4 efflux to the wter column oth y direct uptke nd y creting redox filter from photosynthetic O 2 production (Sundck nd Grneli 1988). Even though net heterotrophy t Creek nd Shol suggests less ctive microlgl community t these s, the dytime NH4 fluxes were reduced y 50% nd 2%, respectively, over the nighttime fluxes. The light drk differences in DIN efflux tht we oserved were equl to nd higher thn those mesured in shllow Rhode Islnd lgoon (25% reduction, Nowicki nd Nixon 1985). Previous estimtes of microlgl N demnd t these s were high ( mmol m 2 d 1 N; Anderson et l. 200); however, in the present study the sediment NH4 efflux t Creek nd Shol indictes tht nitrogen minerliztion exceeded microlgl demnd, the redox filter effect, nd denitrifiction. The higher summertime DIN fluxes tht we oserved t Creek nd Shol re common in temperte esturies (Fisher et l. 1982; Rizzo 1990). Sustrte for the continul relese of minerlized N from orgnic-rich Creek sediments from Mrch through August ws proly supplied y uried mcrolge (pers. os.) or seepge of DIN-enriched groundwter entering through the creeknk (Neikirk 1996). The correltion etween the DO efflux nd DON influx, lthough not s cler cross s s for DIN, suggests temporl importnce of microlgl DON uptke consistent with Rondell et l. (2000), who showed utiliztion of smll DON compounds y microil mt communities dominted y cynocteri. Additionlly, microlgl DO production my stimulte uptke of dissolved orgnic compounds y sediment heterotrophs. In generl, DON fluxes re quite difficult to interpret ecuse single vlue represents the net flux of hundreds of compounds. At est we hve identified 10 40% of the DON pool s ure nd mino cids. Although this leves the ulk of the pool to e identified, closer exmintion of the individul compounds provides more informtion thn ulk DON fluxes lone. The overll rnge of ure fluxes mesured in this study ( mmol m 2 d 1 ; men 0.05) ws comprle with the few other mesurements of ure fluxes in oth shllow (2.1 mmol m 2 d 1 ; Boucher nd Boucher-Rodoni 1988) nd deep systems ( mmol m 2 d 1 ; Lomstein et l. 1989; Blckurn et l. 1996), s well s in Hog Islnd By (Tyler et l. 2001). Even when sediment orgnic C : N is high nd minerlized N is rpidly immoilized y sediment cteri, hydrolysis of detritus t the sediment surfce my still led to positive flux of DON (Lomstein et l. 1998). This flux my e comprised of smll, lile compounds such s mino cids nd ure (Burdige nd Zheng 1998), s we oserved t Hog nd Shol in the fll when high sediment C : N coincided with n efflux of DON, which t Shol ws comprised of ure nd DCAA. Except for the high relese Tle 4. Averge dily uptke nd relese of dissolved N (mol g dw 1 d 1 N SE) y Ulv lctuc for ech. Positive vlues indicte relese from the mcrolge to the wter; negtive numers indicte uptke y the mcrolge from the wter or sediment. Percent contriution to totl uptke is indicted in prentheses. WW Creek Shol Hog NH 4 NO DON Ure DFAA DCAA DON* (7) (10) (2) (1) (9) (8) (2).7.1 (79) (81) (7) (11) (7) (25) (17) (4) () (18) DON* DON (ure DFAA DCAA) nd represents the unknown frction of the DON pool. n for AA nd 18 for ll other components. DON, dissolved orgnic nitrogen; DFAA, dissolved free mino cids; DCAA, dissolved comined mino cids (1)

10 214 Tyler et l. t Shol in Octoer, sediment DCAA fluxes were errtic, not correlted with ny other fluxes or predictor vriles, nd did not pper to e influenced y microlge. Totl, hydrolyzle mino cids my mke up high percentge of sediment pore-wter TDN in some cses (20 70%, Henrichs et l. 1984; 0 40%, Burdige nd Mrtens 1988), ut in Hog Islnd By DCAA were not predictly relesed to the wter column. Microlge (cynocteri) cn survive with only ure s N source nd re cple of uptke in oth the light nd drk, with somewht reduced uptke in the drk (Rondell et l. 2000). The cpcity for drk uptke my explin why we did not oserve light drk differences in sediment fluxes, nd precludes distinct conclusion tht microlge prevent ure fluxes to the wter column. However, the greter relese of ure with lower DO production during the colder months suggests decresed uptke during this period. Further, microlgl uptke in Hog Islnd By my prevent the high summertime ure fluxes mesured y Boucher nd Boucher- Rodoni (1988). There ws often gret del of vriility ssocited with positive ure flux mong individul cores; this heterogeneity my e due to the ptchy distriution of ioturting infun (Lomstein et l. 1989) or enthic microlge. Even though DFAA were only smll proportion of wter column nd sediment influxes of TDN (0 5%) in Hog Islnd By, these highly lile compounds hve such rpid turnover tht low concentrtions or fluxes my not e indictive of reltive importnce (Hgstrom et l. 1984), prticulrly t the time scle of our experiments (6 h). Uptke rtes of His, Gly, nd Al were much greter thn their reltive concentrtion in the wter column, suggesting some preferentil uptke. His, which hd the highest uptke on the sis of the mole % of N, contins 4 N toms, mking it vlule N source, even t low concentrtions. Gly nd Al re liphtic neutrl mino cids, with smll side chins, possily mking them esier to ssimilte thn some of the lrger mino cids. The DFAA uptke tht we oserved contrsts with DFAA relese mesured in the shllow Kysing Fjord, Denmrk (100 mol m 2 d 1 ; Jorgensen 1982) or somewht deeper Cpe Lookout Bight, North Crolin ( mol m 2 d 1 ; Burdige nd Mrtens 1990). Although we my hve slightly underestimted the DFAA flux since we did not mesure Lys, Vl, Pro, or the nonprotein mino cids -minoglutric cid, ornithine, or turine, some of which my e importnt components of sediment fluxes (Jorgensen 1982; Burdige nd Mrtens 1990), the higher-sediment orgnic mtter in Cpe Lookout Bight ( 5% orgnic C, 0.5% N; Burdige nd Mrtens 1988) or wter column nutrients in Kysing Fjord (Jorgensen 1982) my lso hve contriuted to the positive DFAA fluxes mesured in these more nutrient-enriched esturies. Moreover, noxi my limit DFAA minerliztion within orgnic-rich sediments nd foster n efflux (Henrichs et l. 1984), ut DO production ws generlly high in Hog Islnd By, except t Shol nd Creek in the summer, nd eroic minerliztion t the sediment surfce my hve decresed the DFAA flux to the wter column. The high gross minerliztion rte t our s ( mmol m 2 d 1 N; Anderson et l. 200) further indictes tht DFAA could hve een consumed within the sediments y cteri (Lomstein et l. 1998) or microlge, which re cple of oth light nd drk DFAA uptke (Jorgensen 1982; Admirl et l. 1984; Nilsson nd Sundck 1996). Drk uptke of DFAA my provide competitive dvntge to uried microlge (Nilsson nd Sundck 1996). Consistent with this prediction, we oserved significntly greter drk influx of DFAA nd the gretest DFAA uptke occurred t WW, where DO production ws high. The greter drk uptke suggests tht microlgl uptke my hve een importnt, ut uptke y heterotrophic microes ws lso prole contriutor to the net influx from the wter column. Influence of mcrolge on enthic pelgic coupling It is cler tht on n nnul sis, mcrolgl uptke controlled the movement of DIN, ure, nd DFAA etween the sediment nd wter column t Shol nd my therey uncouple sediment wter column interctions. In phytoplnkton-dominted esturies, sediments my contriute 28 5% of the N to support new primry production (Fisher et l. 1982). In this study, the efflux of DIN nd ure ws sufficient to meet 27 75% of the mcrolgl uptke (second numer djusted for high iomss). Some dditionl N ws likely supplied y recycling within the mcrolgl mt (McGlthery et l. 1997; Trimmer et l. 2000). The increse in tissue N oserved t Shol in lte summer, which corresponded to high NH 4, NO, nd ure uptke, ws likely due to the sesonl relese of N from these sediments. The N uptke rtes reported here (NH 4, 0 5 mol g dw 1 h 1 ) re much lower thn the mximum uptke rtes reported for n opportunistic green mcrolg such s U. lctuc (V mx for NH4 18 mol g dw 1 h 1 ; Fujit 1985), ut proly re more representtive of true field uptke ecuse of the low wter column concentrtions present in Hog Islnd By. Mcrolgl N demnd (s mesured uptke) ws met y severl forms of dissolved N, with DON plying n incresingly importnt role s DIN vilility decresed. When DIN (generlly s NH 4 ) ws redily ville in the wrmer months, it constituted the mjority of uptke (75% of men uptke, ll s). Nonetheless, ure (%) ws more importnt thn NO (9%) overll nd ws more importnt seson- lly thn either NH4 or NO. Men DFAA uptke ws lso very low (% of totl), ut likewise temporlly importnt during colder months. Other studies hve shown temporl importnce of ure (Bronk nd Gliert 199) nd DFAA (Mulhollnd et l. 2002) in stisfying the N demnd of phytoplnkton. In ddition, Admirl et l. (1984) showed tht ditoms were cple of more rpid DFAA uptke t times of low DIN vilility. Where DIN concentrtions were lowest, t the Hog, DFAA nd ure comprised nerly 90% of the totl nnul uptke of known compounds (.6 mmol m 2 yr 1 s DIN, ure, nd DFAA). If we include uptke of unknown DON compounds (8.4 mmol m 2 yr 1 ), it is evident tht DON provided nerly ll of the mcrolgl N demnd. Little is known out the uptke kinetics or importnce of DON to mcrolge (Lon nd Hrrison 1997), ut uptke rtes of ure nd DFAA y U. lctuc cn e sustntil (Tyler unpul. dt) nd growth of mcrolge using ure cn e equivlent to those using DIN (e.g., Nvrro-Angulo nd Roledo 1999). Recently, the importnce of DON in nutri-

11 Algl control of nitrogen fluxes 2 ent-poor ecosystems hs received greter ttention, nd it hs een suggested tht plnts growing in these depuperte environments my e etter dpted to use DON, rther thn DIN (Vn Breemn 2002). If this is true, then the Hog mcrolge my e etter cclimted to, or hve induced uptke mechnisms for, DON uptke. U. lctuc ppered to ssimilte ll mesured DFAA (except His), nd Gly nd Ser in prticulr were selectively tken up reltive to their wter column concentrtions. This contrsts with sediment uptke, where His ws n importnt component of the DFAA influx. The higher uptke rtes of DFAA nd ure in the drk re difficult to explin, prticulrly ecuse wter column relese ws not greter (dt not shown). However, s proposed for microlge, drk uptke my provide competitive dvntge when DIN concentrtions re low or during turidity events. Accumultions of mcrolge t the mid-lgoon Shol ppered to control oth sesonl nd internnul vriility in N fluxes. During July 1998, ptches of the mcrolgl loom crshed, relesing very high quntities of oth DON nd DIN to the wter column (Tyler et l. 2001) nd stimulting phytoplnkton production (McGlthery et l. 2001); this episodic relese ws not oserved during the present study, despite higher iomss in the summer of The high-sediment O 2 consumption, DON uptke, nd DIN relese during July 1999 suggest tht the sediments eneth the dense mcrolgl mt were heterotrophic nd ll ville DON ws rpidly minerlized to DIN. Trimmer et l. (2000) showed enhnced rtes of minerliztion eneth mcrolgl mts, which cn led to high nutrient concentrtions within the mt (McGlthery et l. 1997). The sustined sediment relese tht we oserved in the sence of mcrolge (sediment-only cores) indictes tht minerlized mcrolgl detritus ws slowly relesed from the sediments s DIN nd DON during our incutions. In the previous yer, when ptches of the dense mcrolgl mt t the Shol crshed, we oserved n efflux of DIN only where the overlying mt crshed (Tyler et l. 2001), in spite of high minerliztion rtes eneth the living mt nery (Anderson et l. 200). This suggests tht internnul vriility in microlgl ctivity, mcrolgl iomss, nd other fctors leding to mt persistence my ultimtely govern N relese from the sediments. In ddition to supplying orgnic mtter for minerliztion within the sediments, mcrolgl mts hve other potentil impcts on enthic pelgic coupling. Dense mts decrese light vilility t the sediment surfce (90%; Kruse-Jensen et l. 1996), which my inhiit microlgl growth nd explin the inverse reltion etween mcrolgl iomss nd oth sediment Chl nd sediment DO production. A possile decrese in microlgl ctivity eneth mcrolgl mts due to shding my foster greter relese of N to the wter column. In ddition, like microlge, the diel shifts in redox t the sediment surfce induced y DO production nd consumption my influence N fluxes. For exmple, noxi eneth the mt my prevent nitrifiction nd therey increse the NH4 flux from the sediments to the overlying mcrolgl mt. Our clculted mcrolgl N uptke my e n underestimte of in situ conditions ecuse it does not ccount for the longer-term effect of mcrolge reducing light nd oxygen t the sediment surfce, which would stimulte sediment N relese. However, the impct on enthic pelgic coupling remins the sme nd y intercepting sediment wter column N fluxes, mcrolgl mts my outcompete phytoplnkton for sediment-derived nutrients (McGlthery et l. 1997; Vliel et l. 1997). In our previous work, we documented lrge DON relese y living mcrolge; in the presence of mcrolge, enthic DON relese ws 250% higher (Tyler et l. 2001). In the current study, the vriility in totl DON fluxes ws sufficiently high tht there ws not significnt effect of the mcrolge on the fluxes. However, we found tht the men enthic flux of DCAA incresed nerly eightfold in the presence of mcrolge, which corroortes our previous work (Tyler et l. 2001) nd gives new informtion on the nture of leked orgnic mtter. The higher relese of DCAA in the light suggests tht this relese is photosyntheticlly driven process, lthough Hrlin nd Crigie (1975) found no difference in light drk DON relese rtes for rown mcrolge. Phytoplnkton my relese 25 41% of DIN uptke s DON on short time scles (Bronk et l. 1994) nd much of this relese my e DFAA nd DCAA (Flynn nd Berry 1999). Jorgensen (1982) found incresed wter column DFAA in the presence of U. lctuc, ut sed on the mino cid composition concluded tht the DFAA were exudtes from cteri stimulted y lgl DON relese. It is possile tht this lgl DON relese my hve een DCAA. In the current study, mcrolgl DCAA relese ws 22% of the totl N tken up, indicting sustntil loss of N to the wter column. Wheres in some cses the DCAA in esturine wters my not e ville for cteril utiliztion (Keil nd Kirchmn 199), others hve suggested tht DCAA re n importnt sustrte for cteril growth (Hgstrom et l. 1984). If the relesed DCAA re ioville, these exudtes will fuel heterotrophic ctivity in the wters surrounding mcrolgl mt (Vliel et l. 1997) nd increse the oxygen demnd. This rpid relese of N suggests tht mcrolgl N turns over t two different rtes fter uptke: rpid relese s DCAA (nd other compounds) nd slower relese during senescence. The rpid uptke nd relese indictes tht ctul uptke is gretly underestimted if sed solely on tissue N. In conclusion, our work hs shown tht ecuse of temporl nd sptil vriility in enthic primry producers, the reltive role of the enthos in regulting sediment wter column fluxes cn vry considerly from yer to yer nd even over short distnces in smll, shllow lgoon. Autotrophic sediments with undnt microlge took up dissolved N; conversely, heterotrophic sediments, prticulrly those eneth mcrolgl mts, relesed dissolved N. DIN, primrily s NH 4, ws the dominnt nd most predictle component of the sediment wter column N flux, ut DON ws lso n importnt constituent of fluxes nd dominted the wter column TDN pool. Likewise, mcrolgl N demnd ws met primrily y elevted sediment DIN fluxes in the summer, ut when DIN stnding stocks nd fluxes were low, smll DON compounds, such s ure nd DFAA, were importnt N sources. Where dense mcrolgl mts occur, lge controlled enthic pelgic coupling of TDN y intercepting DIN fluxes nd susequently rerelesing DON to the wter column. Relese of DCAA nd other DON compounds

12 216 Tyler et l. y living mcrolge my led to elevted heterotrophic ctivity in the wter column of mcrolgl-dominted lgoons. The primry producers in shllow estury such s Hog Islnd By re clerly importnt in determining the trnsformtions nd retention of N pssing from the lnd through the lgoon nd out to the costl ocen. References ADMIRAAL, W., R. W. P. LAANE, AND H. PELETIER Prticiption of ditoms in the mino cid cycle of costl wter; uptke nd excretion in cultures. Mr. Ecol. Prog. Ser. : AN, S., AND S. B. JOYE Enhncement of coupled nitrifiction denitrifiction y enthic photosynthesis in shllow esturine sediments. Limnol. Ocenog. 46: ANDERSON, I. C., K. J. MCGLATHERY, AND A. C. TYLER Microil medition of rective nitrogen trnsformtions in temperte lgoon. Mr. Ecol. Prog. Ser. 246: BLACKBURN, T. H., P. O. J. HALL, S. HULTH, AND A. LANDEN Orgnic-N loss y efflux nd uril ssocited with low efflux of inorgnic N nd with nitrte ssimiltion in Arctic sediments (Svlrd, Norwy). Mr. Ecol. Prog. Ser. 141: BOUCHER, G., AND R. BOUCHER-RODONI In situ mesurement of respirtory metolism nd nitrogen fluxes t the interfce of oyster eds. Mr. Ecol. Prog. Ser. 44: BRONK, D. A., AND P. M. GLIBERT Appliction of N trcer method to the study of dissolved orgnic nitrogen uptke during spring nd summer in Chespeke By. Mr. Biol. 1: ,, AND B. B. WARD Nitrogen uptke, dissolved orgnic nitrogen relese, nd new production. Science 265: BURDIGE, D. J., AND C. S. MARTENS Biogeochemicl cycling in n orgnic-rich costl mrine sin: 10. The role of mino cids in sedimentry cron nd nitrogen cycling. Geochim. Cosmochim. Act 52: , AND Biogeochemicl cycling in n orgnicrich costl mrine sin: 11. The sedimentry cycling of dissolved, free mino cids. Geochim. Cosmochim. Act 54: , AND S. ZHENG The iogeochemicl cycling of dissolved orgnic nitrogen in esturine sediments. Limnol. Ocenog. 4: DOLLAR, S. J., S. V. SMITH, S. M. VINK, S. OBRESKI, AND J. T. HOLLIBAUGH Annul cycle of enthic nutrient fluxes in Tomles By, Cliforni, nd contriution of the enthos to totl ecosystem metolism. Mr. Ecol. Prog. Ser. 79: 1 5. FISHER, T. R., P. R. CARLSON, AND R. T. BARBER Sediment nutrient regenertion in three North Crolin esturies. Estur. Cost. Shelf Sci. 14: FLYNN, K. J., AND L. S. BERRY The loss of orgnic nitrogen during mrine primry production my e significntly overestimted when using N- sustrtes. Proc. R. Soc. Lond. B 266: FUJITA, R. M The role of nitrogen sttus in regulting trnsient mmonium uptke nd nitrogen storge y mcrolge. J. Exp. Mr Biol. Ecol. 92: GOEYENS, L., N. KINDERMANS, M. A. YUSUF, AND M. ELSKENS A room temperture procedure for the mnul determintion of ure in sewter. Estur. Cost. Shelf Sci. 47: HAGSTROM, A., J. W. AMMERMAN, S. HENRICHS, AND F. AZAM Bcterioplnkton growth in sewter: II. Orgnic mtter utiliztion during stedy-stte growth in sewter cultures. Mr. Ecol. Prog. Ser. 18: HARLIN, M. M., AND J. S. CRAIGIE The distriution of photosynthte in Ascophyllum nodosum s it reltes to epiphytic Polysiphoni lnos. J. Phycol. 11: HENRICHS, S. M., J. W. FARRINGTON, AND C. LEE Peru upwelling region sediments ner S. 2. Dissolved free nd totl hydrolyzle mino cids. Limnol. Ocenog. 29: HOPKINSON, C. S Nutrient regenertion in shllow-wter sediments of the esturine plume region of the nershore Georgi Bight, USA. Mr. Biol. 94: JONES, B. N., S. PAABO, AND S. STEIN Amino cid nlysis nd enzymtic sequence determintion of peptides y n improved o-phthldildehyde precolumn leling procedure. J. Liq. Chromtogr. 4: JORGENSEN, N. O. G Heterotrophic ssimiltion nd occurrence of dissolved free mino cids in shllow estury. Mr. Ecol. Prog. Ser. 8: KEIL, R. G., AND D. L. KIRCHMAN Dissolved comined mino cids: Chemicl form nd utiliztion y mrine cteri. Limnol. Ocenogr. 8: KRAUSE-JENSEN, D., K. J. MCGLATHERY, S. RYSGAARD, AND P. B. CHRISTENSEN Production within dense mts of the filmentous mcrolg Chetomorph linum in reltion to light nd nutrient vilility. Mr. Ecol. Prog. Ser. 14: LOBBAN, C. S., AND P. J. HARRISON Seweed ecology nd physiology. Cmridge Univ. Press. LOMSTEIN, B. A., T. H. BLACKBURN, AND K. HENRIKSEN Aspects of nitrogen nd cron cycling in the northern Bering Shelf sediment. I. The significnce of ure turnover in the minerliztion of NH 4. Mr. Ecol. Prog. Ser. 57: , A.-G. U. JENSEN, J. W. HANSEN, J. B. ANDREASEN, L. S. HANSEN, J. BERNTSEN, AND H. KUNZENDORF Budgets of sediment nitrogen nd cron cycling in the shllow wter of Kneel Vig, Denmrk. Aqut. Micro. Ecol. 14: MARTENS, C. S Biogeochemistry of orgnic-rich costl lgoon sediments. Ocenol. Act 5: MCGLATHERY, K. J., I. C. ANDERSON, AND A. C. TYLER Mgnitude nd vriility of enthic nd pelgic metolism in temperte costl lgoon. Mr. Ecol. Prog. Ser. 216: 1.,D.KRAUSE-JENSEN, S.RYSGAARD, AND P. B. CHRISTENSEN Ptterns of mmonium uptke within dense mts of the filmentous mcrolg Chetomorph linum. Aqut. Bot. 59: MULHOLLAND, M. R., C. J. GOBLER, AND C. LEE Peptide hydrolysis, mino cid oxidtion, nd nitrogen uptke in communities sesonlly dominted y Aureococcus nophgefferens. Limnol. Ocenogr. 47: NAVARRO-ANGULO, L., AND D. ROBLEDO Effects of nitrogen source, N:P rtio nd N-pulse concentrtion nd frequency on the growth of Grcilri corne (Grcilriles, Rhodophyt) in culture. Hydroiologi 99: 20. NEIKIRK, B Exchnges of dissolved inorgnic nitrogen nd dissolved orgnic cron etween slt mrsh sediments nd overlying wter. Mster s thesis, College of Willim nd Mry, Gloucester Point, Virgini. NILSSON, C., AND K. SUNDBACK Amino cid uptke in nturl microphytoenthic ssemlges studied y microutordiogrphy. Hydroiologi 2: NOWICKI, B. L., AND S. W. NIXON Benthic nutrient reminerliztion in costl lgoon ecosystem. Esturies 8: OERTEL, G. F Hypsogrphic, hydro-hypsogrphic nd hydrologicl nlysis of costl y environments, Gret Mchipongo By, Virgini, USA. J. Cost. Res. 17: