COMPOSITION AND CYCLING OF COLLOIDSIN MARINE ENVIRONMENTS

Laodong Guo and Peter H. SantschiDepartment of OceanographyLaboratory for Oceanographic andEnvironmental ResearchTexas A&M University, Galveston

Abstract. Colloidal (COM) or macromolecular or-ganic matter makes up a significant portion of the bulkdissolved organic matter (DOM) pool in aquatic envi-ronments. Because of their high specific surface areasand complexation capacities, marine colloids are of greatimportance not only in the global carbon cycle but alsoin the biogeochemical cycling of many particle-reactivenuclides and trace elements in the ocean. However, thecolloidal pool as a whole is still poorly understood andlargely uncharacterized. Recently, cross-flow ultrafiltra-tion and other separation techniques, which have beensuccessfully used to isolate marine colloids, combinedwith a multitracer approach, have greatly advanced ourunderstanding of the cycling of COM and its associatedtrace elements in marine environments. In this paper we

focus on recent developments on isotopic and elementalcomposition of colloids which allow organic matter cy-cling in marine environments to be constrained. Majorsections review sampling techniques for aquatic colloids,concentrations and distribution of COM, biochemicaland elemental (organic and inorganic) characterization,and stable isotopic (13C and 15N) and radioisotopic (14Cand 234Th) characterization of marine colloids. We dis-cuss sources and turnover rates of organic matter in theocean, importance of benthic boundary layer processesin the cycling of DOM, changes in the paradigms ofmarine organic matter cycling, and research needs for abetter understanding of the biogeochemistry of marinecolloids.

1. INTRODUCTION

Dissolved organic matter (DOM) is the largest or-ganic carbon pool in the ocean and plays a central role inthe marine biogeochemistry of a variety of elements.The organic matter cycle in the ocean is complex and notyet fully understood, partially because of the still rela-tively poor characterization of DOM in terms of molec-ular weights and chemistry. While low molecular weight(LMW) compounds, which can be removed by microbi-ally and photochemically mediated biochemical pro-cesses [e.g., Amon and Benner, 1996, and referencestherein], make up the majority of DOM in the openocean, a significant amount is composed of macromole-cules [e.g., Guo et al., 1995a], which can also be removedfrom the ocean by physical processes such as coagulationor adsorption onto particles [e.g., Jackson and Loch-mann, 1992; Stordal et al., 1996b]. Recent developmentsin isolation techniques of macromolecular organic mat-ter allowed the isotopic and elemental characterizationof this fraction of organic matter [e.g., Benner et al.,1992b; Santschi et al., 1995; Guo et al., 1996b], whichfurther constrains the transport and cycling of organicmatter in the ocean. A schematic of the important pro-cesses governing the transport and cycling of DOM in

marine environments, which include terrestrial inputs,physicochemical and biogeochemical processes, sedi-mentation, resuspension, and benthic boundary layertransport processes, is given in Figure 1.Timescales of transport and transformation processes

can often be derived from the analysis of natural radio-isotopes such as 14C [e.g., Williams and Druffel, 1987].When radiocarbon measurements were carried out inthe bulk DOM pool, apparent 14C ages of ;1000–6000years could be calculated [Williams and Druffel, 1987;Bauer et al., 1992]. These timescales are similar to orgreater than the mixing time of the ocean (;1600 years).Old apparent 14C ages of DOM imply that a largeportion of the DOM in the deep waters of the ocean ischronologically old and is recycled several times beforeremoval or transformation occurs in the water column. Itwas proposed that apparent 14C ages derived from ra-diocarbon are the averages for the bulk DOM pool andthus are the result of mixing of different DOM fractionswith varying 14C ages [Mantoura and Woodward, 1983;Williams and Druffel, 1987]. Indeed, recent measure-ments of radiocarbon in high molecular weight (HMW)DOM fractions indicate that they contain higher D14Cvalues and thus turn over much faster than the bulkDOM in the ocean [e.g., Santschi et al., 1995; Guo et al.,

Copyright 1997 by the American Geophysical Union. Reviews of Geophysics, 35, 1 / February 1997pages 17–40

8755-1209/97/96RG-03195$15.00 Paper number 96RG03195● 17 ●

1996b]. This is consistent with the rapid degradationrates of the HMW DOM observed from microbial uti-lization experiments [e.g., Amon and Benner, 1994] andshort residence times of HMW DOM derived from234Th:238U disequilibra [e.g., Baskaran et al., 1992; Mo-ran and Buesseler, 1992; Huh and Prahl, 1995; Santschi etal., 1995; Guo et al., 1996a]. It thus seems that oceanicDOM contains a variety of organic components withvarying molecular weights and 14C ages and that theHMW DOM fractions cycle more rapidly and, con-versely, the LMW DOM turns over on much longertimescales in the ocean [Amon and Benner, 1994; Guo etal., 1996b].The occurrence of HMW colloidal organic matter

(COM) and its significance for carbon and trace elementcycling have long been recognized, with research effortspeaking in recent years [e.g., Breger, 1970; Sharp, 1973;Maurer, 1976; Ogura, 1977; Zsolnay, 1979; Means andWijayaratne, 1982; Sigleo et al., 1982; Carlson et al., 1985;Moran and Moore, 1989; Sigleo and Means, 1990; White-house et al., 1990;Wells and Goldberg, 1991, 1994; Benneret al., 1992b; Amon and Benner, 1994; Guo et al., 1994,1995a; Sempere et al., 1994; Bianchi et al., 1995; Dai et al.,1995; Martin et al., 1995; Santschi et al., 1995; Guo et al.,1996b]. High molecular weight organic matter in seawa-ter is important in the marine carbon cycle as it cansupport heterotrophic activity [Benner et al., 1992b]. Inaddition, there is mounting evidence that colloidal mac-romolecular material represents a significant pool oftrace element-binding ligands and may be the cause ofthe “particle concentration effect,” a negative relation-ship between log Kd (distribution coefficient) and log Cp(particle concentration), which is frequently observedfor trace element, trace organic, and radionuclide phasepartitioning in the ocean and other aquatic environ-

ments [e.g., Honeyman and Santschi, 1989; Guo et al.,1995b; Santschi et al., 1996]. Therefore colloids may havea major impact on the distribution and fate of manyparticle-reactive and nutrient-type elements [e.g., Hon-eyman and Santschi, 1992; Baskaran et al., 1992; Sholko-vitz, 1992; Sholkovitz et al., 1994; Moran et al., 1996;Stordal et al., 1996a; L.-S. Wen et al., Estuarine tracemetal distributions in Galveston Bay: Colloidal formsand dissolved phase speciation, submitted to MarineChemistry, 1996] (hereinafter referred to as Wen et al.,submitted manuscript, 1996) as well as neutral hydro-phobic organic contaminants [e.g., Means and Wija-yaratne, 1982, 1989; Brownawell, 1986; Sigleo and Means,1990; Chin and Gschwend, 1992].Macromolecular organic matter is polymeric, poly-

functional, and polydisperse. It is internally and exter-nally porous and charged. Its overall charge is a functionof pH and ionic strength. Its surface is also hydrated toa variable degree, with hydrophilic (i.e., charged func-tional groups composed of O, N, and S moieties) andhydrophobic regions (i.e., regions with only C and H[Buffle, 1990]). Such compounds are called amphiphiles,which can form structures termed micelles. Thus it alsohas dispersive properties through its ordered three-di-mensional structure and aggregation properties withother molecules. While its polyfunctionality affects tracemetal speciation, it is the amphiphilic and partial hydro-phobic character of macromolecular organic matterwhich is responsible for the apparent solubility enhance-ment of hydrophobic trace contaminants [e.g., Chiou etal., 1986, 1987]. Macromolecules are also the site ofphotochemical and microbially mediated biochemicalreactions which can lead to low molecular as well ashigher molecular weight material [e.g., Bushaw et al.,1996]. In addition, the bioavailability of selected biomol-

Figure 1. Schematic of processes governing the transport and cycling of dissolved organic matter in marineenvironments. Processes indicated by arrows include terrestrial inputs (1); lateral transport in the benthicboundary layer (BBL) (2); resuspension and sediment-water exchange (3 and 4); and biological, chemical, andphysical processes in the upper water column (5 and 6).

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ecules in seawater appears to be altered from that ob-served in pure solution [e.g., Keil and Kirchman, 1994],likely because of the presence of DOM.Recent studies have shown that marine colloids are

mostly organic in nature, i.e., mostly composed of mac-romolecules [Benner et al., 1992b; Guo et al., 1995a;Santschi et al., 1995]. It is likely that this macromolecularorganic matter contains surface sites which have a highaffinity for particle-reactive trace elements. This, in turn,may allow us to employ them as geochemical tracers.Together with the analysis of specific biomarkers, theirpresence would allow the identification of sources andbiogeochemical pathways of these macromolecular ma-terials in marine environments. If the major componentsof COM become homogeneously tagged with some ofthese particle-reactive trace elements or radionuclides,the biogeochemical cycles and calculated turnover ratesof these trace elements and radionuclides can provideimportant clues about the marine carbon cycle.The objective of this paper is to give an overview of

some recent progress in the study of macromolecularorganic matter cycling in marine environments derivedfrom stable and radioisotopic signatures. Since innova-tions in marine science are driven equally by technolog-ical advances as well as changes in paradigms, we alsoaddress advances in sampling techniques, which allowedfor better chemical characterization of colloidal or mac-romolecular materials in seawater and significant im-provements in models of organic matter cycling.

2. DEFINITION OF COLLOIDS

Even though inorganic and surface chemists havelong used the term “colloids” for metal oxide and silicateor other synthetic particles of defined surface character-istics, the definition of colloids is based on operationaltechniques. According to the International Union ofPure and Applied Chemistry (IUPAC), the term “col-loids” includes microparticles, macromolecules, and mo-lecular assemblies (e.g., micelles) defined by molecularweights or sizes of about 1 nm to 1 mm [e.g., Vold andVold, 1983; Buffle and Leppard, 1995; Stumm and Mor-gan, 1995].In terms of phase speciation, organic matter in sea-

water can be grouped into three classes: particulate,colloidal, and dissolved fractions, with the boundariesbased on the pore size of the membrane used to separateparticles and colloids. Most colloidal organic matter witha size range from 1 nm to 1 mm can pass through0.45-mm filters and is thus included in the dissolvedfraction with a corresponding high molecular weight. Inaddition, small living organisms such as viruses, bacteria,protozoa, and algae which are frequently termed ashydrophilic biocolloids may be included in the colloidalfraction [Ogura, 1977]. Thus the types of organic colloidspresent in seawater include macromolecular organicmatter, microorganisms, viruses, biocolloids, aggregates

of exudates, and clay minerals and oxides of iron, alu-minum, and manganese coated with organic matter [e.g.,Tipping, 1988; Stumm and Morgan, 1995].The terms “colloidal organic matter” or “macromo-

lecular organic matter” are used here synonymously.They are based upon operational definitions and cali-brations, usually between 0.2 and 0.4 mm on the upperlimit and 1 and 10 kilodaltons (kDa) on the lower end ofthe size spectrum. In the following discussion, dissolvedorganic carbon (DOC) or dissolved organic matter is thetraditionally defined dissolved fraction which includescolloidal organic carbon (COC) or COM fraction. Onthe other hand, COC1 or COM1 is the colloidal fractionbetween 1 kDa and 0.2 or 0.4 mm, which includes thecolloidal subfractions COC3 (fraction between 3 kDaand 0.2 or 0.4 mm) and COC10 (between 10 kDa and 0.2or 0.4 mm).

3. SAMPLING TECHNIQUES FORMACROMOLECULAR ORGANIC MATTER

Understanding the chemistry and fate of DOM in theocean depends, to a large extent, on the capability ofsampling or extraction of DOM from seawater whichcontains about 35,000 times as much sea salt than DOC.Thus reliable and unbiased methods for sampling andisolation of DOM are critical for the study of DOM inseawater.A variety of methods have been used for isolating

COM from seawater (Table 1). The isolation of COMfrom seawater is typically done by filtration of waterthrough 0.2- to 1-mm pore-size filters, followed by dif-ferent separation and isolation techniques, e.g., ultrafil-tration techniques [e.g., Buffle et al., 1993; Buesseler et al.,1996], amberlite ion exchange resin (XAD) columns[e.g., Druffel et al., 1992; Hedges et al., 1992], ultracen-trifugation [e.g., Wells and Goldberg, 1991, 1994], fieldflow fractionation [e.g., Beckett et al., 1987; Beckett andHart, 1993], gel filtration [e.g., Sakugawa and Handa,1985], size exclusion chromatography [e.g., Chin andGschwend, 1991], and reverse-phase chromatography[e.g., Burgess et al., 1996]. While the conventionalmethod using XAD resins can only extract about 15% ofthe DOM in seawater and requires pH adjustment[Hedges et al., 1992; Town and Powell, 1993], ultrafiltra-tion requires no pretreatment and can extract at leasttwice as much DOM [Benner et al., 1992b; Guo et al.,1996b]. Thus ultrafiltration has become one of the mostpromising and widely used techniques in recent years[Buesseler et al., 1996; Guo and Santschi, 1996]. Anotheradvantage is that large quantities of COM can be iso-lated in relatively short periods of time using cross-flowultrafiltration techniques, which are recommended forseparation of marine colloids from large volumes ofseawater [Whitehouse et al., 1990; Benner, 1991; Brown-awell, 1991]. For example, cross-flow ultrafiltration with1-kDa spiral-wound cartridges has been used to extract

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 19

several hundred milligrams of COM from seawater forbiochemical and isotopic characterization and molecularsize determinations of DOM [e.g., Benner et al., 1992b;Guo et al., 1995a, 1996b; Santschi et al., 1995].While the cross-flow ultrafiltration technique for sam-

pling macromolecular organic matter seems promising,rigorous cleaning and handling protocols which are crit-ical for obtaining unbiased and reliable results have notalways consistently been applied by different investiga-tors [Buesseler et al., 1996]. Furthermore, frequent cali-bration of ultrafilters before any sampling is indispens-able [Guo and Santschi, 1996] since ultrafilters have alimited lifetime and even new cartridges could have adifferent average pore size than the one given by themanufacturers [e.g., Gustafsson et al., 1996]. Thus theproper ultrafiltration methodology is more time consum-ing and demands greater attention to detail than ex-pected previously. For example, recent studies haveshown that concentrations of organic carbon and tracemetals in the ultrafiltrate (or permeate) change withtime or concentration factor as a consequence of os-motic permeation through the membrane [Guo andSantschi, 1996; Buesseler et al., 1996; Wen et al., 1996a].Therefore discrete sampling of the permeate fractionleads to a biased result of the molecular weight distri-butions of DOC and metals. This may also explain whymost of the previous ultrafiltration results had such largevariations (see next section). Thus, appropriate samplingprotocols for all fractions, including the retentate (col-loids), permeate (ultrafiltrate), and cartridge leachates(for the adsorbed fraction), should be used during ultra-

filtration of seawater in order to assess mass balance andthus obtain reproducible results. Another factor whichcomplicates any comparison between results from dif-ferent investigators is the fact that many different ultra-filter membranes from different manufacturers havebeen used for the separation of marine colloids, withdifferent nominal molecular weight cutoffs and varyingretention characteristics. In addition, as mentioned be-fore, different sampling protocols (e.g., storage and pro-cessing times, cleaning of cartridges, rigor in obtainingmass balance) and concentration factors employed dur-ing ultrafiltration as well as varying prefiltration tech-niques may have given rise to significantly different re-sults in terms of molecular weight distributions andchemical composition of COM in seawater [e.g., Bues-seler et al., 1996] (see Tables 1 and 2).

4. CONCENTRATIONS AND DISTRIBUTIONSOF COC

Studies using ultrafiltration techniques to quantifyCOC concentrations or to examine the molecular weightdistributions of DOC in seawater carried out over thelast decade are summarized in Table 2. Concentrationsor percentages of COC in the bulk DOC show a consid-erable spread either in the same water using differentultrafilters or in different marine environments using thesame ultrafilters (Table 2). According to these recentstudies, COC . 10 kDa makes up 3–30% of the bulkDOC, whereas COC . 3 kDa represents 8–36% of the

TABLE 1. Methods Used for Isolating DOM From Seawater

MethodMWCO,kDa

PercentExtracted Reference

UF (forced dialysis) 50 8–16 Sharp [1973]UF and dialysis 1 10–15 Maurer [1976]UF (stirred cell) 20 11 Zsolnay [1979]UF (stirred cell) 10 NA Sigleo et al. [1982]UF and CFUF 5 NA Means and Wijayaratne [1984]UF (stirred cell) 1 10–64 Carlson et al. [1985]CFUF 10 ,10 Whitehouse et al. [1990]CFUF 0.5 NA Brownawell [1991]UF and SEC 3 ,50 Chin and Gschwend [1991]CFUF 1 25–35 Benner et al. [1992b]CFUF 1 45 Guo et al. [1994]CFUF 1 30–50 Guo et al. [1995a]CFUF 10 18 Martin et al. [1995]CFUF 10 3–5 Santschi et al. [1995]CFUF 1 0–67 Buesseler et al. [1996]CFUF 1 19–82 J. R. Ertel (Isolation of dissolved organic matter from coastal

waters: Comparison of XAD-adsorption and ultrafiltrationtechniques, submitted to Marine Chemistry, 1996) (hereinafterreferred to as Ertel, submitted manuscript, 1996)

XAD 5–15 Hedges et al. [1992]XAD 2–31 Lara and Thomas [1994]XAD 10–72 Ertel (submitted manuscript, 1996)

MWCO, nominal molecular weight cutoff; CFUF, cross-flow ultrafiltration; UF, ultrafiltration; SEC, size exclusion chromatography; XAD,amberlite ion exchange resins (e.g., XAD-2, XAD-4, XAD-8); NA, not available.

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bulk DOC. Colloidal organic carbon .1 kDa was evenmore variable, ranging from undetectable to 82% of thebulk DOC (Table 2).The first attempt to quantify the concentrations of

COC in seawater using ultrafiltration techniques startedas early as 1970 [e.g., Sharp, 1973; Ogura, 1974; Maurer,1976; Wheeler, 1976; Zsolnay, 1979]. Later, Carlson et al.[1985] reexamined the molecular weight distribution ofDOC in seawater and summarized most earlier results inthe literature. According to their account, most of theearlier studies suffered from contamination problemsand may have had large uncertainties in the COC frac-tions, likely due to procedural artifacts. For example, nodifference in molecular weight distribution of DOC wasfound between surface and deeper waters, nor betweennearshore and open ocean waters [Carlson et al., 1985,and references therein]. In addition to the contamina-tion problems, quantifying the COC fraction by concen-tration difference between the initial solution and theultrafiltrate may have further increased the variability inthe results from earlier studies (also see Table 2).Carlson et al. [1985] first examined the DOC mass

balance during ultrafiltration by measuring organic car-bon concentrations in all the ultrafiltration fractions.Such an approach has also been used in the most recentstudies [e.g., Whitehouse et al., 1990; Benner, 1991; Guoet al., 1994]. However, because of changes of organiccarbon concentrations in the ultrafiltrate during ultrafil-

tration as a consequence of osmotic pressure differen-tials [Guo and Santschi, 1996], procedural artifacts arestill possible if this is not recognized as such and samplesare improperly handled (see also section 3). Even aDOC mass balance of close to 100% is no guarantee forthe sample’s integrity [Buesseler et al., 1996]. Nonethe-less, because of attention to detail and quality assuranceand control, examinations of DOC molecular weightdistributions in different marine environments were pos-sible and more consistent features of the molecularweight distributions of DOC emerged [e.g., Benner et al.,1992a, b; Guo et al., 1994, 1995a].Benner et al. [1992a] showed that concentrations of

COC1 isolated by ultrafiltration (.1 kDa) decreasedlinearly from Mississippi River to the open Gulf ofMexico. The percentage of COC1 they recovered afterdesalting was 45% in the river and ;27% in the gulf.Because desalting by diafiltration removes some of thelower molecular weight COM from the retentate [e.g.,Guo and Santschi, 1996, and references therein], per-centages of COC are somewhat lower when this proce-dure is applied. Guo et al. [1995a] quantified the con-centration of COC and its percentage in the bulk DOCwithout desalting in seawater from both the Gulf ofMexico and the Middle Atlantic Bight. They found thatconcentrations of COC fractions (both in COC1 andCOC10 fractions) decreased from river to nearshore andto offshore waters in the Gulf of Mexico and the Middle

TABLE 2. Percentage of COC in the Bulk DOC in Different Marine Environments Using Ultrafiltration Techniques

ReferencePrefilter PoreSize, mm MWCO, kDa

Location(or Water Type) DOC, mM COC/DOC, %

Carlson et al. [1985] 0.7 1 seawater 45–416 10–64Benner et al. [1992a] 0.2 1 Mississippi Plume 83–333 27–45Benner et al. [1992b] 0.2 1 Pacific 38–82 25–35Ogawa and Ogura [1992] 0.45 1 Pacific 51–64 30–37Guo et al. [1994] 0.4 1 Gulf of Mexico 50–131 466 6Guo et al. [1995a] 0.2 1 Atlantic 47–90 20–44Guo et al. [1995a] 0.2 1 Gulf of Mexico 45–86 14–36Buesseler et al. [1996] 0.2 1 seawater 30–120 0–67Ertel (submitted manuscript, 1996) 0.45 1 coastal NA 19–82Guo et al. [1995a] 0.2 3 Gulf of Mexico 45–70 10–16Guo et al. [1995a] 0.2 3 Atlantic 69–90 20–24Ertel (submitted manuscript, 1996) 0.45 3 coastal NA 8–36Moran and Moore [1989] 0.45 10 North Atlantic 45–75 10–15Whitehouse et al. [1989] 0.2 10 estuarine 80–400 8–19Whitehouse et al. [1990] NA 10 seawater 42–60 ,10Ogawa and Ogura [1992] 0.45 10 Pacific 51–64 4–5Kepkay et al. [1993] 0.2 10 Bedford Basin 70–158 4–16Guo et al. [1994] 0.4 10 Gulf of Mexico 50–130 8–14Dai et al. [1995] 0.4 10 Rhone Delta 82–148 8–30Guo et al. [1995a] 0.2 10 Atlantic 50–90 5–10Guo et al. [1995a] 0.2 10 Gulf of Mexico 45–86 3–5Guo [1995] 0.2 10 Galveston Bay 139–495 6–11Guo [1995] 0.2 10 Chesapeake Bay 118–205 10–16Martin et al. [1995] 0.4 10 Venice Lagoon 116–312 10–26Niven et al. [1995] 0.2 10 Bedford Basin 56–101 3–17Sempere et al. [1994] 0.7 500 Rhone Delta 92–179 7–49Sempere and Cauwet [1995] 0.7 0.02 mm estuary (Krka River) 103–147 22–54

MWCO, nominal molecular weight cutoff; NA, not available.

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Atlantic Bight (Figure 2). The percentages of COC1 inthe total DOC changed from ;60% in Galveston Bay to42% at the nearshore station to 40% at the open oceanstation [Guo et al., 1995a]. Similarly, surface water

COC10 varied from ;8% of the bulk DOC in GalvestonBay to;5% at the nearshore station to;4% of the bulkDOC at the open gulf station [Guo et al., 1995a]. Inseawater off Cape Hatteras, surface water COC1 was, onaverage, about 59% of the bulk DOC in Chesapeake Bayand decreased to ;38% of the bulk DOC at the MiddleAtlantic Bight stations, whereas surface water COC10decreased from ;12% of the bulk DOC in ChesapeakeBay to ;6% at Middle Atlantic Bight stations [Guo,1995]. The decrease of COC from fresh to coastal toopen ocean waters (Figure 2) implies that terrestrialinputs could be important sources of HMW colloidalorganic matter to the ocean [Benner et al., 1992a; Guo etal., 1995a].Vertical distribution of COC, on the other hand,

showed that both concentrations and percentages ofCOC decreased from surface to deep waters (Figure 3),e.g., in the Pacific [Benner et al., 1992b], in the Gulf ofMexico [Guo et al., 1994, 1995a], and in the MiddleAtlantic Bight [Guo et al., 1995a]. While the percentageof the HMW organic matter decreased from surface tobottom waters, the percentage of the LMW fraction(e.g., ,1 kDa fraction) increased from surface to deepwaters [e.g., Benner et al., 1992b; Guo et al., 1995a]. Thedecrease of COC from river to the sea and from surfaceto deeper water suggests that HMW organic matter is areactive component and that COC is transported fromnearshore to offshore, being produced in the upperwater column and then consumed during its transport tothe deep water.Examination of the molecular weight distribution of

bulk DOC shows that on average, ;4% of the totalDOC was in the 10-kDa to 0.2-mm fraction, ;9% was inthe 3- to 10-kDa fraction, and ;23% was in the 1- to

Figure 2. Variation of HMW colloidal organic carbon (COC)concentrations from nearshore to offshore stations in (a) theGulf of Mexico and (b) the Middle Atlantic Bight off CapeHatteras (modified from Guo et al. [1995a]).

Figure 3. Vertical distribution of HMW colloidal organic carbon (COC) in the Gulf of Mexico and the MiddleAtlantic Bight (modified from Guo et al. [1995a]).

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3-kDa fraction, leaving ;64% of the total DOC in theLMW fraction (,1 kDa) in Gulf of Mexico waters(Figure 4). Similarly, in seawater from the Middle At-lantic Bight,;7% of the bulk DOC was in the 10-kDa to0.2-mm fraction, ;14% was in the 3- to 10-kDa fraction,;25% was in the 1- to 3-kDa fraction, and ;54% was inthe ,1-kDa fraction (Figure 4). From results of theDOC molecular weight distribution it is clear that theCOC (.1 kDa) fraction usually composed ;30–50% ofthe bulk DOC and varied depending on locations anddepths in the water column. Moreover, the majority ofthe bulk DOC pool in seawater was in the LMW fraction(,1 kDa).However, compared with the particulate organic car-

bon (POC) pool in seawater, HMW COC is still a largerreservoir in marine environments [Guo, 1995]. For ex-ample, mass concentrations of organic colloids (COM1,assuming [COM]5 23 [COC]) could range from 335 to1015 mg L21 in the Gulf of Mexico and from 484 to 968mg L21 in the Middle Atlantic Bight, which are muchhigher than the mass concentrations of suspended par-ticulate matter (SPM), which ranged from 16 to 361 mg

L21 in the same areas [Guo, 1995]. In estuarine waters,the COC pool (e.g., COC1) is always larger than theLMW DOC pool [e.g., Benner and Hedges, 1993; Guo,1995]. For example, in Galveston Bay waters, POC madeup ;12% of the total organic carbon (TOC) pool, whileCOC1 consisted of ;54% of the TOC. Only ;34% ofthe TOC was in the,1-kDa LMW fraction (Figure 5). Asimilar distribution pattern was also observed in estua-rine waters of Chesapeake Bay (Figure 6). As will bediscussed later, most of the colloidal mass is composedof COM [Santschi et al., 1995]. Therefore a measure-ment of the COC concentration can also be used tocalculate the mass concentration of colloids.

Figure 4. Molecular weight distribution of DOC in seawaterfrom the Gulf of Mexico and the Middle Atlantic Bight (mod-ified from Guo et al. [1995a]).

Figure 5. Size fractionation of dissolved (DOC) and totalorganic carbon (TOC) in estuarine waters of Galveston Bay[from Guo, 1995; L. Guo et al., Trace metal composition ofestuarine colloidal organic matter, submitted to EnvironmentalScience and Technology, 1996; hereinafter referred to as Guo etal., submitted manuscript, 1996]. (Reprinted with permissionfrom Environmental Science and Technology, submitted forpublication. Unpublished work copyright 1997 AmericanChemical Society.) POC is particulate organic carbon. COC10and COC1–10 are the .10-kDa and 1- to 10-kDa colloidalorganic carbon fractions, respectively. UOC1 is the ,1-kDaorganic carbon fraction.

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5. BIOCHEMICAL AND ELEMENTALCHARACTERIZATION

5.1. Organic CompositionA great amount of work has been carried out to

characterize the DOM extracted by the conventionalXAD method [e.g., Meyers-Schulte and Hedges, 1986;Moran et al., 1991; Hedges et al., 1992]. Meyers-Schulteand Hedges [1986] isolated dissolved humic substancesfrom the open ocean and compared the total phenolyields with those of humic substances from the Amazon.They concluded that ;10% of dissolved marine humicsubstances are derived from terrestrial origin. Using thesame isolation method, Hedges et al. [1992] found thatseawater humic substances only contain a small amountof riverine dissolved humic substances. Values of C/Nratios in these isolates ranged from ;32 to 47 [Meyers-Schulte and Hedges, 1986; Hedges et al., 1992], which are

significantly higher than those from isolates by ultrafil-tration (Table 3). Higher C/N ratios are consistent withthe nature of the isolates extracted by the XAD method,which selectively extracts mainly hydrophobic com-pounds.Studies conducted by Maurer [1976] showed that 10–

15% of the HMW (.1 kDa) organic matter isolated byultrafiltration followed by dialysis was carbohydrate(polysaccharides) while 20% was protein, leaving 65%uncharacterized. Wheeler [1976] reported that most ofthe dissolved carbohydrates were in the 1- to 30-kDamolecular weight ranges in coastal waters off Georgia.Sigleo et al. [1982] isolated colloidal materials (1.2 nm to0.4 mm) from Chesapeake Bay waters and found thatcarbohydrates and proteins were the major organic com-ponents of the HMW fraction. They concluded thataquatic microorganisms were the major source of colloi-dal organic material in the study area. Amino acid anal-ysis in HMW COM also showed that hydrolizable aminoacids and associated ammonia composed ;80% of thenitrogen present in the colloidal samples [Sigleo et al.,1983]. Means and Wijayaratne [1984] measured the bio-chemical components in the estuarine colloidal organicmaterial and showed that carbohydrates, amino acids,and lipids represented 35–60%, 4–13%, and ,1%, re-spectively, of the organic carbon content in the COMfrom Chesapeake Bay waters. Atomic C/N ratios in theChesapeake Bay colloidal organic material (.1 kDa)ranged from 7.2 to 11 with one value as high as 37 [Sigleoet al., 1983].More recent characterizations of HMW organic ma-

terial (.1 kDa), isolated from seawater in the PacificOcean using ultrafiltration followed by diafiltration, in-dicated that polysaccharides accounted for ;50% of theisolates in surface water and ;25% in deeper watersamples [Benner et al., 1992b]. They also reported thatC/N ratios in the isolates, ranging from 15 to 23, wereconsiderably lower than those in isolates collected usingXAD methods (Table 3). Direct assessments of carbo-hydrates in seawater using 3-methyl-2-benzothiazolin-one hydrazone hydrochloride (MBTH) analysis revealedthat total carbohydrates accounted for 21 6 7% of thebulk DOC in seawater from oceanic environments [Pa-kulski and Benner, 1994], consistent with the results fromthe analysis of COM. They also found that polysaccha-rides were the major component of the total carbohy-drates in seawater but their proportion decreased fromsurface to deeper waters while monosaccharide concen-trations changed little vertically in the ocean. This indi-cates that polysaccharides, a HMW organic componentin seawater, are some of the most reactive compoundclasses in the marine carbon cycle [Pakulski and Benner,1994]. Carbon 13 nuclear magnetic resonance (NMR)spectroscopy characterization confirmed that carbohy-drates are a major component of the HMW organicmatter (.1 kDa) isolated from seawater in the NorthPacific and the Gulf of Mexico, representing ;50% ofthe total carbon [McCarthy et al., 1993]. Values of C/N

Figure 6. Size fractionation of dissolved (DOC) and totalorganic carbon (TOC) in estuarine waters of Chesapeake Bay[from Guo, 1995; Guo et al., submitted manuscript, 1996].(Reprinted with permission from Environmental Science andTechnology, submitted for publication. Unpublished workcopyright 1997 American Chemical Society.) POC is particu-late organic carbon. COC10 and COC1–10 are the.10-kDa and1- to 10-kDa colloidal organic carbon fractions, respectively.UOC1 is the ,1-kDa organic carbon fraction.

24 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

ratios they reported, ranging from 13 to 22, were alsosignificantly lower than typical values obtained for ma-rine humic isolates (Table 3).In general, C/N ratios in the COM1 fraction de-

creased from estuarine to coastal seawaters and in-creased from surface to deeper waters in the Gulf ofMexico (Figure 7). The vertical changes of C/N ratios inCOM are likely due to the diagenesis of organic matterin the water column, consistent with the trend of C/Nratios previously reported for the Gulf of Mexico and theMiddle Atlantic Bight [Guo et al., 1996b]. High C/Nratios in the riverine samples point to a larger terrestrialcomponent for organic matter, while lower C/N ratios inseawater are related to a planktonic origin of organicmatter. The increase of C/N ratios from surface to bot-tom water indicates that colloidal material is being pro-duced in the upper water column and undergoes modi-fication through diagenesis during the transport fromthe surface to the bottom.Recently, plankton pigments (e.g., chlorophyll a and

b, fucoxanthin, zeaxanthin) have been identified in theCOM1 fraction in seawater in the Gulf of Mexico andthe Middle Atlantic Bight [Bianchi et al., 1995; Santschiet al., 1995]. The predominance of the carotenoids fu-coxanthin (a marker for diatoms) and zeaxanthin (amarker for cyanobacteria) indicated that these classes ofphytoplankton which represented the dominant forms ofPOC may also be the most likely sources of COM in thenorthwestern Gulf of Mexico. They concluded that themajority of pigments found in COM1 are likely derivedfrom direct exudation products and/or from sloppy feed-ing by zooplankton [Bianchi et al., 1995]. Carbon 13-NMR spectra of COM1 revealed that samples collectedfrom Galveston Bay water contained a higher aromaticcontent, which is characteristic of terrestrial humic sub-stances, while samples from the open Gulf of Mexicohad a more carbohydrate-like carbon composition whichdecreased from surface to deeper water (T. S. Bianchi et

al., Sources and transport of land-derived particulateand dissolved organic carbon in the Gulf of Mexico(Texas Shelf/Slope), submitted to Organic Geochemistry,1996) (hereinafter referred to as Bianchi et al., submit-ted manuscript, 1996). Their observations are broadlysimilar to the findings of Benner et al. [1992b] andMcCarthy et al. [1993].Along with the organic carbon and nitrogen contents,

Table 4 shows the organic sulfur concentrations inCOM1 samples collected from the Gulf of Mexico andthe Middle Atlantic Bight. Colloidal materials isolatedby ultrafiltration were desalted by diafiltration [Guo andSantschi, 1996] or dialysis [Sigleo and Means, 1990] andthen freeze-dried. Estuarine colloids contained 6–37%of organic carbon and 0.2–6% of nitrogen depending onsalinity and sampling seasons (Table 4). In the Gulf ofMexico and the Middle Atlantic Bight, organic carbon,nitrogen, and sulfur constituted 23–34%, 1.2–2.6%, and1.6–2.2% of the colloidal mass, respectively, after cor-recting for the amount of sea salt remaining in thecolloidal material (Table 4). These colloidal C and Nconcentrations are similar even though they are fromdifferent study areas. The colloidal sulfur concentrationsare close to those reported for humic substances (Table4). Marine colloids are therefore mostly organic in na-ture as is evident from the data given in Table 4 andindicated by the inductively coupled plasma-mass spec-trometry (ICP-MS) analysis of inorganic elements inisolated colloidal samples [e.g., Santschi et al., 1995].

5.2. Inorganic CompositionWhile attempts to characterize organic components

of colloidal materials have made some progress, reliablestudies to assay its inorganic components are still few.Little is known about the chemical composition of ma-rine colloids in terms of inorganic components.The first attempt to study the inorganic composition

of estuarine colloidal material was carried out by Sigleo

TABLE 3. Reported C/N Ratios of HMW Organic Matter in Marine Environments

Reference Location HMW Fraction C/N Ratio

Sigleo et al. [1983] Chesapeake Bay 1 kDa to 0.4 mm 7–12 (summer)9–37 (winter)

Meyers-Schulte and Hedges [1986] Pacific XAD isolates 32–37Benner et al. [1992b] Pacific 1 kDa to 0.2 mm 15–23Druffel et al. [1992] oceanic water XAD isolates 19–57Hedges et al. [1992] Pacific XAD isolates 36–47McCarthy et al. [1993] oceanic water 1 kDa to 0.2 mm 13–22Guo [1995] Gulf of Mexico 1 kDa to 0.2 mm 9–21Guo [1995] Galveston Bay 1 kDa to 0.2 mm 17–24Guo [1995] Galveston Bay 10 kDa to 0.2 mm 16–18Guo et al. [1996b] Chesapeake Bay 1 kDa to 0.2 mm 19–22Guo et al. [1996b] Chesapeake Bay 10 kDa to 0.2 mm 13–15Guo et al. [1996b] MAB 1 kDa to 0.2 mm 11–24Guo et al. [1996b] MAB 10 kDa to 0.2 mm 15–25 (36)Guo and Santschi [1996] Pacific 1 kDa to 0.2 mm 19Guo and Santschi [1996] Vineyard Sound 1 kDa to 0.2 mm 20

MAB, Middle Atlantic Bight.

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 25

and Helz [1981] and summarized by Sigleo and Means[1990]. Using neutron activation analysis, more than 30elements were measured on estuarine colloidal material(1 nm to 0.4 mm) collected by ultrafiltration followed bya desalting process [Sigleo and Helz, 1981]. Significantdifferences in colloidal composition were found betweenseasons and locations in the Patuxent River. For exam-ple, contents of clay minerals and other lithogenic ele-ments of estuarine colloids decreased with increasingsalinity and from winter to summer, whereas carbon-richcomponents showed the opposite trend. Benoit et al.[1994] also reported on the direct analysis of freeze-dried isolated colloidal material (10 kDa to 0.4 mm) andconcluded that colloidal Fe, Al, Pb, and Zn accountedfor most of the filter-passing forms of these metals inGalveston Bay. Recently, using ICP-MS, Vernon-Clarkand Goldberg [1995] surveyed most of the inorganicelements in several colloidal samples (1 kDa to 0.4 mm)collected off the California coast. They concluded that

concentrations of most elements they measured wereless than those reported for dissolved (,0.45 mm) con-centrations of seawater. The relevance of their approachis limited by the quality of desalting procedure used forthe isolation of the colloids and the long processingtimes, which may have caused changes in the colloidalstate. Therefore the procedure is still highly operational,and independent procedures are needed to confirmthese results.In addition to this type of approach in characterizing

inorganic components in the isolated colloidal material,direct measurements of trace elements in colloidal (so-lution) phase have increased in the recent years (seeTable 5). These studies involved measurements of traceelements in the permeate (fraction passing through ul-trafilters) and/or retentate fraction collected by ultrafil-tration techniques and the quantification of the colloidalfraction of these trace elements in seawater. As shown inTable 5, ultrafilters with 1- and 10-kDa cutoff are the

Figure 7. Variations of C/N ratios in COM1(1 kDa to 0.2 mm) from nearshore to offshorestations and from surface to bottom waters(data from Guo [1995]).

26 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

most frequently used ones to quantify the colloidal metalfraction, even though the prefilter in separating partic-ulate and dissolved phases varied as well. Takayanagiand Wong [1984] measured inorganic and organic Seconcentrations in the ultrafiltrate (permeate) fraction(,10 kDa) and found that most of the colloidal Se inseawater was in the organic fraction while inorganic andorganic Se were equally important in river water. Usingradioisotopic tracers in controlled model ecosystems(i.e., marine ecosystem research laboratory (MERL)),Santschi et al. [1987] also observed that 30–60% of Sewas in a colloidal form in Narragansett Bay waters. Inaddition, they reported that about 60% of Hg in the#0.45-mm fraction was observed in a colloidal form,2–20% was observed for As and Zn, and 10–70% wasobserved for particle reactive elements, such as Sn, Pa,and Fe [Santschi et al., 1987].Using a 10-kDa ultrafilter, Moran and Moore [1989]

reported 1–15% of the total dissolved Al was in a col-loidal form (10 kDa to 0.45 mm) in Atlantic seawater. Byexamining the ultrafiltration technique,Whitehouse et al.[1990] showed that colloidal Fe, Mn, and Cu may com-pose a significant portion of the total dissolved tracemetals. A narrowly defined colloidal fraction (0.2–0.4mm) using traditional filtration was also reported for Fein North Atlantic seawater, ranging from 20 to 40% ofthe #0.4-mm fraction [Wu and Luther, 1994]. It shouldbe noted that most previous studies of colloidal tracemetals using ultrafiltration techniques either sufferedfrom unsatisfactory recoveries or ignored the mass bal-ance assessment (see review by Wen et al. [1996a]).Recently, more consistent colloidal trace metal studiesemerged (Table 5), but most of these studies focused onestuarine environments. Martin et al. [1995] found that asignificant fraction of traditionally defined dissolved(,0.4 mm) trace metals was actually in a colloidal phase(10 kDa to 0.4 mm), ranging from 18% for Ni to 87% forFe and percentages in between those for Cd, Cu, Pb, andMn in the Venice Lagoon in Italy (see Table 5). Thepercentages were, however, calculated from the concen-tration difference between the total dissolved and ultra-filtrate fractions. Using the same technique, Dai andMartin [1995] and Dai et al. [1995] also examined colloi-dal trace metals in Arctic estuaries and the Rhone Delta(see Table 5). Furthermore, Swarzenski et al. [1995]reported a decrease of colloidal U fractions (10 kDa to0.4 mm) along a salinity gradient in Amazon shelf waters,from ;65% at a salinity of 0.3‰ to ;15% at a salinityof ;35‰. Stordal et al. [1996a] recently examined indetail the distribution of colloidal Hg in Texas estuaries.They reported that 47–93% of the Hg concentration in,0.45 mm was in a colloidal form (1 kDa to 0.45 mm) inGalveston Bay depending on water salinity or locations.Further colloidal trace metal data sets, from both estu-arine and open ocean waters, are currently in review[e.g., Bruland et al., 1996; Powell et al., 1996; Sanudo-Wihelmy et al., 1996; Wen et al., 1996b; M. C. Stordal etal., Dissolved and colloidal arsenic, antimony and sele-

nium within three Texas estuaries, submitted to AquaticGeochemistry, 1996; hereinafter referred to as Stordal etal., submitted manuscript, 1996; Wen et al., submittedmanuscript, 1996]. Among those,Wen et al. [1996a; Wenet al., submitted manuscript, 1996] have presented acomprehensive data set of colloidal trace metals in es-tuarine waters of Galveston Bay using their ultracleanultrafiltration procedures [Wen et al., 1996a]. In addition,Wen et al. [1996b] demonstrated the presence of signif-icant colloidal fractions (1 kDa to 0.4 mm) of Ag (15–70% of the total dissolved), a trace element which pre-viously was not considered to be organically complexed[Miller and Bruland, 1995]. They hypothesized that thiswas due to the significant content of reduced sulfur inCOM.Overall, the percentage of the colloidal fraction of

trace metals generally decreases from river water toestuarine water and to seawater. In addition, the re-moval sequences reported in different estuaries are con-sistent with those found in laboratory mixing experi-ments [e.g., Sholkovitz, 1976]. By examining those tracemetal data summarized in Table 5, it seems that a similartrend in partitioning of trace metals among differentgroups of elements exists [e.g., Wen et al., 1996a] eventhough difficulties in properly using ultrafiltration tech-niques to study colloidal trace metals still need to beovercome [Reitmeyer et al., 1996]. Therefore more sys-tematic studies of elemental associations with macromo-lecular organic matter are desirable.

TABLE 4. Elemental (C, N, and S) Composition of ColloidalSamples (COM1) From Surface Waters

Sample Name or Station Salinity C, % N, % S, %

Chesapeake Bay*Winter colloids 0.1–12 6.4–33 0.2–4.5 z z zSummer colloids 0.1–9 26–37 2.7–5.9 z z z

Galveston Bay†

B01 0 27 1.2 1.8B02 23 23 1.4 1.6

Gulf of Mexico†

G01 35.0 23 1.6 z z zG03 35.7 24 1.9 z z zG04 35.9 27 2.0 z z zG09 35.9 34 2.6 2.2

Middle Atlantic Bight†

A16 32.5 29 2.5 1.9A02 30.8 32 2.3 z z zA01 31.6 28 2.0 z z z

Humic substances‡

Soil humic acids 0 53.8–58.7 0.8–4.3 0.1–1.5Soil fulvic acids 0 40.7–50.6 0.9–3.3 0.1–3.6

Stream humic acids 0 56 1.27 0.93Stream fulvic acids 0 55 0.87 0.74

*From Sigleo and Means [1990].†From L. Guo and P. H. Santschi (unpublished results, 1996).‡From Aiken et al. [1985].

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 27

6. STABLE ISOTOPIC (13C AND 15N)CHARACTERIZATION

Carbon and nitrogen isotopes have proven to beuseful tracers for sources and transport of DOM in theocean [e.g., Sackett, 1989; Druffel and Williams, 1992;Thornton and McManus, 1994]. The average value ofd13C for terrestrial organic matter is about 227‰,whereas organic matter with marine origin has a value ofabout 220‰ [Sackett, 1989]. Some recent measure-ments of stable carbon and nitrogen isotopic signatureson HMW organic matter are listed in Table 6. Forcomparison, typical values of d13C and d15N in bulkDOM from seawater samples are also listed. Overall,colloidal d13C values reported in the literature are sim-ilar to those of the bulk DOM (Table 6).

Sigleo and Macko [1985] measured stable carbon andnitrogen isotopic signatures in the HMW organic matterfraction (5 kDa to 0.4 mm) in the Patuxent River estuary.They found that the average carbon isotope ratios (d13C)in the colloidal samples were 224.8‰, while the valuesof d15N were 8.5–10.8‰ (Table 6). Benner et al. [1992a]reported that values of d13C in COM1 increased linearlyfrom 225‰ at a freshwater station to 221.3‰ at aGulf of Mexico station with a salinity of ;36‰. Theyfound a different distribution pattern for d15N than ford13C, with lower d15N values (;3‰) in river and coastalend-members and higher d15N values at estuarine sta-tions. The maximal d15N values point to a source forfreshly produced COM in waters of intermediate salinity[Benner et al., 1992a].Values of d13C in colloidal organic matter (COM1)

TABLE 5. Concentrations of Colloidal Trace Elements in Estuarine and Seawater

Reference Size of Fraction Element Location SalinityColloidalPercentage

Takayanagi and Wong [1984] 1 kDa to 0.4 mm Se Chesapeake Bay 20.2 40–64Santschi et al. [1987] 1 kDa to 0.45 mm Hg MERL z z z 60

Se Narragansett Bay 30–60As, Zn 2–20Sn, Pa, Fe 10–70

Moran and Moore [1989] 1 kDa to 0.45 mm Al North Atlantic 31–34 1–15Whitehouse et al. [1990]* 10 kDa to 1.2 mm Fe Halifax Harbor ;30 78

Mn 22Cu 35

Wu and Luther [1994]* 0.2–0.4 mm Fe North Atlantic 35–36.7 20–40Dai et al. [1995]* 10 kDa to 0.4 mm Cd Rhone Delta 0–38 0–38

Cu (Mediterranean) 24–39Ni 0–18

Martin et al. [1995]* 10 kDa to 0.4 mm Cd Venice Lagoon 0–35 34Cu (Mediterranean) 46Fe 87Ni 18Pb 58Mn 54

Swarzenski et al. [1995] 10 kDa to 0.4 mm U Amazon Shelf 0.3–35.4 15–65Bruland et al. [1996] 1 kDa to 0.2 mm Fe Narragansett Bay NA 90

Cu 50Zn ND

Powell et al. [1996] 1 kDa to 0.4 mm Fe North Atlantic z z z 70–90Reitmeyer et al. [1996] 1 kDa to 0.2 mm Fe seawater z z z 26–16†

Sanudo-Wilhelmy et al. [1996] 10 kDa to 0.2 mm Fe, Ag, Al San Francisco Bay ,10 .85Cu, Co 16–40

Stordal et al. [1996a] 1 kDa to 0.4 mm Hg Texas estuaries 0–30 12–93(57 6 20)

Stordal et al. (submittedmanuscript, 1996)

1 kDa to 0.4 mm Se Galveston Bay 0–34 23–70As 0.5–4.6Sb 1–5

Wen et al. (submittedmanuscript, 1996)

1 kDa to 0.4 mm Cd Galveston Bay 0–34 44 6 13Cu 55 6 6Co 19 6 7Ni 36 6 9Pb 64 6 12Zn 91 6 8Fe 79 6 15

Wen et al. [1996b] Ag Galveston Bay 0–34 30–70

NA, not available.*Data calculated by the authors from the difference in concentrations between permeate and initial concentration.†Data from intercomparison study.

28 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

extracted from the Gulf of Mexico waters also showedan increase with increasing salinity [Santschi et al., 1995],indicating that organic carbon sources change frommore terrestrial origin in coastal waters to more marinesources in open gulf waters. More detailed studies on thevariation of colloidal d13C have been conducted in the

Gulf of Mexico and the Middle Atlantic Bight waters[Guo, 1995]. While distributions of colloidal d13C as afunction of st showed more variability in middle Atlanticwaters off Cape Hatteras, the pattern in the Gulf ofMexico was more typical (Figure 8), increasing fromnearshore to offshore, consistent with those distributionsreported by Benner et al. [1992a] and Santschi et al.[1995]. In addition, an inverse correlation between d13Cand D14C values was observed in COM1 from both the

TABLE 6. Stable Isotopic (13C and 15N) Composition of HMW Organic Matter in Seawater

Reference Location Sample Fraction d13C, ‰ d15N, ‰

Sigleo and Macko [1985] Patuxent estuary 5 kDa to 0.4 mm 224.8 8.5–10.8Druffel et al. [1992] open ocean XAD isolates 223.3 to 220.4 NABenner et al. [1992a] Mississippi Plume 1 kDa to 0.2 mm 225 to 221.3 ;3–9Guo [1995] Galveston Bay 1 kDa to 0.2 mm 228.3 to 224.9 NA

10 kDa to 0.2 mm 228.9 to 223.9Santschi et al. [1995] Gulf of Mexico 1 kDa to 0.2 mm 224.7 to 221 NA

MAB 1 kDa to 0.2 mm 223.2 to 221.7 NAGuo et al. [1996b] Chesapeake Bay 1 kDa to 0.2 mm 230 to 223 NA

10 kDa to 0.2 mm 225 to 223 NAGuo et al. [1996b] MAB 1 kDa to 0.2 mm 228 to 220 NA

10 kDa to 0.2 mm 228 to 223 NAEadie et al. [1978] open ocean bulk DOM 221.8 NASackett [1989] open ocean bulk DOM 222 6 2 NA

NA, not available; MAB, Middle Atlantic Bight.

Figure 8. Relationship between d13C values of COM1 (1 kDato 0.2 mm) and st in the Middle Atlantic Bight (MAB) and theGulf of Mexico [from Guo et al., 1996b; Guo, 1995].

Figure 9. Relationship between D14C and d13C in COM1 in theGulf of Mexico and the Middle Atlantic Bight [from Guo,1995; Guo et al., 1996b].

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 29

Gulf of Mexico and the Middle Atlantic Bight [Santschiet al., 1995; Guo et al., 1996b] (Figure 9). Lower d13Cvalues in coastal waters are indicative of terrestrialsources of DOM, whereas higher d13C values in offshorestations are consistent with the marine origin of organicmatter [Sackett, 1989]. Organic matter sources derivedfrom d13C values are consistent with those from organicC/N ratios discussed in the previous section.

7. RADIOISOTOPIC SIGNATURES

7.1. RadiocarbonIn addition to stable carbon isotopes, radiocarbon

signatures have also been used to study the cycling ofDOM and POM in marine environments (Table 7). It isclear from previous studies that apparent 14C ages of thebulk DOC are old and indicative of recycling within theocean on long timescales [Williams and Druffel, 1987;Bauer et al., 1992].Evidence from both lignin-derived phenols of dis-

solved humic substances [e.g., Meyers-Schulte andHedges, 1986] and d13C signatures of oceanic DOC [e.g.,Sackett, 1989] suggests that oceanic DOM is primarilyderived from marine sources and only a small percent-age of the DOM is terrestrially derived. In addition,measurements of radiocarbon in HMW dissolved humicsubstances extracted by XAD resins showed that appar-ent 14C ages of the XAD isolates were of the same orderor older than those of the bulk DOM pool [e.g., Bauer etal., 1992; Druffel et al., 1992] (see also Table 7), yieldingno evidence for a component of DOM cycled on time-scales shorter than the bulk DOM pool [Bauer et al.,1992]. If this fraction of dissolved humic substances is ofterrestrial origin, old apparent 14C ages indicate that thefraction of dissolved humic substance extracted by XADresins is refractory and has been cycled several times in

the ocean. However, recent studies have demonstratedthat the HMW COM extracted by cross-flow ultrafiltra-tion techniques had short residence times (of the orderof days or months). Evidence comes from microbialdegradation experiments [Kirchman et al., 1991; Amonand Benner, 1994], from the application of 234Th:238Udisequilibra [e.g., Baskaran et al., 1992;Moran and Bues-seler, 1992; Huh and Prahl, 1995; Santschi et al., 1995;Guo et al., 1996a], and from contemporary or higherD14C values [Santschi et al., 1995; Guo et al., 1996b]. Thedifferent apparent reactivities of HMW DOM revealedby different sampling techniques are, however, still anunresolved issue.It was proposed that apparent 14C ages of the bulk

DOM are the result of mixing of different organic car-bon components in seawater [e.g., Mantoura and Wood-ward, 1983]. However, direct measurements of radiocar-bon on different fractions of DOM have only recentlybeen reported [e.g., Santschi et al., 1995; Guo et al.,1996b]. Indeed, Santschi et al. [1995] found that theHMW COM10 fraction (10 kDa to 0.2 mm, which makesup ,10% of the bulk DOM) from surface water con-tained contemporary D14C values, indicating that a frac-tion of DOM is cycling in the ocean on a much shortertimescale. This conclusion is consistent with the shortresidence time of the same material derived from 234Thmeasurements (see discussion below). This contempo-rary COM10 material was also found for most of thesurface water COM10 samples in the Middle AtlanticBight [Guo et al., 1996b]. D14C values of deep waterCOM10 samples in the Gulf were not contemporary butwere still significantly higher than those of the wholeCOM1 fraction (1 kDa to 0.2 mm). However, the HMWCOM10 from bottom waters did not always containhigher D14C values. Instead, very old apparent 14C ageshave been found in bottom water HMW COM10 in theMiddle Atlantic Bight [Guo et al., 1996b], likely due to

TABLE 7. Radiocarbon Content of Organic Matter in Marine Environments

Reference LocationWater Depth,

m Sample Fraction D14C, ‰Apparent 14C Age,

years B.P.

Williams and Druffel [1987] Pacific 6000 ,1 mm 2540 to 2150 1310–6240Druffel and Williams [1990] Pacific 5700 .0.8 mm 143 to 1139 bomb 14CBauer et al. [1992] Sargasso Sea ;4500 ,1 mm ;2420 to 2200 NABauer et al. [1992] Sargasso Sea ;4500 XAD isolates ;2540 to 2380 NADruffel et al. [1992] Sargasso Sea 50–3237 XAD isolates 2587 to 2329 NASantschi et al. [1995] Gulf of Mexico 2–1650 1 kDa to 0.2 mm 246 to 2431 382–4538Santschi et al. [1995] Gulf of Mexico 2–1650 10 kDa to 0.2 mm 285 to 190 modern-711Guo [1995] Galveston Bay 2–10 1 kDa to 0.2 mm 251 to 197 modern-418Guo [1995] Galveston Bay 2–10 10 kDa to 0.2 mm 2200 to 274 391–1790Guo et al. [1996b] MAB 25–2600 1 kDa to 0.2 mm 2403 to 289 751–4143Guo et al. [1996b] MAB 25–2650 10 kDa to 0.2 mm 26 to 2709 49–9931Williams et al. [1992] Santa Monica Basin 100–850 POM (sinking) 224 to 1117 postbombAnderson et al. [1994] MAB POM (sinking) NA ;1000 years B.P.

to postbombP. H. Santschi et al.(unpublished results, 1996)

MAB 800 POM (sinking) 228 to 14 postbomb

NA, not available; MAB, Middle Atlantic Bight.

30 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

fractionation and resuspension processes in the benthicboundary layer (see discussion below). Moreover, oldHMW COM10 from bottom water of the Middle Atlan-tic Bight also had a short turnover time (derived from234Th) in spite of their old apparent 14C ages [Guo et al.,1996a]. The observation that old HMW COM10 (interms of apparent 14C ages) can turn over rapidly in thewater column is not necessarily contradictory since 234Thtraces only water column processes. The results areconsistent with recent studies reported by Keil et al.[1994], who showed that preserved organic matter canstill be labile once it is released to the water column orundergo rapid degradation upon desorption. Thereforeold 14C ages could be expected if the carbon source isfrom sedimentary organic matter. It seems then that theD14C value can become a good indicator of the source ofCOM. However, the apparent 14C age may not be adirect measurement of organic carbon turnover time ifthe carbon sources are not exclusively from the upperwater column or if the portion of organic matter recycleson decadal or shorter timescales.

7.2. Thorium IsotopesBecause of its strong chemical reactivity to particle

surfaces and its suitable decay timescale (half-life of 24.1days), the naturally occurring 234Th has been used as apowerful tracer for studying particle dynamics and traceelement scavenging in seawater [e.g., Coale and Bruland,1987; Buesseler et al., 1995; Baskaran et al., 1996]. Sincemarine colloids are primarily organic in nature and havesurface sites (such as dicarboxylic groups) with a highaffinity for trace elements such as thorium [Santschi etal., 1995], thorium isotopes of different half-lives (e.g.,24 days for 234Th, 1.9 years for 228Th, 7.5 3 104 years for230Th, and 1.4 3 1010 years for 232Th) may be used as

natural tracers for the cycling of a large fraction of DOMin marine environments.7.2.1. Concentrations of colloidal 234Th. The

first studies to measure colloidal thorium isotopes and toestimate the residence times of a fraction of HMWorganic matter in seawater were conducted by Baskaranet al. [1992], who determined the colloidal (10 kDa to 0.4mm) 234Th in seawater from the Gulf of Mexico, and byMoran and Buesseler [1992], who evaluated colloidal (10kDa to 0.2 mm) 234Th in seawater near Bermuda. Sub-sequent studies (see Table 8) have contributed signifi-cantly to our knowledge of the interaction of Th isotopeswith DOM in seawater. These results thus enhance thevalue of the application of Th isotopes as tracers for thecycling of DOM in marine environments.However, Table 8 shows that the HMW colloidal

234Th fraction (.10 kDa), as a percentage of the totaldissolved 234Th, has a very large range. For example,Baskaran et al. [1992] used a 0.4-mm prefilter and re-ported a colloidal 234Th (.10 kDa) of 10–50%, with onenumber as high as 78%. Similarly, Niven et al. [1995] alsoreported relatively high colloidal 234Th (.10 kDa) of6–70%, using a 0.2-mm prefilter. On the other hand,Moran and Buesseler [1993] reported colloidal 234Th(.10 kDa) as low as 0.04% in the Gulf of Maine. Theseerratic numbers and large differences between differentstudies are beyond those expected from natural variabil-ity. Even though different investigators used differentprefilters, this cannot be the cause of these large varia-tions. Clearly, sampling protocols and the integrity ofultrafilters or other procedural artifacts must be partlyresponsible for these variabilities. Therefore the samereservations as those described in the methodology sec-tion apply here for the measurements of colloidalTh(IV) fraction (see below). Direct comparisons of re-

TABLE 8. Thorium 234 Characterization of Colloidal Organic Matter in Marine Environments

Reference Location Sample Fraction Salinity RangeFc/d-

234Th,%

Apparent ResidenceTime, days

Baskaran et al. [1992] Gulf of Mexico 10 kDa to 0.4 mm 30–36.2 10–78 4–26Moran and Buesseler [1992] Atlantic 10 kDa to 0.2 mm NA 11 10Baskaran and Santschi [1993] coastal seawater 10 kDa to 0.4 mm 24 33 ;1Moran and Buesseler [1993] Buzzards Bay 10 kDa to 0.2 mm 31.25–31.77 3–34 0.11–0.68

Gulf of Maine 31.77–34.9 0.04–1 0.06–0.47Huh and Prahl [1995] NE Pacific 10 kDa to 0.45 mm 32–34 13 6Niven et al. [1995] Bedford Basin 10 kDa to 0.2 mm ;28–30 6–70 NASantschi et al. [1995] Gulf of Mexico 10 kDa to 0.2 mm 30.6–36.4 3–9 1–20Santschi et al. [1995] MAB 10 kDa to 0.2 mm 31–34.6 9–13 1–3Guo et al. [1996a] Gulf of Mexico 10 kDa to 0.2 mm 30–36.4 4–11 1–7Guo et al. [1996a] MAB 10 kDa to 0.2 mm 31–36.3 7–17 1–14Liang et al. (submitted manuscript, 1996) Puget Sound 10 kDa to 0.45 mm 28.8–30.4 4–10 0.1Santschi et al. [1995] Gulf of Mexico 1 kDa to 0.2 mm 30.6–36.4 11–58 3–30Santschi et al. [1995] MAB 1 kDa to 0.2 mm 30.8–35.2 24–64 3–30Guo et al. [1996a] Gulf of Mexico 1 kDa to 0.2 mm 30–36.4 39–67 7–65Guo et al. [1996a] MAB 1 kDa to 0.2 mm 31–39.3 25–65 5–53

Fc/d is the percentage of the colloidal fraction in the total dissolved fraction (,0.2-mm or 0.4-mm fraction). If Fc/d data were not available,they were calculated from particulate and total concentrations given by the authors. MAB is Middle Atlantic Bight. NA is not available.

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 31

sults from different studies using different sampling pro-tocols thus have to be made with extreme caution.Very recently, more consistent colloidal 234Th data

emerged from studies with more rigorous controls onmass balance and integrity (Table 8). For example,Santschi et al. [1995] reported that 3–9% of the totaldissolved 234Th was in the .10-kDa colloidal fraction,Huh and Prahl [1995] reported a mean colloidal (.10kDa) 234Th of ;13% in the NE Pacific, and Y. Liang etal. (Behavior of colloidal 234Th in Puget Sound, WA,submitted to Journal of Marine Research, 1996) (herein-after referred to as Liang et al., submitted manuscript,1996) reported 4–10% in the Puget Sound. Guo et al.[1996a] also showed 4–11% of colloidal 234Th (.10kDa) in the Gulf of Mexico and 7–17% in the MiddleAtlantic Bight.While macromolecular organic matter in the size

range of 10 kDa to 0.2 or 0.4 mm fraction only accountedfor ;10% of the bulk DOM in seawater, the 1-kDa to0.2-mm fraction composed up to 50% of the total DOM(see previous section and Table 2). Very few of thethorium isotopic studies reported on the degree thoriumis complexed in the truly dissolved fraction (,1 kDa), aswell as in the 1- to 10-kDa colloidal fraction. OnlySantschi et al. [1995] andGuo et al. [1996a] had collecteda larger spectrum of COM (.1 kDa) in order to char-acterize its 234Th activities. Some results using 1-kDaultrafilters are listed in Table 8. Indeed, 234Th in the1-kDa to 0.2-mm fraction, in general, is significantlyhigher than that in the 10-kDa to 0.2-mm fraction in thesame study areas (Table 8). For example, the .1-kDacolloidal 234Th was 11–58% in the Gulf of Mexico and3–9% for the .10-kDa fraction [Santschi et al., 1995].Similarly, the .1-kDa colloidal 234Th was 25–65% ver-sus 7–17% for the .10-kDa fraction in the MiddleAtlantic Bight [Guo et al., 1996a].7.2.2. Apparent turnover times derived from 234Th.

Apparent colloidal residence times derived from 234Thare,1–26 days for the HMW COM10 (10-kDa to 0.2- or0.4-mm fraction) and 3–65 days for the COM1 fractionbetween 1 kDa and 0.2 mm (Table 8). The mean resi-dence times of both the HMW COM10 and COM1 indifferent oceanic environments are consistently short,indicating that the HMW COM fraction is turning overmuch faster than the bulk DOM, which is cycling in theocean on thousands of years of timescales [Williams andDruffel, 1987; Bauer et al., 1992]. Thus macromolecularorganic matter fractions in seawater are of higher reac-tivities and thus belong to a more labile pool in themarine carbon cycle. It seems that the reactivities ofDOM in seawater are correlated with the predominantphases defined by molecular weight, consistent with re-sults in the previous sections. Therefore DOM in sea-water is heterogeneous not only in terms of molecularweights but also in terms of turnover times and chemicalreactivities [Guo et al., 1996b]. The cycling of DOM inthe ocean is thus more complex than previously believedand presents further challenges.

Short residence times for the HMW COM10 fractionderived from 234Th have been widely reported (see Ta-ble 8) and are consistent with its contemporary D14Cvalues in the upper water column. However, if ;30–50% of the DOM (e.g., COM1 or 1-kDa to 0.2-mmfraction) turns over on such a short timescale, then themajority of DOM in seawater should recycle on a muchlonger timescale than that derived from the apparent14C ages in the bulk DOM pool. In estuarine and coastalseawater, where higher D14C values have been observedfor the COM1 fraction, thorium-derived residence timesfor the COM1 seem to be compatible with those fromapparent 14C ages [Santschi et al., 1995; Guo et al.,1996b]. However, short residence times derived from234Th for COM1 are often in contradiction with oldapparent 14C ages of the same colloidal pool in openocean environments.Guo et al. [1996a] have argued that turnover times of

COM derived from 234Th using the current thoriumscavenging models [Baskaran et al., 1992; Moran andBuesseler, 1992] likely underestimate values of the trueresidence time of colloids in the ocean since in situscavenging might not adequately be represented by se-rial processes. Colloidal residence times of 1 day forCOM10, as are frequently being calculated for both theMiddle Atlantic Bight and the Gulf of Mexico, are notcompatible with those calculated from the colloidalpumping model in the serial formulation of Honeymanand Santschi [1989], using a reasonable set of parametervalues.Furthermore, laboratory studies suggest that revisions

for the use of Th(IV) for obtaining rate information onparticle cycling in ocean waters may be needed [Quigleyet al., 1996]. For example, Quigley et al. [1996], by exam-ining the sorption rates and intensity of Th(IV) ontohematite particles, found that while tracer Th(IV) sorbsas an inner-sphere complex, its sorption rate is rapid(,1 min) and irreversible on timescales of days toweeks. Moreover, they found that slow apparent sorp-tion rates can be experimentally produced through con-trolled particle coagulation and apparent desorption ofTh(IV) can be produced through disaggregation ofTh(IV) bearing colloidal hematite.While 234Th is likely an appropriate tracer for the

dynamics of particles and HMW COM in the upperwater column, it may not be a good tracer for dissolvedand lower molecular weight colloidal fraction (e.g., 1–10kDa) if this fraction were to turn over on timescales of$10 years. As an extreme example, the 234Th-derivedresidence time will be #10 years if 234Th/238U is 0.99 inthe colloidal fraction. However, 10 years is still a con-temporary age for 14C (i.e., younger than ;40 yearssince the beginning of atomic bomb tests). Clearly, both234Th and 14C have limitations as tracers for those or-ganic carbon fractions which may turn over on decadaltimescales.

32 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

7.2.3. Partitioning of Th between dissolved, colloi-dal, and particulate phases. The distribution of differ-ent molecular weight fractions of 234Th in the totaldissolved 234Th is broadly similar to the partitioning oforganic carbon (Figure 10). The similarity of thoriumand organic carbon partitioning among dissolved, colloi-dal, and particulate phases suggests that Th(IV) com-plexes uniformly to organic matter of all sizes [Guo et al.,1996a].Coefficients for the partitioning of 234Th between

particulate ( p) and truly dissolved (d) forms, Kp 5[Thp]/([Thd] 3 Cp), colloidal (.1-kDa or .10-kDafractions) and the truly dissolved (,1 kDa) form, KC1 5[ThC1]/([Thd] 3 CC1) or KC10 5 [ThC10]/([Thd] 3CC10), and particulate and traditionally defined “dis-solved” (D) forms (#0.4 or #0.2 mm), Kd 5 [Thp]/([ThD] 3 Cp), are listed in Table 9. The activity con-centration of 234Th in the total “dissolved” form includesthose of truly dissolved and colloidal fractions, i.e.,[234ThD] 5 [234Thd] 1 [234Thc]. In addition, Cp, CC1,and CC10 are the mass concentrations of suspendedparticles, .1 kDa colloids, and .10 kDa colloids, re-spectively. Mass concentrations of colloids, CC1 andCC10, can be calculated from measured concentrationsof COC1 and COC10 in the same ultrafiltration samplesassuming [COM]5 23 [COC] since marine colloids aremostly organic in nature.

Table 9 shows that average values of KC (both KC1and KC10) are similar to those of Kp (also see Baskaranet al. [1992] and Moran and Buesseler [1993]). In otherwords, average values of coefficients for the partitioningof 234Th are not significantly different for Kp, KC10, andKC1 [Guo et al., 1996a]. The similarity between thesedistribution coefficients (i.e., Kp, KC10, and KC1) sug-gests that the complexation between 234Th and organiccarbon in the ocean is not simply related to the specificsurface area, or pool size. This result is surprising, sincespecific surface areas or site concentrations should in-crease with decreasing size of the particle or colloid. Itthus appears that the specific surface site density ofTh(IV) complexing ligands is decreasing with decreasingcolloidal or particle size. In addition, specific complexingsites for Th(IV) might also change as a function of“freshness” or production rate (or mechanism) of or-ganic carbon in the ocean. Furthermore, organic coat-ings likely control the adsorption of metals onto particlesas suggested by Balistrieri et al. [1981], Davis [1982], andothers.

8. COAGULATION RATES OF COLLOIDS

Coagulation is the formation of particles from multi-ple collisions of colloids or macromolecules in aquaticenvironments. The importance of coagulation has longbeen recognized [e.g., Sholkovitz, 1976; Honeyman andSantschi, 1989; Jackson and Lochmann, 1992] as a con-trol for the fate and transport of chemical species [Hon-eyman and Santschi, 1992; Stumm and Morgan, 1995], aswell as for particle dynamics [e.g., Jackson, 1990].Therefore the role of coagulation and colloids in the

transfer of trace elements from the dissolved to theparticulate pool has received great attention over theyears. Most of these studies have been conducted usingmodel colloids under well-defined laboratory conditions[e.g., Liang and Morgan, 1990; Honeyman and Santschi,1991]. Recently, direct evidence for the aggregation ofcolloids in seawater has been reported from size distri-bution measurements [e.g.,Wells and Goldberg, 1993]. Inaddition, coagulation rates of colloids using natural wa-ter, natural colloids, and natural particles in radiotracerexperiments have been directly studied [e.g., Santschi etal., 1987; Stordal et al., 1996b].

Figure 10. Relationship between the partitioning of colloidal234Th and colloidal organic carbon in marine environments[from Guo et al., 1996a]. MAB, Middle Atlantic Bight; GOM,Gulf of Mexico.

TABLE 9. Partition Coefficients (K) of 234Th Between Dissolved, Colloidal, and Particulate Phases in Seawater

ReferenceKd,

105 mL g21Kp,

105 mL g21KC10,*

105 mL g21KC1,

105 mL g21

Baskaran et al. [1992] 3.1–8.7 3.5–14.3 (4–30) z z zMoran and Buesseler [1993] 6.0–47 6.1–47 (0.3–3.8) z z zGuo et al. [1996a] 1.3–49 2.5–60 5.5–69 4.3–37

See text for definitions of Kd, Kp, KC10, and KC1.*Numbers in parentheses were calculated by the referenced authors from estimated colloidal mass concentrations.

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 33

Using natural colloids isolated from riverine watersand tagged with 203Hg tracer, Stordal et al. [1996b] ob-served a transfer of radioisotopic mercury from thecolloidal (1 kDa to 0.4 mm) to the particulate pool (.0.4mm), on timescales of hours to days, with rates depend-ing on the particle concentrations in the system. Thetransfer occurred by two separate first-order processes, afaster initial process and a slower coagulation process[Stordal et al., 1996b]. Even though 85% of the initialorganic colloidal 203Hg was found in the particulatefraction after 3 days, less than 10% of the organic carbonwas transferred into the particulate fraction during theexperiment. It thus seems that coagulation processes aremore important for the removal and transport of tracemetals than for macromolecular organic matter.

9. DISCUSSION

9.1. Marine Versus Terrestrial OriginOnly parts of terrestrial DOM enter the ocean due to

removal by precipitation and/or flocculation in estuarieswhen riverine waters mix with seawater [e.g., Sholkovitz,

1976]. This is especially true for HMW humic substancessince more river-borne DOM is of HMWmaterials [e.g.,Benner and Hedges, 1993; Guo, 1995]. Thus most marineDOM is produced in situ. However, an exact accountingof the sources of DOM in seawater, the percentage ofterrestrial organic matter present, and the mechanismsand rates of cycling in the ocean are still unclear.Striking differences in the chemical properties be-

tween terrestrial and marine DOM include aromaticity,lignin-phenolic content, acidity, elemental composition(e.g., C/N/S ratio), and isotopic signatures (e.g., 2H, 13C,14C, and 15N). These have been used to identify sourcesof DOM in marine environments. For example, lignin-phenolic signals in oceanic DOM suggested that ;10%of dissolved marine humic substances are of terrestrialorigin [e.g., Hedges et al., 1992], which amounts to;0.5% of the bulk DOM [e.g., Meyers-Schulte andHedges, 1986]. Values in between these have been re-ported for COM1 by Bianchi et al. (submitted manu-script, 1996).Moreover, a linear increase of d13C values from river

to estuarine and then to coastal waters has been shownfor COM1 (.1 kDa) in the Gulf of Mexico [Benner et al.,1992a; Santschi et al., 1995]. The increase of d13C withincreasing salinity clearly demonstrated a mixing be-tween terrestrial and marine DOM. However, the trendof d15N values of COM1 during estuarine mixing wasdifferent from that of d13C [Benner et al., 1992a]. Usingradiocarbon signatures, Santschi et al. [1995] showedthat D14C values of COM decreased from river to oce-anic waters. A typical example for distinguishing differ-ent source functions of COM1 using both D14C valuesand elemental composition (or C/N ratios) is shown inFigure 11. COM1 extracted from estuarine waters con-tained higher C/N ratios and high D14C values [Guo etal., 1996b]. As marine DOM components increased fromestuarine to coastal waters, C/N ratios and D14C valuesof COM1 decreased both in the Gulf of Mexico and inthe Middle Atlantic Bight (see Figure 11). Moreover,during COM transport from the upper water column tothe bottom, C/N ratios of COM1 increased again fromsurface to bottom waters due to COM degradation,whereas D14C values decreased monotonically from sur-face to deep waters (Figure 11).While these results are encouraging, a more quanti-

tative evaluation of terrestrial versus marine sources ofDOM in the ocean is needed. A multiple tracer ap-proach [e.g., Santschi et al., 1995; Guo et al., 1996b]and/or measurements of isotope ratios of single com-pounds [e.g., Eglington et al., 1996] appear to be mostpromising.

9.2. Benthic Boundary Layer TransportBenthic boundary layer transport is an important

process whose study could provide more clues for un-raveling the organic carbon cycling puzzle of the ocean[e.g., Anderson et al., 1994; Bianchi et al., submittedmanuscript, 1996]. Fluxes of dissolved and colloidal or-

Figure 11. Relationship between D14C values and organic C/Natomic ratios of COM1 (1 kDa to 0.2 mm) in (a) the Gulf ofMexico and (b) the Middle Atlantic Bight [from Guo et al.,1996b].

34 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

ganic matter from sediment pore waters have beenshown to be significant [e.g., Burdige et al., 1992; Alperinet al., 1994] and may be accelerated during resuspensionevents. Under strong bottom currents which producehigh bottom shear conditions, prevalent in the dynamicareas of the continental margins, sediment resuspensioncan cause aggregation or sorption of COM as well asdisaggregation or peptization of particulate and sedi-mentary organic matter [e.g., Santschi et al., 1987; New-man et al., 1990]. Therefore benthic boundary layerprocesses could significantly contribute to the produc-tion of possibly old and more refractory DOM to theoverlying water column.For example, both aromatic carbon percentages, as

derived from the 13C-NMR spectra, and lignin-phenolconcentrations in the POM and COM in shelf and slopewaters from the Gulf of Mexico were considerablyhigher when compared with results from oceanic DOM(Bianchi et al., submitted manuscript, 1996). The rela-tively high aromaticity and loliolide content of COM inopen gulf waters, at salinities of 35–36‰, were thoughtto be the result of nepheloid layer transport of sedimen-tary organic matter containing diagenetically altered ma-rine and terrestrial compounds (Bianchi et al., submittedmanuscript, 1996). Therefore lateral transport at theshelf/slope edge through benthic boundary layer pro-cesses could be an important mechanism for the injec-tion of terrestrially and/or sedimentary derived organicmatter into deep slope waters. Efficient terrestrial par-ticle transport through benthic boundary layers in con-tinental margin waters was also indicated from thehigher 230Th and 232Th contents of the waters of theMiddle Atlantic Bight [Guo et al., 1995b]. Other evi-dence comes from the relatively old apparent 14C agesfound in the POM collected by sediment traps in theMiddle Atlantic Bight [e.g., Anderson et al., 1994] (seeTable 7) and from the unusually old apparent 14C ages inthe HMW COM fraction of bottom waters in the sameregion [Guo et al., 1996b]. The old organic carbon frac-tion may have been derived from sedimentary organicmatter via sediment resuspension and other benthicfractionation processes.

9.3. Changes in the Paradigms of Marine OrganicMatter CyclingWhile DOM in oceanic mixed layers appears to be

more variable and its concentrations controlled by bio-chemical and physical processes, deep water DOM con-centrations are more constant and regulated by pro-cesses on timescales similar to those for oceanic mixing.The old paradigm of organic matter diagenesis consid-ered HMW organic matter a geopolymer, i.e., the prod-uct of slow polymerization of lower molecular weightfractions and thus its most refractory component. Thisview has to be modified in light of the recent evidencesummarized here. A reversal of the carbon flow is sug-gested for the upper water column, where the HMWorganic carbon fraction is mainly composed of biopoly-

mers such as labile lipopolysaccharides [e.g., Benner,1996; Aluwihare et al., 1996] and D14C values decreasedfrom POM to HMW COM to LMW DOM [Santschi etal., 1995; Guo et al., 1996b]. Physical associations such asmicelles might protect more labile HMW compoundsfrom rapid biodegradation [e.g., Borch and Kirchman,1996], thus prolonging their mean life in the euphoticzone.

9.4. Future Research NeedsThe characterization of marine colloids in terms of

chemistry and molecular sizes is still incomplete, despitedecades of research. Since the reactivity (e.g., mobility,bioavailability, and toxicity) and biogeochemical behav-ior of chemical species in aquatic environments areclosely related to their speciation (which includes bothchemical and phase speciation), further studies areneeded to characterize the chemical composition of ma-rine colloids and examine the molecular size distributionof each chemical species, organic and inorganic. Theoutcome of this research has strong implications for thehypothesis that colloids act as reactive intermediates inregulating the transport and fate of trace elements in theocean.The reactivity of organic colloids has so far been

constrained by estimates of apparent ages or turnoverrates using short-lived 234Th and long-lived 14C. Becauseboth 234Th and 14C have decay timescale limitations(half-life of 234Th is too short and 14C too long) whentracing dissolved organic matter fractions which mayturn over on decadal time scales, new tracers or multipletracer approaches are needed. Alternative tracers are210Pb (with a half-life of 22 years) and 230Th (7520years), which are particle reactive radionuclides and thushave, at times, been found to be associated with colloids(210Pb [Baskaran and Santschi, 1993], 230Th (L. Guo et al.,unpublished results, 1996)). Because of the complexityof retardation and fractionation processes in the benthicboundary layer, more work is needed to study the detailsof these mechanisms. Examples are the selective bio-chemical degradation and physical size separation pro-cesses which act to fractionate organic matter during itstransport from rivers to pelagic sediments and the sizeselective deposition, resuspension, and bioturbation pro-cesses in the regions near sediment-water interface.More applied research needs include (1) detailed

studies of chemical fractionation during the separationor isolation of colloids from the bulk solution, (2) inter-comparison studies between different laboratories usingthe same sampling techniques, and (3) intercomparisonstudies between sampling techniques using the samestandard materials or processing the same samples.

10. CONCLUSIONS

Recent advances in our knowledge of the occurrenceand characterization of colloidal organic matter in ma-

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 35

rine environments have significantly contributed to ourunderstanding of the cycling of dissolved organic matter(DOM) in the ocean. Results summarized here includethe oceanographically consistent distribution of colloidalorganic matter (COM) in seawater and the biochemical,elemental, and isotopic (stable and radionuclide) char-acterization of marine colloids.Macromolecular or colloidal organic carbon (COC)

in seawater can be operationally separated into severalfractions, e.g., 1 kDa to 0.2 mm (COC1), 3 kDa to 0.2 mm(COC3), and 10 kDa to 0.2 mm (COC10). Both theconcentrations of COC and its percentages in the totaldissolved fraction decreased from estuarine to coastaland then to oceanic waters and vertically from surface todeep waters in the ocean. On average, 4–7% of the totalDOC was in the COC10 fraction, 7–14% was in the 3- to10-kDa fraction, and ;24% was in the 1- to 3-kDafraction, leaving ;60% in the ,1-kDa fraction in theGulf of Mexico and the Middle Atlantic Bight. The COCfractions seem to partition in a predictable way in sea-water with DOC concentration as a master variable.Mass concentrations of COM are much higher thanthose of particulate organic matter or total suspendedparticulate matter.Polysaccharides and oligosaccharides, the major com-

pounds of COM, are more abundant in surface watersthan in deep waters, whereas concentrations ofmonosaccharides increased from surface water to deepwaters. Values of C/N ratios of COM decreased fromestuarine to oceanic water but increased from surface todeep waters, consistent with what we know about diage-netic alterations of organic matter in the water column.Among colloidal organic matter fractions the C/N ratiosincreased from lower molecular weight to higher molec-ular weight portions of COM.Measurements of lignin-phenol concentrations in

oceanic DOM have been successfully used to acquirequalitative information on the sources of macromolecu-lar organic matter. In addition, altered and unalteredplant pigments have been detected in COM fractionacross the continental margin waters and thus may beused as planktonic and sedimentary biomarkers ofCOM. The detectable unaltered plant pigments point toa phytoplanktonic source and altered pigments (e.g.,loliolides) to a sedimentary source of marine macromo-lecular organic matter. Further measurements of multi-ple biomarkers in varying fractions of macromolecularorganic matter will put significant constraints on thesource functions and fate of DOM.Colloids could be important intermediates for the

removal of trace elements in aquatic systems. Indeed,most trace elements have been found to associate, to avariable extent, with colloidal material in estuarine andmarine environments. In turn, the inorganic elementalcomposition of colloids may be used to trace the terres-trial sources of colloids in seawater.Signatures from the disequilibrium of 234Th/238U in

COM fractions have been used to derive residence times

of these fractions, resulting in days to weeks of turnovertimes for HMW COM (e.g., 10-kDa to 0.2-mm fraction).Short turnover times indicate that macromolecular or-ganic matter is cycling more rapidly than the bulk DOMpool in the water column, consistent with fast microbialutilization rates of HMW DOM. Radiocarbon measure-ments have demonstrated, for the first time, that theHMW COM fraction in surface waters contained con-temporary D14C values, and thus D14C values of bulkDOM are the result of mixing of different organic matterfractions with varying molecular weights and D14C val-ues. However, bottom water HMW COM in the MiddleAtlantic Bight could be even older than the bulk DOM,indicating that sedimentary organic matter can be asource to the organic carbon pool in the water column.The cycling of DOM in the ocean is thus more com-

plex than previously thought and presents further chal-lenges. Evidence from apparent 14C ages and microbialutilization rates of organic matter suggests that organiccarbon flows largely from particulate organic matter tomacromolecular COM to LMW DOM in the ocean.Conversely, many trace elements appear to move in theopposite direction (i.e., by coagulation). It seems thatold paradigms on the nature of marine DOM have to bemodified. The recent biochemical, microbiological, andisotopic evidence of the lability of HMW organic matterin the upper ocean suggests biopolymers as the majorcomponents of pelagic colloids, while the radiocarbonand biomarker results from the analysis of deep waterCOM suggest a more geopolymeric nature of thesebenthic colloids. Radionuclides and biomarkers havebeen successfully used as tracers to study the cycling ofCOM in marine environments. However, more multi-tracer approaches and isotopic analysis of individualcompounds are needed for making further progress.

ACKNOWLEDGMENTS. We thank Thomas Torgersenand two anonymous reviewers for their helpful commentswhich improved the manuscript. This work was supported bythe Office of Health and Environmental Research of the De-partment of Energy (grant DE-FG05-92ER61421), the Officeof Naval Research (grant N00014-93-1-0877), and the TexasInstitute of Oceanography.Thomas Torgersen was the editor responsible for this pa-

per. He thanks cross-disciplinary reviewers Heidi Houston andDavid DeHor.

REFERENCES

Aiken, G. R., D. M. Mcknight, R. L. Wershaw, and P. Mac-Carthy, Humic Substances in Soil, Sediment, and Water, 675pp., John Wiley, New York, 1985.

Alperin, M. J., D. B. Albert, and C. S. Martens, Seasonalvariations in production and consumption rates of dissolvedorganic carbon in an organic rich coastal sediment,Geochim. Cosmochim. Acta, 58, 4909–4930, 1994.

Aluwihare, L. I., D. J. Repeta, and R. F. Chen, Structuralcharacterization of high molecular weight colloidal organic

36 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

matter. Is DOC a biopolymer?, Eos Trans. AGU, 77(3),Ocean Sci. Meet. Suppl., OS41, 1996.

Amon, R. M. W., and R. Benner, Rapid cycling of high-molecular-weight dissolved organic matter in the ocean,Nature, 369, 549–552, 1994.

Amon, R. M. W., and R. Benner, Photochemical and microbialconsumption of dissolved organic carbon and dissolvedoxygen in the Amazon River system, Geochim. Cosmochim.Acta, 60, 1783–1792, 1996.

Anderson, R. F., G. T. Rowe, R. F. Kemp, S. Trumbore, andP. E. Biscaye, Carbon budget for the mid-slope depocenterof the Middle Atlantic Bight, Deep Sea Res., Part II, 41,669–703, 1994.

Balistrieri, L., P. G. Brewer, and J. W. Murray, Scavengingresidence times of trace metals and surface chemistry ofsinking particles in the deep ocean, Deep Sea Res., Part A,28, 101–121, 1981.

Baskaran, M., and P. H. Santschi, The role of particles andcolloids in the transport of radionuclides in coastal environ-ments of Texas, Mar. Chem., 43, 95–114, 1993.

Baskaran, M., P. H. Santschi, G. Benoit, and B. D. Honeyman,Scavenging of Th isotopes by colloids in seawater of theGulf of Mexico,Geochim. Cosmochim. Acta, 56, 3375–3388,1992.

Baskaran, M., P. H. Santschi, L. Guo, T. S. Bianchi, andC. Lambert, 234Th:238U disequilibria in the Gulf of Mexico:The importance of organic matter and particle concentra-tion, Cont. Shelf Res., 16, 353–380, 1996.

Bauer, J., P. M. Williams, and E. R. M. Druffel, 14C activity ofdissolved organic carbon fractions in the northcentral Pa-cific and Sargasso Sea, Nature, 357, 667–670, 1992.

Beckett, R., and B. T. Hart, Use of field-flow fractionationtechniques to characterize aquatic particles, colloids, andmacromolecules, in Environmental Particles, vol. 2, editedby J. Buffle and H. P. van Leeuwen, pp. 165–206, Lewis,Boca Raton, Fla., 1993.

Beckett, R., Z. Jue, and J. C. Giddings, Determination ofmolecular weight distributions of fulvic and humic acidsusing field flow fractionation, Environ. Sci. Technol., 21,289–295, 1987.

Benner, R., Ultra-filtration for the concentration of bacteria,viruses, and dissolved organic matter, in Marine Particles:Analysis and Characterization, Geophys. Monogr. Ser., vol.63, edited by D. C. Hurd and D. W. Spencer, pp. 181–185,AGU, Washington, D. C., 1991.

Benner, R., Dissolved organic matter in marine systems:Changing paradigms from a biological perspective, EosTrans. AGU, 77(3), Ocean Sci. Meet. Suppl., OS41, 1996.

Benner, R., and J. I. Hedges, A test of the accuracy of freshwater DOC measurements by high-temperature catalyticoxidation and UV-promoted persulfate oxidation, Mar.Chem., 41, 161–165, 1993.

Benner, R., C. Chin-Leo, W. Gardner, B. Eadie, and J. Cotner,The fates and effects of riverine and shelf-derived DOM onMississippi River Plume/gulf shelf processes, in NutrientEnhanced Coastal Ocean Productivity, NECOP WorkshopProceedings, October 1991, TAMU-SG-92-109, pp. 84–94,Tex. A&MUniv. Sea Grant Coll. Program, College Station,1992a.

Benner, R., J. D. Pakulski, M. McCarthy, J. I. Hedges, andP. G. Hatcher, Bulk chemical characteristics of dissolvedorganic matter in the ocean, Science, 255, 1561–1564,1992b.

Benoit, G., S. Oktay, A. Cant, M. O. Hood, C. H. Coleman, O.Corapcioglu, and P. H. Santschi, Partitioning of Cu, Pb, Ag,Zn, Fe, Al and Mn between filter-retained particles, col-loids and solution in 6 Texas estuaries, Mar. Chem., 45,307–336, 1994.

Bianchi, T. S., C. Lambert, P. H. Santschi, M. Baskaran, and

L. Guo, Plant pigments as biomarkers of high-molecular-weight dissolved organic carbon, Limnol. Oceanogr., 40,422–428, 1995.

Borch, N. H., and D. L. Kirchman, Uptake and degradation oflow and high molecular weight organic matter in the Del-aware Bay, Eos Trans. AGU, 77(3), Ocean Sci. Meet.Suppl., OS41, 1996.

Breger, I. A., Organic colloids and natural waters, in OrganicMatter in Natural Waters, edited by D. W. Hood, Occas.Publ. 1, pp. 563–574, Inst. of Mar. Sci., Univ. of Alaska,Fairbanks, 1970.

Brownawell, B. J., The role of colloidal organic matter in themarine geochemistry of PCBs, Ph.D. dissertation, 318 pp.,Woods Hole Oceanogr. Inst./Mass. Inst. of Technol. JointProgram in Oceanogr., Cambridge, Mass., 1986.

Brownawell, B. J., Methods for isolating colloidal organicmatter from seawater: General considerations and recom-mendations, in Marine Particles: Analysis and Characteriza-tion, Geophys. Monogr. Ser., vol. 63, edited by D. C. Hurdand D. W. Spencer, pp. 187–194, AGU, Washington, D. C.,1991.

Bruland, K. W., M. L. Wells, and G. J. Smith, The distributionof particulate and colloidal metals in surface waters ofNarragansett Bay, RI, Eos Trans. AGU, 77(3), Ocean Sci.Meet. Suppl., OS166, 1996.

Buesseler, K. O., J. A. Andrews, M. C. Hartman, R. Belastock,and F. Chai, Regional estimates of the export flux of par-ticulate organic carbon derived from thorium-234 duringthe JGOFS EQPAC program, Deep Sea Res., Part II, 42,777–804, 1995.

Buesseler, K. O., et al., An intercomparison of cross-flowfiltration techniques used for sampling marine colloids:Overview and organic carbon results,Mar. Chem., 55, 1–31,1996.

Buffle, J., Complexation Reactions in Aquatic Systems: An An-alytical Approach, 629 pp., Ellis Horwood, New York, 1990.

Buffle, J., and G. G. Leppard, Characterization of aquaticcolloids and macromolecules, 1, Structure and behavior ofcolloidal material, Environ. Sci. Technol., 29, 2169–2175,1995.

Buffle, J., D. Perret, and M. Newman, The use of filtration andultrafiltration for size fractionation of aquatic particles,colloids and macromolecules, in Environmental Particles,vol. 1, edited by J. Buffle and H. P. van Leeuwen, pp.171–230, Lewis, Boca Raton, Fla., 1993.

Burdige, D. J., M. J. Alperin, J. Homstead, and C. S. Martens,The role of benthic fluxes of dissolved organic carbon inoceanic and sedimentary carbon cycle, Geophys. Res. Lett.,19, 1851–1854, 1992.

Burgess, R. M., R. A. Mckinney, W. A. Brown, and J. G.Quinn, Isolation of marine sediment colloids and associatedpolychlorinated biphenyls: An evaluation of ultrafiltrationand reverse-phase chromatography, Environ. Sci. Technol.,30, 1923–1932, 1996.

Bushaw, K. L., R. G. Zepp, M. A. Tarr, D. Schulz-Jander,R. A. Bourbonniere, R. E. Hodson, W. L. Miller, D. A.Bronk, and M. A. Moran, Photochemical release of biolog-ically available nitrogen from aquatic dissolved organic mat-ter, Nature, 381, 404–407, 1996.

Carlson, D. J., M. L. Brann, T. H. Mague, and L. M. Mayer,Molecular weight distribution of dissolved organic materi-als in seawater determined by ultrafiltration: A re-examina-tion, Mar. Chem., 16, 155–171, 1985.

Chin, Y.-P., and P. M. Gschwend, The abundance, distribution,and configuration of porewater organic colloids in recentsediments, Geochim. Cosmochim. Acta, 55, 1309–1317,1991.

Chin, Y.-P., and P. M. Gschwend, Partitioning of polycyclic

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 37

aromatic hydrocarbons to marine porewater organic col-loids, Environ. Sci. Technol., 26, 1621–1626, 1992.

Chiou, C. T., R. L. Malcolm, T. I. Brinton, and D. E. Kiel,Water solubility enhancement of some organic pollutantsand pesticides by dissolved humic and fulvic acids, Environ.Sci. Technol., 20, 502–508, 1986.

Chiou, C. T., D. E. Kile, T. I. Brinton, R. L. Malcolm, andJ. A. Leenheer, A comparison of water solubility enhance-ments of organic solutes by aquatic humic materials andcommercial humic acids, Environ. Sci. Technol., 21, 1231–1234, 1987.

Coale, K. H., and K. W. Bruland, Oceanic stratified euphoticzone as elucidated by 234Th:238U disequilibria, Limnol.Oceanogr., 32, 189–200, 1987.

Dai, M.-H., and J.-M. Martin, First data on trace metal leveland behaviour in two major Arctic river-estuarine systems(Ob and Yenisey) and in the adjacent Kara Sea, Russia,Earth Planet. Sci. Lett., 131, 127–141, 1995.

Dai, M.-H., J.-M. Martin, and G. Cauwet, The significant roleof colloids in the transport and transformation of organiccarbon and associated trace metals (Cd, Cu, and Ni) in theRhone Delta (France), Mar. Chem., 51, 159–175, 1995.

Davis, J. A., Adsorption of natural dissolved organic matter atthe oxide/water surface, Geochim. Cosmochim. Acta, 46,2381–2393, 1982.

Druffel, E. R. M., and R. M. Williams, Identification of a deepmarine source of particulate organic carbon using bomb14C, Nature, 347, 172–174, 1990.

Druffel, E. R. M., and P. M. Williams, Importance of isotopemeasurements in marine organic geochemistry, Mar.Chem., 39, 209–216, 1992.

Druffel, E. R. M., P. M. Williams, J. E. Bauer, and J. R. Ertel,Cycling of dissolved and particulate organic matter in theopen ocean, J. Geophys. Res., 97, 15,639–15,659, 1992.

Eadie, B. J., L. M. Jeffrey, and W. M. Sackett, Some observa-tions on the stable carbon isotope composition of dissolvedand particulate organic carbon in the marine environment,Geochim. Cosmochim. Acta, 42, 1265–1269, 1978.

Eglinton, T. I., B. Nelson, A. P. McNichol, J. E. Bauer, andE. R. M. Druffel, Radiocarbon ages of sedimentary lipids astracers of organic carbon input to marine sediments, paperpresented at the Spring 1996 ACS Meeting, Am. Chem.Soc., New Orleans, La., 1996.

Guo, L., Cycling of dissolved and colloidal organic matter inoceanic environments as revealed by carbon and thoriumisotopes, Ph.D. dissertation, 230 pp., Tex. A&M Univ.,College Station, 1995.

Guo, L., and P. H. Santschi, A critical evaluation of cross-flowultrafiltration technique for sampling colloidal organic car-bon in seawater, Mar. Chem., 55, 113–127, 1996.

Guo, L., C. H. Coleman Jr., and P. H. Santschi, The distribu-tion of colloidal and dissolved organic carbon in the Gulf ofMexico, Mar. Chem., 45, 105–119, 1994.

Guo, L., P. H. Santschi, and K. W. Warnken, Dynamics ofdissolved organic carbon (DOC) in oceanic environments,Limnol. Oceanogr., 40, 1392–1403, 1995a.

Guo, L., P. H. Santschi, M. Baskaran, and A. Zindler, Distri-bution of dissolved and particulate 230Th and 232Th inseawater from the Gulf of Mexico and off Cape Hatteras asmeasured by SIMS, Earth Planet. Sci. Lett., 133, 117–128,1995b.

Guo, L., P. H. Santschi, and M. Baskaran, Interaction ofthorium isotopes with colloidal organic matter in oceanicenvironments, Colloids Surf. A, in press, 1996a.

Guo, L., P. H. Santschi, L. A. Cifuentes, S. Trumbore, andJ. Southon, Cycling of high molecular weight dissolvedorganic matter in the Middle Atlantic Bight as revealed bycarbon isotopic (13C and 14C) signatures, Limnol. Ocean-ogr., 41, 1242–1252, 1996b.

Gustafsson, O., K. O. Buesseler, and P. M. Gschwend, Tests onthe integrity of cross-flow filtration for marine colloids,Mar.Chem., 55, 93–111, 1996.

Hedges, J. I., P. G. Hatcher, J. R. Ertel, and K. J. Meyers-Schulte, A comparison of dissolved humic substances fromseawater with Amazon River counterparts by 13C-NMRspectrometry, Geochim. Cosmochim. Acta, 56, 1753–1757,1992.

Honeyman, B. D., and P. H. Santschi, Brownian-pumpingmodel for oceanic trace metal scavenging: Evidence fromTh isotopes, J. Mar. Res., 47, 951–992, 1989.

Honeyman, B. D., and P. H. Santschi, Coupling adsorption andparticle aggregation: Laboratory studies of “colloidalpumping” using 59Fe-labeled hematite, Environ. Sci. Tech-nol., 25, 1739–1747, 1991.

Honeyman, B. D., and P. H. Santschi, The role of particles andcolloids in the transport of radionuclides and trace metals inthe oceans, in Environmental Particles, IUPAC Environ.Anal. Chem. Ser., vol. 1, edited by J. Buffle and H. P. vanLeeuwen, chap. 10, pp. 379–423, Lewis, Boca Raton, Fla.,1992.

Huh, C.-A., and F. G. Prahl, Role of colloids in upper oceanbiogeochemistry in the northeast Pacific elucidated from238U-234Th disequilibria, Limnol. Oceanogr., 40, 528–532,1995.

Jackson, G. A., A model of the formation of marine algal flocsby physical coagulation processes, Deep Sea Res., Part A, 37,197–211, 1990.

Jackson, G. A., and S. E. Lochmann, Effect of coagulation onnutrient and light limitation of an algal bloom, Limnol.Oceanogr., 37, 77–89, 1992.

Keil, R. G., and D. L. Kirchman, Abiotic transformation oflabile protein to refractory protein in sea water, Mar.Chem., 45, 187–196, 1994.

Keil, R. G., D. B. Montlucon, F. G. Prahl, and J. I. Hedges,Sorptive preservation of labile organic matter in marinesediments, Nature, 370, 549–552, 1994.

Kepkay, P. E., S. E. H. Niven, and T. G. Milligam, Lowmolecular weight and colloidal DOC production during aphytoplankton bloom, Mar. Ecol. Prog. Ser., 100, 233–244,1993.

Kirchman, D. L., Y. Suzuki, C. Garside, and H. W. Ducklow,High turnover rates of dissolved organic carbon during aspring phytoplankton bloom, Nature, 352, 612–614, 1991.

Lara, R. J., and D. N. Thomas, Isolation of marine dissolvedorganic matter: Evaluation of sequential combinations ofXAD resins 2, 4, and 7, Anal. Chem., 66, 2417–2419, 1994.

Liang, L., and J. J. Morgan, Chemical aspects of iron oxidecoagulation in water: Laboratory studies and implicationsfor natural systems, Aquat. Sci., 52, 32–55, 1990.

Mantoura, R. F. C., and E. M. S. Woodward, Conservativebehavior of riverine dissolved organic carbon in the SevernEstuary: Chemical and geochemical implications, Geochim.Cosmochim. Acta, 47, 1293–1309, 1983.

Martin, J.-M., M.-H. Dai, and G. Cauwet, Significance ofcolloids in the biogeochemical cycling of organic carbonand trace metals in a coastal environment—Example of theVenice Lagoon (Italy), Limnol. Oceanogr., 40, 119–131,1995.

Maurer, L. G., Organic polymers in seawater: Changes withdepth in the Gulf of Mexico, Deep Sea Res., 23, 1059–1064,1976.

McCarthy, M. D., J. I. Hedges, and R. Benner, The chemicalcomposition of dissolved organic matter in seawater, Chem.Geol., 107, 503–507, 1993.

Means, J. C., and R. D. Wijayaratne, Role of colloids in thetransport of hydrophobic pollutants, Science, 215, 968–970,1982.

Means, J. C., and R. D. Wijayaratne, Chemical characteriza-

38 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS

tion of estuarine colloidal organic matter: Implications foradsorptive processes, Bull. Mar. Sci., 35, 449–461, 1984.

Means, J. C., and R. D. Wijayaratne, Sorption of Benzedrine,toluidine, and azobenzene on colloidal organic matter, inAquatic Humic Substances, edited by I. H. Suffet andP. MacCarthy, pp. 209–221, Am. Chem. Soc., Washington,D.C., 1989.

Meyers-Schulte, K. J., and J. I. Hedges, Molecular evidence fora terrestrial component of organic matter dissolved inocean water, Nature, 321, 61–63, 1986.

Miller, L. A., and K. W. Bruland, Organic speciation of silverin marine waters, Environ. Sci. Technol., 29, 2616–2621,1995.

Moran, M. A., L. A. Pomeroy, E. S. Sheppard, L. P. Atkinson,and R. E. Hodson, Distribution of terrestrially deriveddissolved organic matter on the southern U.S. continentalshelf, Limnol. Oceanogr., 36, 1134–1149, 1991.

Moran, S. B., and K. O. Buesseler, Short residence time ofcolloids in the upper ocean estimated from 238U-234Thdisequilibra, Nature, 359, 221–223, 1992.

Moran, S. B., and K. O. Buesseler, Size fractionated 234Th incontinental shelf waters off New England: Implications forthe role of colloids in oceanic trace metal scavenging, J.Mar. Res., 51, 893–922, 1993.

Moran, S. B., and R. M. Moore, The distribution of colloidalaluminum and organic carbon in coastal and open oceanwaters off Nova Scotia, Geochim. Cosmochim. Acta, 53,2519–2527, 1989.

Moran, S. B., P. A. Yeats, and P. W. Balls, On the role ofcolloids in trace metals solid-solution partitioning in conti-nental shelf waters: A comparison of model results and fielddata, Cont. Shelf Res., 16, 397–408, 1996.

Newman, K., S. L. Frankel, and K. D. Stolzenbach, Flowcytometric detection and sizing of fluorescent particles de-posited at a sewage outfall site, Environ. Sci. Technol., 24,513–518, 1990.

Niven, S. E. H., P. E. Kepkay, and A. Boraie, Colloidal organiccarbon and colloidal 234Th dynamics during a coastal phy-toplankton bloom, Deep Sea Res., Part II, 42, 257–273, 1995.

Ogawa, H., and N. Ogura, Comparison of two methods formeasuring dissolved organic carbon in sea water, Nature,356, 696–698, 1992.

Ogura, N., Molecular weight fractionation of dissolved organicmatter in coastal seawater by ultrafiltration, Mar. Biol. Ber-lin, 24, 305–312, 1974.

Ogura, N., High molecular weight organic matter in seawater,Mar. Chem., 5, 535–549, 1977.

Pakulski, J. D., and R. Benner, Abundance and distribution ofcarbohydrates in the ocean, Limnol. Oceanogr., 39, 930–940, 1994.

Powell, R. T., W. M. Landing, and J. E. Bauer, Distributions ofcolloidal trace metals and carbon in the North Atlantic, EosTrans. AGU, 77(3), Ocean. Sci. Meet. Suppl., OS193, 1996.

Quigley, M. S., B. D. Honeyman, and P. H. Santschi, Thoriumsorption in the marine environment: Equilibrium partition-ing at the hematite/water interface, sorption/desorption ki-netics and particle tracing, Aquat. Geochem., 1, 277–301,1996.

Reitmeyer, R., R. T. Powell, W. M. Landing, and C. I. Mea-sures, Colloidal Al and Fe in seawater: An intercomparisonbetween various cross-flow ultrafiltration systems, Mar.Chem., 55, 75–91, 1996.

Sackett, W. M., Stable carbon isotope studies on organic mat-ter in the marine environment, in Handbook of Environ-mental Isotope Geochemistry, pp. 139–169, Elsevier, NewYork, 1989.

Sakugawa, H., and N. Handa, Isolation and chemical charac-terization of dissolved and particulate polysaccharides in

Mikawa Bay, Geochim. Cosmochim. Acta, 49, 1185–1193,1985.

Santschi, P. H., M. Amdurer, D. Adler, P. O’Hara, Y.-H. Li,and P. Doering, Relative mobility of radioactive trace ele-ments across the sediment-water interface in the MERLmodel ecosystems of Narragansett Bay, J. Mar. Res., 45,1007–1048, 1987.

Santschi, P. H., L. Guo, M. Baskaran, S. Trumbore, J. Southon,T. Bianchi, B. Honeyman, and L. Cifuentes, Isotopic evi-dence for the contemporary origin of high-molecular weightorganic matter in oceanic environments, Geochim. Cosmo-chim. Acta, 59, 625–631, 1995.

Santschi, P. H., J. J. Lenhart, and B. D. Honeyman, Hetero-geneous process affecting trace contaminant distribution inestuaries: The role of natural organic matter, Mar. Chem.,in press, 1996.

Sanudo-Wilhelmy, S. A., E. R. Breuer, M. Yang, I. Rivera-Duarte, and A. R. Flegal, The role of colloids in thetransport of trace metals in the San Francisco Bay estuary,Eos Trans. AGU, 77(3), Ocean Sci. Meet. Suppl., OS166,1996.

Sempere, R., and G. Cauwet, Occurrence of organic colloids inthe stratified estuary of the Krka River (Croatia), EstuarineCoastal Shelf Sci., 40, 105–114, 1995.

Sempere, R., G. Cauwet, and J. Randon, Ultrafiltration ofseawater with a zirconium and aluminum oxide tubularmembrane: Application to the study of colloidal organiccarbon distribution in an estuarine bottom nepheloid layer,Mar. Chem., 46, 49–60, 1994.

Sharp, J. H., Size classes of organic carbon in seawater, Lim-nol. Oceanogr., 18, 441–447, 1973.

Sholkovitz, E. R., Flocculation of dissolved organic and inor-ganic matter during the mixing of river water and seawater,Geochim. Cosmochim. Acta, 40, 831–845, 1976.

Sholkovitz, E. R., Chemical evolution of rare earth elements:Fractionation between colloidal and solution phases of fil-tered river water, Earth Planet. Sci. Lett., 114, 77–84, 1992.

Sholkovitz, E. R., W. M. Landing, and B. L. Lewis, Oceanparticle chemistry: The fractionation of rare earth elementsbetween suspended particles and seawater, Geochim. Cos-mochim. Acta, 58, 1567–1579, 1994.

Sigleo, A. C., and G. R. Helz, Composition of estuarine col-loidal material: Major and trace elements, Geochim. Cos-mochim. Acta, 45, 2501–2509, 1981.

Sigleo, A. C., and S. A. Macko, Stable isotope and amino acidcomposition of estuarine dissolved colloidal material, inMarine and Estuarine Geochemistry, edited by A. C. Sigleoand A. Hattori, pp. 29–46, Lewis, Boca Raton, Fla., 1985.

Sigleo, A. C., and J. C. Means, Organic and inorganic compo-nents in estuarine colloids: Implications for sorption andtransport of pollutants, Rev. Environ. Contam. Technol.,112, 123–147, 1990.

Sigleo, A. C., T. C. Hoering, and G. R. Helz, Composition ofestuarine colloidal material: Organic components,Geochim. Cosmochim. Acta, 46, 1619–1626, 1982.

Sigleo, A. C., P. E. Hare, and G. R. Helz, The amino acidcomposition of estuarine colloidal material, EstuarineCoastal Shelf Sci., 17, 87–96, 1983.

Stordal, M., G. Gill, L.-S. Wen, and P. H. Santschi, Mercuryphase speciation in the surface waters of three Texas estu-aries: Importance of colloidal forms, Limnol. Oceanogr., 41,52–61, 1996a.

Stordal, M. C., P. H. Santschi, and G. A. Gill, Colloidalpumping: Evidence for the coagulation process using natu-ral colloids tagged with 203Hg, Environ. Sci. Technol., inpress, 1996b.

Stumm, W., and J. J. Morgan, Aquatic Chemistry, 3rd ed.,Wiley-Interscience, New York, 1995.

Swarzenski, P. W., B. A. McKee, and J. G. Booth, Uranium

35, 1 / REVIEWS OF GEOPHYSICS Guo and Santschi: CYCLING OF MARINE COLLOIDS ● 39

geochemistry on the Amazon Shelf: Chemical phase parti-tioning and cycling across a salinity gradient, Geochim.Cosmochim. Acta, 59, 7–18, 1995.

Takayanagi, K., and G. T. F. Wong, Organic and colloidalselenium in southern Chesapeake Bay and adjacent waters,Mar. Chem., 14, 141–148, 1984.

Thornton, S. F., and J. McManus, Application of organiccarbon and nitrogen stable isotope and C/N ratios as sourceindicators of organic matter provenance in estuarine sys-tems: Evidence from the Tay estuary, Scotland, EstuarineCoastal Shelf Sci., 38, 219–233, 1994.

Tipping, H., Colloids in the aquatic environment, Chem. Ind.London, 15, 485–490, 1988.

Town, R. M., and H. K. Powell, Limitations of XAD resins forthe isolation of the non-colloidal humic fraction in soilextracts and aquatic samples, Anal. Chim. Acta, 271, 195–202, 1993.

Vernon-Clark, R. N., and E. D. Goldberg, Organic and inor-ganic characterizations of marine colloids, Chem. Ecol., 11,69–83, 1995.

Vold, R. D., and M. J. Vold, Colloid and Interface Chemistry,Addison-Wesley, Reading, Mass., 1983.

Wells, M. L., and E. D. Goldberg, Occurrence of small colloidsin seawater, Nature, 353, 342–344, 1991.

Wells, M. L., and E. D. Goldberg, Colloid aggregation inseawater, Mar. Chem., 41, 353–358, 1993.

Wells, M. L., and E. D. Goldberg, The distribution of colloidsin the North Atlantic and Southern Oceans, Limnol. Ocean-ogr., 39, 286–302, 1994.

Wen, L.-S., M. C. Stordal, D. Tang, G. A. Gill, and P. H.Santschi, An ultraclean cross-flow ultrafiltration techniquefor the study of trace metal phase speciation in seawater,Mar. Chem., 55, 129–152, 1996a.

Wen, L.-S., P. H. Santschi, G. A. Gill, C. L. Paternostro, and

R. Lehma, Colloidal and particulate silver in river andestuarine waters of Texas, Environ. Sci. Technol., in press,1996b.

Wheeler, J. R., Fractionation of molecular weight of organicsubstances in Georgia coastal water, Limnol. Oceanogr., 21,846–852, 1976.

Whitehouse, B. G., R. W. Macdonald, K. Iseki, M. B. Yunker,and F. A. McLaughlin, Organic carbon and colloids in theMackenzie River and Beaufort Sea, Mar. Chem., 26, 371–378, 1989.

Whitehouse, B. G., P. A. Yeats, and P. M. Strain, Cross-flowfiltration of colloids from aquatic environments, Limnol.Oceanogr., 35, 1368–1375, 1990.

Williams, P. M., and E. R. M. Druffel, Radiocarbon in dis-solved organic matter in the central North Pacific Ocean,Nature, 330, 246–248, 1987.

Williams, P. M., K. J. Robertson, A. Soutar, S. M. Griffin, andE. R. M. Druffel, Isotopic signatures (14C, 13C, 15N) astracers of sources and cycling of soluble and particulateorganic matter in the Santa Monica Basin, California, Prog.Oceanogr., 30, 253–290, 1992.

Wu, J., and G. W. Luther, Size-fractionated iron concentrationin water column of the northwest Atlantic Ocean, Limnol.Oceanogr., 38, 1119–1129, 1994.

Zsolnay, A., Coastal colloidal carbon: A study of its seasonalvariation and the possibility of river input, Estuarine CoastalMar. Sci., 9, 559–567, 1979.

L. Guo and P. H. Santschi, Department of Oceanography,Laboratory for Oceanographic and Environmental Research,Texas A&M University, 5007 Avenue U, Galveston, TX 77551.

40 ● Guo and Santschi: CYCLING OF MARINE COLLOIDS 35, 1 / REVIEWS OF GEOPHYSICS