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Estuarine, Coastal and Shelf Science 77 (2008) 422e432www.elsevier.com/locate/ecss

Degradation of phytoplankton-derived organic matter: Implicationsfor carbon and nitrogen biogeochemistry in coastal ecosystems

Michael S. Wetz*, Burke Hales, Patricia A. Wheeler

College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, USA

Received 15 January 2007; accepted 3 October 2007

Available online 29 October 2007

Abstract

Experiments were conducted using seawater from the Oregon continental shelf to determine: (1) rates of phytoplankton-derived particulateorganic matter (POM) and dissolved organic matter (DOM) degradation by natural microbial communities, and (2) whether inorganic nutrientsor flagellate grazing limit the bacterial response to, and subsequent degradation of, the DOM. In the initial seawater samples, nutrients weredepleted and organic matter concentrations were elevated above concentrations found in upwelled water, indicative of recent bloom conditions.In whole water treatments incubated for 3 d, an average of 24% of the total organic C and 33% of the POC was degraded, with some portion ofthe POC being converted to DOC. In treatments incubated after POM was removed by filtration, DOC degradation was initially rapid and thenproceeded at a slower rate. After 3 d, an average of 41% of the DOC was degraded. Selective degradation of the C-component of both the POMand DOM relative to the N-component was observed. Reductions in flagellate grazing resulted in increases in bacterial abundance and enhancedDOC degradation, while inorganic nutrient amendments had little effect. Overall, these results suggest that a fraction of the phytoplankton-derived POM and DOM can be rapidly degraded, contributing to oxygen consumption on the continental shelf. The long degradation timeof a less labile DOC fraction relative to potential offshelf transport mechanisms suggests that Oregon’s coastal waters may be a source ofDOC to adjacent offshore waters of the North Pacific.� 2007 Elsevier Ltd. All rights reserved.

Keywords: dissolved organic matter; particulate organic matter; decay; phytoplankton; diatoms; bacteria; carbon; upwelling

1. Introduction by diatom-dominated productivity followed by the transfer of

Eastern boundary current upwelling systems are sites ofseasonally intense organic matter production and processing,accounting for w10e15% of global ocean new production(Chavez and Toggweiler, 1995). Important exchanges of carbon(C) take place between the air and sea in these regions, withsignificant implications for global C budgets. For example,the upwelling system off Oregon is a major sink for atmosphericCO2 during the summer upwelling season (Hales et al., 2005a).This net influx of CO2 from the atmosphere is facilitated

* Corresponding author. Present address: The University of North Carolina-

Chapel Hill, Institute of Marine Sciences, 3431 Arendell Street, Morehead

City, NC 28557, USA.

E-mail addresses: wetz@email.unc.edu (M.S. Wetz), bhales@coas.

oregonstate.edu (B. Hales), pwheeler@coas.oregonstate.edu (P.A. Wheeler).

0272-7714/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2007.10.002

particulate organic matter (POM; i.e., phytoplankton biomass)from surface to bottom waters and ultimately offshelf to deeperwaters (Hales et al., 2006). Some of the POM may be sufficien-tly labile such that it is degraded on timescales shorter than thoseof export events, contributing to shelf respiration and develop-ment of coastal hypoxia (e.g., Grantham et al., 2004). Fewstudies have attempted to quantify diatom POM degradationrates in coastal systems, hindering efforts to understand andmodel the biogeochemistry of this important fraction of C, Nand P biogeochemical cycles.

In addition to POM, some of the diatom production accumu-lates as C-rich dissolved organic matter (DOM) (Williams,1995; Alvarez-Salgado et al., 2001a; Hill and Wheeler, 2002;Wetz and Wheeler, 2004). This DOM is derived from eitherexcretion by phytoplankton or trophic interactions leadingto DOM liberation (i.e., grazing, viral lysis) (reviewed by

Table 1

Experimental treatments employed in this study

Treatment Description

<0.8 mmþHgCl2 Control for abiotically induced changes

<0.8 mmþNutrients Contains bacterial assemblage but no bacterivores,

alleviates nutrient limitation

<0.8 mm Contains bacterial assemblage but no bacterivores

<3 mmþNutrients Contains bacterial and bacterivore assemblages,

alleviates nutrient limitation

<3 mm Contains bacterial and bacterivore assemblages

Whole Contains phytoplankton, bacterial and bacterivore

assemblages

423M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

Carlson, 2002). In contrast to POM, which can sink out ofsurface waters, export of DOM is largely limited to advectiveprocesses. Recent studies suggest that autochthonous DOMmay be exported from coastal systems (Hopkinson et al., 2002),including those influenced by seasonal upwelling (Alvarez-Salgado et al., 2001a,b). Alvarez-Salgado et al. (2001a) arguedthat depending on the lability of the DOM, the export flux tooligotrophic offshore surface waters from coastal upwellingsystems might be sufficiently large to alter the balance betweenpelagic heterotrophy and autotrophy in the oligotrophic systems.

It is not entirely clear why DOM accumulates and persistsin coastal systems, although several environmental factorshave been proposed as potentially limiting bacterial use ofthe DOM. Bacterivory by flagellates (McManus and Peterson,1988; Sanders et al., 1992; Li et al., 2004), a lack of inorganicnutrients (Zweifel et al., 1993; Barbosa et al., 2001), or a com-bination of both factors (Thingstad et al., 1997) are amongthe most common factors reported. It has also been arguedthat some fraction of the DOM may simply be resistant todegradation over relevant timescales (Søndergaard et al.,2000; Barbosa et al., 2001).

Because coastal systems are highly productive and are im-portant to both regional and global biogeochemical cycles andfood webs, it is necessary to quantify organic matter degrada-tion rates and to understand what regulates the degradation incoastal systems. This, combined with knowledge of circulationpatterns and shelf water residence times, will help to betterunderstand and model ecosystem-level processes and biogeo-chemical cycles in those systems. In this paper, results are pre-sented from experiments designed to quantify degradationrates of phytoplankton-derived DOM and POM from Oregon’scoastal waters, and to test whether nutrients and/or flagellategrazing limit the bacterial response to accumulated DOM.The Oregon upwelling system is an ideal, representativecoastal location to study phytoplankton-derived organic matterdegradation and controls upon its degradation. Large, episodicphytoplankton blooms occur here over the continental shelf inthe spring through fall, and as these blooms become nutrient-limited, significant quantities of DOM accumulate (Hill andWheeler, 2002; Wetz and Wheeler, 2003). In many ways,the bloom dynamics off Oregon are similar to those in othercoastal settings. Bloom development off Oregon is spurredby injection of inorganic nutrients into the euphotic zone viaupwelling, followed by water column stratification (Smalland Menzies, 1981). After a few days to weeks, bloom senes-cence initiates when the inorganic nutrients are depleted.These patterns of bloom dynamics are not dissimilar to otherhighly productive coastal systems, although the nutrient sourcemay differ (e.g., riverine vs. upwelled) (reviewed by Cloern,1996). In addition, it appears that the phylogenetic compositionof the bacterial community that responds to the blooms is alsosimilar between Oregon (Longnecker et al., 2006; Morris et al.,2006) and other coastal systems (e.g., Kerkhof et al., 1999; Rie-mann et al., 2000), suggesting that results will be comparablebetween systems. Finally, the Oregon upwelling system isa good location for studying degradation of phytoplankton pro-duction because recent field efforts have made major advances

in understanding and modeling circulation there (e.g., as sum-marized by Barth and Wheeler, 2005), which is necessary toput degradation studies in a larger context of water mass trans-port, export of non-degraded organic matter and regional andglobal biogeochemical budgets.

2. Methods

2.1. Background and experimental design

Experiments were run on three dates in 2005; 18 April, 4August and 16 September. The April experiment was run us-ing water from a laboratory-grown diatom-dominated bloomthat had depleted nitrate 1 d prior to the start of these experi-ments. The bloom was initiated from water collected on the in-coming tide in Yaquina Bay, Newport, Oregon. The dominantphytoplankton species were the diatoms Thalassiosira sp. andGuinardia sp. The August and September experiments wererun using surface water collected from mid-shelf locationsoff Newport, Oregon (44�39.10 N, 124�17.70 W and 44�39.30

N, 124�24.70 W, respectively). Upwelling off Oregon typicallypeaks in July/early August and declines in late August throughSeptember. Upwelling was occurring at the time of the 4 Au-gust experiments and a large diatom bloom that had depletednitrate was in place. A mixture of diatoms dominated thebloom, including Asterionellopsis sp., Thalassiosira sp., Chae-toceros sp., Skeletonema sp., and Guinardia sp. 15 Septemberfollowed a period of prolonged (>1 week) light winds andconditions showed no indication of active upwelling basedon the temperature and salinity characteristics of the water.However, POM was still elevated and was likely bloom-derived since significant riverine input of terrestrial POMonly occurs in the winter off Oregon (e.g., Wetz et al.,2006a). Phytoplankton identification samples were not col-lected for the September experiment.

An unamended (i.e., whole water) treatment was set up toexamine POM and DOM degradation as it would occur in situ.Experimental water was also exposed to five treatments desig-ned to test whether nutrient limitation and/or grazing controlthe abundance of coastal bacteria and affect degradation oforganic matter (Table 1). To do this, treatments with (i.e.,<3 mm filtered) and without (i.e., < 0.8 mm filtered) heterotro-phic flagellates (HFLAG), and treatments with and withoutinorganic nutrient amendments were employed. A control

424 M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

treatment to account for abiotic losses of organic carbon wasprepared by adding saturated HgCl2 to <0.8 mm filtered water.Both the <0.8 mm and <3 mm treatments represent the naturalmicrobial communities except that nearly all fresh algal POMis removed by gently filtering raw seawater through 142 mmGF/D filters. Previous incubation (Wetz and Wheeler, 2003)and field measurements (Sherr et al., 2005) have shown that dur-ing blooms off Oregon, most of the phytoplankton biomass(>95%) is in the>3 mm size fractions. The<0.8 mm treatmentswere set up by filtering raw seawater through 142 mm, 0.8 mmpolycarbonate membrane filters. Prior to filtering seawaterthrough the membrane filters, w500e1000 ml of deionizedwater was filtered to minimize contamination caused by leach-ing of organic matter from the filters. Treatments involvingnutrient additions were spiked with 11e16 mmol L�1 NH4Cland 3e5 mmol L�1 KH2PO4. It should be noted that while theseadditions were designed to alleviate inorganic nutrient limita-tion, they do not necessarily mimic natural conditions foundduring upwelling bloom senescence, when recycling withinthe euphotic zone is the only significant source of nutrients.

In this manuscript, data are presented showing the initialDOC or TOC concentrations, as well as observed changes intheir concentrations over time. Additionally, the percentageof initial ‘‘excess’’ DOC or TOC that degraded over the courseof the experiments is reported. ‘‘Excess’’ DOC or TOC is de-fined here as the concentration of initial organic C that waspresent in excess of concentrations found in upwelled waters.The upwelled organic C is presumably refractory, and thereforeshould not be considered in discussions relating to the degrada-tion of fresh phytoplankton-derived organic C. Data from a 7year sampling program indicates that organic C concentrationsaverage 46 mmol L�1 in the halocline (salinity¼ 33e33.5) dur-ing the summer off northern Oregon (Wetz et al., 2006b), whichis the water mass that typically upwells and outcrops at the sur-face in this region (e.g., Wheeler et al., 2003).

After the treatments were prepared, the seawater wasplaced in either 15e20 L tri-laminate gas impermeable bags(April experiment; Kruse, 1993) or 3e10 L high-density poly-ethylene Cubitainers (August and September experiments) andincubated in the dark at 12 �C. Recently upwelled water offthe Oregon coast generally averages w8e10 �C, but as a par-cel of water advects away from the core zone of active upwell-ing, temperatures rise to �12 �C over a period of days toa week due to surface heating (e.g., Barth et al., 2005). Itwould be during this 3e7-d time period that the phytoplanktonblooms mature and reach senescence, and this would also bewhen the potential for degradation of the phytoplankton-derived organic matter is maximal. For the April experiment,water was continuously circulated through the bags, while inAugust and September, the Cubitainers were mixed manually1e2 times per day. Samples were collected every 12e24 hover a 3-d period.

2.2. Biological measurements

Bacterial and heterotrophic flagellate (HFLAG) abundanceswere determined from duplicate samples taken from each

experimental bag. Upon collection, bacteria samples werepreserved with 3% (final. conc.) borate-buffered formalin.Immediately after preservation, 5 mL samples were stainedwith 2.5� (final. conc.) SYBR Gold in the dark for 10 min.After staining, the samples were filtered (<200 mm Hg) onto0.02 mm Acrodisc filters and stored at �20 �C until analysis.Slides were viewed on an Olympus BX-61 epifluorescent mi-croscope at 1000� magnification and five fields were countedper slide. Size measurements were made on �50 cells per slidewith a SensiCamQE CCD camera calibrated with an ocular mi-crometer. Length, width and areal dimensions of the cells wereconverted to biovolume, and cell C estimated assuming a rela-tively conservative carbon: volume ratio of 120 fg C mm�3

(Ducklow, 2000). Samples for HFLAG abundance determina-tions were preserved in a three-step process with additions of0.06% (final conc.) alkaline Lugols solution, 3% (final conc.)borate-buffered formalin and 0.12% (final conc.) sodium thio-sulfate. After preservation, the samples were stored at 4 �C for12 h to allow the HFLAG to shrink and harden. A subsamplefrom each replicate was stained with DAPI (final conc.25 mg ml�1 sample) for 10 min in the dark, and then filteredthrough a 0.8 mm polycarbonate membrane filter. Sampleswere analyzed at 600� magnification using an OlympusBX-61 epifluorescent microscope and 20 fields per slide werecounted.

2.3. Chemical measurements

Nutrient samples were collected in duplicate acid-washed30 ml HDPE bottles and immediately frozen at �30 �C. Sam-ples were analyzed on a Technicon AA-II according to standardwet chemical methods of Gordon et al. (1995). Standard curveswith four different concentrations were run daily at the begin-ning and end of each run. Fresh standards were made prior toeach run by diluting a primary standard with low nutrient sur-face seawater. Deionizied water (DIW) was used as a blank,and triplicate DIW blanks were run at the beginning and endof each run to correct for baseline shifts.

Total nitrogen (TN) samples were collected in duplicateacid-washed 30 ml Teflon bottles and immediately frozen at�30 �C until analysis. Organic N was converted to nitrate us-ing a persulfate wet oxidation method (Libby and Wheeler,1997), and then analyzed using a Technicon AA-II. Instrumentcalibration was performed daily using a standard curve pre-pared from triplicate digested leucine standards at three con-centrations. Fresh standards were made prior to each run bydiluting a primary standard with artificial seawater. Digestedartificial seawater was used as a blank, and the standard curvewas corrected for N content of the blank by determining theconcentration of N in the persulfate solution and then calculat-ing the amount of N in the artificial seawater. Artificial seawa-ter N content was estimated as the difference between theblank and persulfate signals.

Total organic carbon (TOC) samples were collected in acid-washed borosilicate vials with Teflon cap liners. Each vialcontained approximately 5 ml of seawater that was preservedwith 50 ml of 90% phosphoric acid. Samples were stored at

425M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

room temperature until processing using the High TemperatureCatalytic Combustion method on a Shimadzu TOC-5000A an-alyzer. Standard curves were run twice daily using a DIWblank and four concentrations of an acid potassium phthalatesolution. Three to five subsamples were taken from each stan-dard and water sample and injected in sequence. Variance be-tween subsamples averaged 1.5� 1.2%. Certified ReferenceMaterial Program (CRMP) deep-water standards of knownTOC concentration were injected in triplicate at the beginning,middle, and end of each run to account for baseline shifts. Thedata from each date were then normalized to the average dailyCRMP TOC concentration. Average daily CRMP TOC con-centrations (05e04 batch) were 43.1� 2.2 mmol L�1.

For the April experiment, we also analyzed the total dis-solved inorganic C (tCO2) using a modification of the Bandstraet al. (2006) method. These measurements showed that therewas closure for the total C budget in the experimental incuba-tion containers. That is, decreases in TOC were matched by in-creases in tCO2. Because we made these measurements on onlya subset of the experiments and they served only to confirm theTOC-based results, we do not present the tCO2 data here.

Particulate organic carbon (POC) and particulate organicnitrogen (PON) were determined from material that was vac-uum filtered (<200 mm Hg) onto precombusted GF/F filters.After filtration, filters were stored in glass Vacutainers� andimmediately frozen at �30 �C until laboratory analysis. Filterswere fumed with concentrated HCl to remove inorganic C anddried, followed by analysis using a Control Equipment Corp.440HA CHN elemental analyzer calibrated with acetanilide.During analysis, filter blanks were run after every 12 samples.Filter blanks averaged 17.6� 2.9 mg C and 1.1� 0.8 mg N,and these values were subtracted from each measured valueas a blank correction. The analytical uncertainty, representedas the average coefficient of variation of duplicate samples,was 2% for both POC and PON.

Dissolved organic carbon (DOC) was determined bysubtracting POC values from TOC values. Dissolved organicnitrogen (DON) was determined by subtracting PON andDIN (NH4

þ, NO2�þNO3

�) from TN.

3. Results

3.1. Initial conditions

Table 2

Initial organic C (mmol L�1) and organic nitrogen concentrations (mmol L�1),

and the C:N (mol:mol) of the organic matter

Experiment [DOC] [DON] DOM C:N [POC] [PON] POM C:N

April 155.3 12.0 13.0 324.5 26.3 12.3

August 105.1 10.0 10.5 246.9 24.5 10.1

September 58.3 8.2 7.1 108.5 15.8 6.9

For each experiment, nitrate and ammonium were belowdetection limits (w0.26 and 0.05 mmol L�1, respectively) inthe raw seawater used to initiate each experiment, except inApril where some ammonium was detected (w0.17 mmol L�1)(data not shown). Phosphate concentrations were always abovedetection limits (w0.02 mmol L�1), averaging 0.08 mmol L�1

in April, 0.33 mmol L�1 in August, and 0.16 mmol L�1 inSeptember (data not shown). Organic matter concentrationswere elevated above those found in recently upwelled water,which off Oregon usually contains w46 mmol L�1 DOC andw4 mmol L�1 DON (Wetz et al., 2006b). Initial mean DOCconcentrations ranged from 58 to 155 mmol L�1, while initialmean DON concentrations ranged from 8 to 12 mmol L�1

(Table 2). Initial POM concentrations in the whole water treat-ments on each date were also high, ranging from 109 to325 mmol L�1 POC and from 16 to 26 mmol L�1 PON (Table 2).

3.2. Organic matter degradation in whole water

On all dates the TOC pool decreased over time and maxi-mum TOC losses after 3 d ranged from 29 to 89 mmol L�1

(Fig. 1A). TOC degradation occurred more rapidly over thefirst 24 h of each experiment than over the proceeding 2 d(Fig. 1A). In September, TOC degradation actually ceased af-ter the first 24 h (Fig. 1A). POC initially increased during thefirst day of the April experiment, after which degradation pro-ceeded rapidly for 1 d and then slowed (Fig. 1A). In Augustand September, POC degradation began in the first 12 h andproceeded almost linearly over the 3-d period (Fig. 1A). Max-imum POC losses in the three experiments ranged from 34 to159 mmol L�1. After 1 d, 0e13% of the POC had been de-graded and the net degradation of excess TOC ranged from5% to 26% (mean¼ 16� 11%) of initial concentrations. After3 d, 17e49% (mean¼ 33� 16%) of the POC had been de-graded and the net degradation of excess TOC ranged from16% to 32% (mean¼ 24� 8%) of initial concentrations.

The pathway of POC breakdown involves a conversion ofPOC to DOC, followed by oxidation of DOC to tCO2, andthe relative rates of these processes are not well known. Thefact that all experiments showed only decreases in TOC overtime demonstrates that there is always net organic C degrada-tion, and the fact that there is internal consistency between ourTOC and tCO2 (data not shown) measurements demonstratesclosure of the total C budget. However, individual experimentshint at the multiple steps in the process, particularly in April.The initial POC increase even as TOC decreased, and the sub-sequent rapid POC decrease that actually exceeded TOC deg-radation, can only be the result of cycling between the DOCand POC pools as the organic material was degraded. In theother experiments, the final POC decrease ranged from 48%to 100% of the TOC decrease, but the strong evidence of cy-cling between the DOM and POM pools in the April experi-ment cautions us against further interpreting the relativeoxidation rates of the two pools.

It is important to point out that oxygen could not have beendepleted over the course of these 3-d experiments. While ox-ygen was not directly measured, it is possible to conservativelyestimate the minimum amount of oxygen that would be left af-ter 3 d based on other data. The April experimental water wascollected just after the peak of a large, laboratory-grown dia-tom bloom and was free to exchange with the laboratory air.

-250

-200

-150

-100

-50

0

50

Apr POC

Apr TOC

Aug POC

Aug TOC

Sep POC

Sep TOC

-5

-4

-3

-2

-1

0

1

2

3

4

5

Day0

Apr PON Aug PON

Sep PON Apr TON

Aug TON Sep TON

B

A

4321

Org

anic

N c

hang

e (µ

mol

L-1

)O

rgan

ic C

cha

nge

(µm

ol L

-1)

Fig. 1. (A) Change in POC and TOC, and (B) change in PON and TON in

April, August, and September whole water treatments.

426 M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

The August and September experiments were from surfacewaters off the Oregon coast and both had elevated phytoplank-ton biomass and organic matter, indicative of bloom condi-tions. Shelf surface waters off Oregon during the summerare usually supersaturated with respect to oxygen, and surfaceO2 concentrations of well over 200 mmol L�1 are common(Hales et al., 2006). The initiation of these experiments withwaters that had recently experienced a large bloom in quies-cent laboratory conditions in all likelihood resulted in simi-larly strongly O2-supersaturated waters. The maximumamount of organic C that was degraded and the maximumamount of CO2 that accumulated in our experiments wasw87 mmol L�1. If we assume that O2 consumption proceedsat 138 mol O2 per 106 mol C, then the maximum oxygenloss would be on the order of 113 mmol L�1. Thus, after 3 d,the lowest amount of oxygen would be >87 mmol L�1, wellabove hypoxic (w2 mg L�1 or 63 mmol L�1; Rabalais et al.,2002) or anoxic levels.

In contrast to the relatively large amount of organic C deg-radation that took place, organic nitrogen degradation was

minimal (Fig. 1B). In April, PON decreased by 2 mmol L�1

from days 0 to 1, but then returned to near initial concentra-tions for the rest of the experiment (Fig. 1B). April TON con-centrations were unchanged over the 3-d period, not deviatingfrom initial concentrations by more than the analytical uncer-tainty of the measurement (Fig. 1B). August PON did not de-viate significantly from initial concentrations, nor was thereany net change in TON after 2e3 d (Fig. 1B). After 2e3 din September, there was a noticeable decrease in PON (by1.8e3 mmol L�1) and TON (by 2.9e4.2 mmol L�1) (Fig. 1B),although TN concentrations decreased by 1.1e2.3 mmol L�1,indicative of incomplete sampling of the PON pool. Hence,the observed decreases in PON and TON may be over-estimated by a factor of two. The limited PON and TON deg-radation, coupled with the significant degradation of organic C,implies that the C-component of the organic matter was selec-tively remineralized, both for the POM and DOM.

TOC decay constants in the April and August experimentsduring the initial 24 h of incubation were 0.17 and 0.36 d�1,respectively, followed by 0.06 and 0.10 d�1 over the remaining2 d. In September, TOC decay occurred during the first 24 h at0.19 d�1, then ceased. In the August and September experi-ments where POC decreased monotonically over 3 d, decayconstants, calculated as the difference in the natural logarithmof POC between days 0 and 3 divided by 3 d, were 0.06 and0.13 d�1. In April, POC decayed rapidly for a day at0.68 d�1 and then more slowly at 0.04 d�1.

3.3. Impact of nutrient amendments and/or grazingreduction on bacterial abundances and DOMdegradation

Initial bacterial abundances were similar between the <3 mmtreatments and the <0.8 mm treatments on all three dates, indi-cating that the <0.8 mm treatments did not remove a significantportion of the bacterial community (i.e., cells> 0.8 mm) duringexperimental setup. Initial bacterial abundances were generallysimilar for the April and August experiments, ranging from0.2� 106 cells mL�1 to 0.6� 106 cells mL�1 (Table 3), butwere much higher for the September experiment, ranging from1.4 to 1.7� 106 cells mL�1. HFLAG abundances in the <3 mmtreatments in each experiment ranged from 1.5� 103 cells mL�1

to 11.6� 103 cells mL�1 (Table 3). In April, HFLAG abun-dances were an order of magnitude lower in the <3 mm treat-ments than in the whole water because most of the HFLAGwere larger than 3 mm. This contrasts to the other two dateswhere most of the HFLAG were �3 mm. HFLAG abundancesvaried little over the course of each experiment (data not shown).

In the April experiments, there was only a small net increasein bacterial abundance in the <3 mm treatment after 3 d(Fig. 2A). Abundances increased slightly after 1 d in the<3 mmþ nutrients treatment, but subsequently decreased tonear initial levels (Fig. 2A). In August, abundances in the<3 mm and <3 mmþ nutrients treatments initially increasedafter 1 d (Fig. 2B), but subsequently decreased to initial levels.Much of the initial elevated (relative to previous samplingdates) bacterial abundances in September appeared to be

Table 3

Initial bacterial (�106 cells mL�1) and HFLAG abundances

(�103 cells mL�1). Note that due to a sample processing error, no HFLAG

abundances are available for the April< 0.8 mm treatment. Due to contamina-

tion, the September< 0.8 mmþ nuts treatment has also been omitted

Experiment Treatment Bact. abundance HNAN abundance

April <0.8 mmþNuts 0.33 0.1

<0.8 mm 0.59

<3 mmþNuts 0.53 1.5

<3 mm 0.53 1.7

Whole 0.34 23.7

August <0.8 mmþNuts 0.26 0.1

<0.8 mm 0.23 0.1

<3 mmþNuts 0.22 11.6

<3 mm 0.22 9.9

Whole 0.54 10.3

September <0.8 mmþNuts

<0.8 mm 1.44 0.0

<3 mmþNuts 1.60 5.1

<3 mm 1.66 5.3

Whole 1.79 6.5

< 0.8 + nuts< 0.8< 3 + nuts< 3

1

0

-1

B

3

1

1

0

-1

A

0

Day

C

3

2

0

-1

Bac

teri

a ab

unda

nce

chan

ge (

x 10

6 cel

ls m

l-1)

3

2

2

4321

Fig. 2. Change in bacterial abundance (�106 cells mL�1) in (A) April, (B)

August and (C) September experiments.

427M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

readily grazed over the 3-d period, as abundances and biomassin the <3 mm treatment decreased dramatically throughout theexperiment (Fig. 2C) and abundances in the<3 mmþ nutrientstreatment increased slightly after 1 d, but subsequentlydecreased over the next 2 d (Fig. 2C). Abundances in the treat-ment without HFLAG (i.e., <0.8 mm) increased by various de-grees on all three dates (Fig. 2AeC) and remained elevated overthe 3-d period. Likewise, abundances in the <0.8 mmþnutrients treatment increased and remained elevated throughoutthe April and August experiments (Fig. 2A, B). A filter rupturedduring the setup process of the September sample, whichresulted in contamination of that treatment (w/high POC,bacteria, HFLAG, etc.). Thus, it is not included in this analysis.Overall, HFLAG grazing reductions clearly resulted in in-creased bacterial growth in August and September, and to lesserdegree in April.

DOC concentrations varied by an average of only 3.8% inthe fixed control treatment over the course of each experiment(data not shown). For clarity, the DOC data from each exper-iment have been normalized to the mean fixed control DOCconcentration for that experiment. Changes in bacterial andHFLAG C, which would be included in the DOC measure-ments, contributed only minimally to the observed DOCchanges in the first two experiments (i.e., <few mmol L�1 rel-ative to 30e50 mmol L�1 DOC changes). Therefore, it was notnecessary to correct those DOC data for bacterial C biomass.In September, changes in bacterial C (w5e8 mmol L�1) repre-sented a significant portion of the DOC change, and thus thatDOC data have been corrected for bacterial C.

In April and August, DOC degradation began in the first12 h of the experiments (Fig. 3A, B). The only exception wasthe August <0.8 mm treatment, in which noticeable degrada-tion did not start until between 12 and 24 h (Fig. 3B). In Sep-tember, net DOC degradation also occurred in the first 24 h(Fig. 3C). In general, the largest DOC decreases occurred inthe first 24 h, after which degradation proceeded but at slower

pace through the end of the experiments. The total amount ofDOC that was degraded after 3 d on the first two dates rangedfrom 32 to 60 mmol L�1 (Figs. 3A,B), while in September therewas no net DOC degradation in the <3 mm treatment and only3e13 mmol L�1 was degraded in the <3 mmþ nutrients and<0.8 mm treatments (Fig. 3C). As a percentage of the initialexcess DOC pool, 15e64% (mean¼ 34� 20%) was degraded

< 0.8 + nuts< 0.8< 3 + nuts< 3

-60

-50

-40

-30

-20

-10

0

B

-60

-50

-40

-30

-20

-10

0

-60

-50

-40

-30

-20

-10

0

0

Day

C

A

4321

DO

C c

hang

e (µ

mol

L-1

)

Fig. 3. Change in DOC (mmol L�1) in (A) April, (B) August, and (C) September.

-9

-6

-3

0

3

6

9

< 0.8 + nuts

< 0.8

< 3 + nuts

< 3

-9

-6

-3

0

3

6

9

B

C

-9

-6

-3

0

3

6

9

0 1 2 3 4

Day

A

DIN

cha

nge

(µm

ol L

-1)

Fig. 4. Change in DIN (mmol L�1) in (A) April, (B) August, and (C) September.

428 M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

after 1 d and 25e70% was degraded after 3 d (mean¼ 49�19%) in April and August. The net excess DOC degradationthat occurred in two of the September treatments rangedfrom 13% to 44% of the initial concentration. In Augustand September, when reductions in HFLAG grazing (i.e.,<0.8 mm treatments) resulted in significant increases in bac-terial abundance, DOC degradation was enhanced over treat-ments in which HFLAG grazing was not alleviated. Theeffect was less clear in April, when HFLAG grazing reduc-tions had less of an effect on bacterial growth.

The response of the DON pool to the experimental treat-ments varied between experiments. In the April nutrientaddition treatments, DIN decreased dramatically after 3 d

(by 6.8e7.6 mmol L�1; Fig. 4A) and DON accumulated pro-portionally (by 7.2e8 mmol L�1; Fig. 5A). In the non-nutrientaddition treatments, there were only slight (<1 mmol L�1) netincreases in DON or decreases in DIN after 3 d. In contrast tothe April results, DIN increased (by 0.8e5.7 mmol L�1;Fig. 4B, C) and DON decreased (by 2.7e6.6 mmol L�1;Fig. 5B, C) after 3 d in the August and September nutrient ad-dition treatments. However, non-nutrient addition treatmentsresulted in relatively little change in the DON or DIN poolsover 3 d, except in the September <0.8 mm treatment in whichDON decreased by ca. 3.4 mmol L�1 after 3 d (Fig. 5C). Therewere a few sample times and treatments in August andSeptember where net changes in DON occurred, but these

-9

-6

-3

0

3

6

9

< 0.8 + nuts< 0.8< 3 + nuts< 3

-6

-3

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3

6

9

B

-9

-6

-3

0

3

6

9

-9

0

Day

C

A

4321

DO

N c

hang

e (µ

mol

L-1

)

Fig. 5. Change in DON (mmol L�1) in (A) April, (B) August, and (C) September.

429M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

changes were within the analytical uncertainty of the DONmeasurement. These included days 2 and 3 of the<0.8 mmþ nutrients treatment and day 3 of the <3 mm treat-ment in August, days 2 and 3 of the <0.8 mm treatment inSeptember, and day 3 of the <3 mmþ nutrients treatmentand <3 mm treatment in September.

4. Discussion

Off Oregon and in other coastal upwelling systems, periodsof upwelling tend to last for several days to a week and areinterspersed between periods of relaxed or even downwel-ling-favorable winds (Huyer, 1983). As surface water moves

away from the core of the upwelling front or after wind relax-ation or reversals, large phytoplankton blooms can rapidly (<1week) deplete inorganic nutrients while producing significantamounts of organic matter (Kokkinakis and Wheeler, 1987;Wetz and Wheeler, 2003; Hales et al., 2005b). Nutrients(NO3

� and PO43�) were depleted in the raw seawater used to

start each experiment here and organic matter concentrationsexceeded those typically found in recently upwelled waters,indicative of bloom conditions.

Significant quantities of POC were degraded in the wholewater treatments of these experiments. After 3 d, an averageof 33% of the phytoplankton-derived POC had been degraded.The rate constants from the two experiments where POC deg-radation was linear with time (0.06 and 0.13 d�1) are similar tothose from the first rapid phase of degradation reported by Pett(1989), which was w0.08 d�1. A fraction of the POC that wasdegraded was respired, although some of the POC was appar-ently converted to DOC. Nonetheless, in all experiments, therewas still significant net degradation of the TOC accompanyingthe POC breakdown.

Much of the POC derived from diatom blooms in coastal up-welling systems sinks or is mixed to bottom waters via downw-elling, sometimes in as little as a few days (e.g., Karp-Bosset al., 2004). As demonstrated here, a fraction of this POCcan decay rapidly and would contribute to oxygen utilizationin bottom waters if not exported on timescales less than thatof its degradation times. Off Oregon in 2002, severe hypoxicconditions persisted in shelf bottom waters over a severalmonth period during the summer (Grantham et al., 2004).This hypoxia was attributed primarily to anomalous inputs oflow oxygen water onto the shelf at mid-depths. Hales et al.(2006), however, pointed out that the most extreme hypoxicevents in 2002 coincided with a nearly 6-week period of unin-terrupted upwelling-favorable winds which presented few op-portunities for export of the continuously produced diatomorganic matter from the shelf. Hales et al. (2006) speculatedthat if the organic matter raining into near-bottom watersfrom surface diatom blooms was labile on timescales signifi-cantly shorter than 1e2 months, that its degradation couldhave been a significant factor driving the hypoxia observedin 2002. The work reported here strongly supports this notion,demonstrating that a significant fraction of the POC depositedin near-bottom waters over the 6-week period would probablyhave been degraded locally.

In two of three experiments, there was no evidence of sig-nificant PON degradation accompanying the POC degradation,while a small amount of PON was degraded in a third experi-ment. This preferential degradation of the C-component ofPOM relative to the N-component is contrary to various geo-chemical studies showing that as POM sinks, N is preferen-tially remineralized (Lee and Wakeham, 1988; Grossart andPloug, 2001). There is some evidence from the Oregon upwell-ing system that may support this notion of preferential POCdegradation, at least over short timescales. Karp-Boss et al.(2004) found that at a shelf location off central Oregon, surfacewater POM that coincided with elevated phytoplanktonbiomass had a C:N ranging from w8 to 10 (Fig. 11 from

430 M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

Karp-Boss et al., 2004), consistent with the initial conditionsof our experiments. The C:N of POM in the underlying bottomboundary layer was much lower, averaging <6. If the surfacePOM pool were the ultimate source of the bottom POM, as wasthe case for an adjacent site off northern Oregon, then thiswould indicate preferential POC degradation. In laboratoryexperiments that examined oxic degradation of a commonmarine diatom, Harvey et al. (1995) found that the decay ofN-poor cellular carbohydrates proceeded faster than that ofproteins, but this preferential degradation apparently had min-imal impact on the bulk C:N of the diatom POM. One possibleexplanation for the preferential POC degradation seen in ourstudy is that it was due degradation of transparent exopolymerparticles (Koeve, 2005) and not phytoplankton cellular POM.TEP contains very little N relative to C and is often measuredas POM when using glass fiber filters to separate diatom POMfrom DOM (Passow, 2002; Wetz and Wheeler, 2007). Coastaldiatoms can exude large quantities of TEP that drives the C:Nof the POM (as well as the bulk organic matter pool) far aboveRedfield stoichiometry (see Passow, 2002; Wetz and Wheeler,2007). Kepkay et al. (1997) showed that TEP, and hence its as-sociated C, can be remineralized relatively rapidly, and conse-quently TEP is not believed to contribute significantly to theexport and longer-term sequestration of C (Koeve, 2005).

In the treatments where POC was removed and where DOCdegradation was observed, degradation appeared to occur rap-idly over the first day or so before slowing down, consistentwith laboratory degradation dynamics (e.g., Biddanda, 1988;Chen and Wangersky, 1996). After 3 d in the April and Augustexperiments, an average of 49% of the DOC had been de-graded. In September, the initial DOC concentrations weremuch lower than in April or August, while bacterial biomasswas elevated. Net DOC degradation only occurred after 3 din one of the three treatments, while in the others, mineraliza-tion (by HFLAG) of bacterial C biomass to the DOC poolappeared to negate any net DOC degradation.

Based on the high DOC concentrations and the lack of mea-surable nutrients observed during bloom senescence in situand at the start of these experiments, it would be temptingto speculate that nutrients limit the bacterial response to thelarge supplies of fresh phytoplankton DOC. Our results argueagainst this and instead suggest that grazing is a much moreimportant control on bacterial abundances and biomass as op-posed to nutrients, which supports the findings of previousstudies in high-productivity coastal systems (e.g., Sanderset al., 1992; Li et al., 2004). Reductions in grazing led tonet increases in bacterial abundance and biomass in two ofthree experiments, and also to enhanced DOC degradation.In a third experiment (April), grazing reductions did not elicitthe obvious bacterial response seen in the other two experi-ments, presumably because most of the HFLAG in Aprilwere �3 mm and likely were not bacterivores (e.g., Hansenet al., 1994). It is important to point out that although grazingreductions in general stimulated DOC degradation, the degra-dation rate still appeared to slow (at least in August and Sep-tember) with time. In addition, DOC degradation still occurredeven in treatments with grazers (in April and August), albeit at

a slower rate than in treatments without grazers. Nutrient ad-ditions, unless accompanied by grazing reductions, had littleeffect on either bacterial abundances or DOC degradation.These findings of a lack of nutrient stimulation of DOC deg-radation and of progressively slowing DOC degradation rateswith time regardless of treatment are consistent with thework of Søndergaard et al. (2000). Those authors showedthat nutrient additions did not enhance degradation of DOMoriginating from a phytoplankton bloom, and they arguedthat the chemical composition of a portion of the DOMmade it resistant to short-term bacterial degradation and al-lowed for its accumulation in coastal systems.

Production of degradation-resistant DOC could have ex-tremely important consequences for in situ net ecosystemmetabolism in shelf waters and perhaps more importantly, ad-jacent oligotrophic waters. Coastal upwelling regions are sitesof net DOC production (Hansell and Carlson, 1998), and re-cent work by Alvarez-Salgado et al. (2001a) suggests that de-pending on the lability of the DOM, the magnitude of DOMexported to oligotrophic offshore surface waters from coastalupwelling systems may be sufficiently large to alter the bal-ance between heterotrophy and autotrophy. Subsequent studiesin the Iberian upwelling system have shown that filaments,which break off from shelf waters and carry shelf wateraway from the coast, are capable of transporting significantamounts of autochthonous DOM to adjacent oligotrophicwaters (Alvarez-Salgado et al., 2001b, Barbosa et al., 2001).Off central and northern Oregon, Barth et al. (2005) have iden-tified several locations where offshelf transport of surfacewaters occurs during the upwelling season, with offshelfmovement happening on the order of <1e4 weeks. By extrap-olating the observed DOC degradation in these experimentsout to 14 d, well within the timeframe for offshelf export, itis estimated that at least 15% of the excess DOC would stillbe intact. Thus given the long degradation times of a portionof the DOC (relative to this potential offshelf transport mech-anism), Oregon’s coastal waters may be an important source oforganic matter to adjacent offshore waters of the North Pacific,as has been observed in the Iberian system. This phenomenonclearly needs more study in the field setting.

Despite the observed DOC degradation, there was very littleevidence of DON degradation, at least in the whole water treat-ments and the <3 mm treatment which are the most represen-tative of the natural microbial community. This finding ofselective degradation of the C-component of the DOM issomewhat surprising given that most field studies tend toshow that the N and P components of DOM are selectively re-mineralized, particularly over timescales of offshelf movementof coastal water masses (weeks to months) (e.g., Hopkinsonet al., 2002). Also, considering the low ambient DIN concen-trations, one might have expected the N-component of theDOM to be preferentially degraded over the C-component.However, it is important to remember that especially in thewhole water and <3 mm treatments, micrograzers were presentand while they consume bacteria, they also excrete nutrientsthat promote continued bacterial growth and metabolism(Strom, 2000). Thus although DIN concentrations may have

431M.S. Wetz et al. / Estuarine, Coastal and Shelf Science 77 (2008) 422e432

been low, rates of DIN cycling may still have been high. Fur-thermore, during coastal diatom blooms, there is a tendency to-wards high rates of polysaccharide production (Nieto-Cidet al., 2004), which contain very little N. This polysaccharideproduction can temporarily drive the C:N of the DOM wellabove the Redfield ratio. Because of its labile nature however,it is rapidly remineralized, sometimes on timescales as short asbloom duration (e.g., Kepkay et al., 1997). The net effect ofthis selective remineralization of C-rich compounds, on bothshort (i.e., bloom event) and seasonal timescales, is that theC:N of the DOM may be reduced back to near Redfield stoichi-ometry (e.g., Kepkay et al., 1997; Koeve, 2006).

The preferential degradation of C relative to N in the POMand DOM pools has significant implications for the C and Ncycles of this setting. It suggests that potentially, N may bepreferentially exported from the system relative to C, eitheras POM or DOM. As a result, net C fixation may ultimatelybe limited by the export of organic N while the organic C isinternally recycled. If, however, the form of this recycling isin the production and degradation of high C:N organic mate-rial (i.e., TEP and other carbohydrates) while material withmore Redfield-like C:N stoichiometry is exported, the systemmay have the macroscopic appearance of being governed byRedfield-like stoichiometry (as argued by Hales et al.,2005a) while many internal reactions show decoupling of Cand N diagenesis.

5. Conclusions

This study demonstrates that while some portion of phyto-plankton-derived DOM and POM is labile and rapidly de-graded, another fraction may not be as easily degraded. Theportion of POM that is labile contributes to respiration signalsin shelf bottom waters, while the less easily degraded fractionmay be transported offshelf through the bottom boundarylayer. While reductions in HFLAG grazing on bacteria stimu-lated bacterial growth and DOC degradation, that degradationstill slowed with time, pointing to the chemical composition ofthe DOC as being an important factor in its degradability. Theless labile fraction of DOM appears to be resistant to degrada-tion on timescales longer than water mass residence timesobserved on Oregon’s continental shelf, and thus may be ex-ported offshelf. Further work is needed to quantify offshelfexport fluxes of this DOC in situ. Selective C degradation (rel-ative to N) was observed for both the POM and DOM frac-tions and is a phenomenon that requires further study in thecontext of the in situ observations of C and N export. Alsoneeded are laboratory or field studies to determine what spe-cific compounds are more or less easily degraded over relevanttimescales.

Acknowledgments

We thank Jennifer Wetz, Julie Arrington and Leah Bandstrafor their technical assistance. We also thank two anonymousreviewers for their constructive comments. This research wassupported by an NSF Graduate Research Fellowship and

a Sigma Xi Grant In Aid of Research to MSW, NSF grantOCE-0434810 to Patricia A. Wheeler and NSF grant OCE-9907854 to Patricia A. Wheeler and Burke Hales.

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