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  • matiodiv

    dystrophic, which can be translated as defectively

    The concentration of humic matter in lake water is

    tter). Such lakes have low biomass and produc-n of phytoplankton as well as low biomass andersity of benthic fauna. These are characteristics

    usually assessed by measuring the absorbance of thewater (commonly at around 430 nm), or by com-paring the color of the lake water sample with asurrounding watershed (i.e., allochthonous organic

    centration of dissolved organic substances from the

    Occurrence of Humic WatersDystrophyL J Tranvik, Uppsala University, Uppsala, Sweden

    2009 Elsevier Inc. All rights reserved.

    Introduction and Historical Outlook

    Dystrophy refers to the limnological conditions ofwater in lacustrine and riverine systems with highconcentrations of colored dissolved organic matterderived from the watershed, giving the water a yellowor brown color. Because of the dark appearance whenviewed from the surface, dystrophic waters some-times are referred to as blackwater lakes and rivers.The colored organic matter of external origin(allochthonous) is largely composed of humic sub-stances (humic and fulvic acids), in contrast to theorganic matter derived from the indigenous (autoch-thonous) primary production of the aquatic system.The development of classification schemes for lakes

    was an important theme for limnologists throughoutmuch of the twentieth century. Dystrophic lakes wereearly recognized as a special case, particularly whenlakes were classified according to their productivity,and received considerable attention from some ofthe most influential of the early limnologists. EinarNaumann described this lake type from the borealforest region of southern Sweden in several publica-tions around 1920. August Thienemann originallycoined the term dystrophic in a publication from1921, and further discussed it in Die BinnengewasserMitteleuropas (Inland Waters of Central Europe) in1925. Thus, the dystrophic lake type stood separatelyfrom the eutrophic (nutrient rich) and oligotrophic(nutrient poor) lake types. Although Thienemannpointed out early that there may be gradients betweenall normal or ideal lakes described in his lake typol-ogy, limnologists still often treat dystrophic lakes as aspecial case peripheral to the major pattern of lakesbeing distributed along a continuum from oligotro-phy to eutrophy. However, as will be demonstratedlater, dystrophy can be regarded a common and gen-eral feature of inland waters. Lakes with little, inter-mediate, or large influence from terrestrially derivedhumic substances can be denoted as oligo-, meso-,and polyhumic.Important characteristics of the dystrophic lake

    type, as identified by the earliest investigators, includebrown to yellow water color caused by a high con-nourished. The conventional view of the primaryproduction of the phytoplankton as the critical stepof energy mobilization into the food web is in accor-dance with the perception of these lakes as poorhabitats. Other characteristics of dystrophic lakes,identified already by Naumann and Thienemann,include low oxygen concentrations (in particular inthe hypolimnion during stratification), due to bacte-rial degradation of imported organic carbon, andhigh zooplankton production. The low oxygen con-centration is very typical of dystrophic lakes, whilehigh zooplankton production has not been unequivo-cally supported in later studies of specific lakes.These traits indicate substantial microbial meta-

    bolism, as well as a considerable resource base forzooplankton. The possible significance of the alloch-thonous organic carbon for the production of thedystrophic lakes led G. E. Hutchinson, in the secondvolume of ATreatise on Limnology (1967), to specu-late that the term dystrophic suggests a more patho-logical condition than perhaps exists.Limnological research during the last decades dem-

    onstrate that dystrophic lakes are sites of intensemineralization (decomposition) of organic matterwhere allochthonous organic matter constitutes a ter-restrial subsidy to the aquatic food web. Although theterm dystrophy is unfortunate, it is established inthe limnological literature and also among research-ers who are aware of the substantial flow of energyoccurring in these lakes. A useful alternative to dys-trophic is humic, which characterizes the chemistryof the water with no implications regarding biologicalconditions. The sediments of dystrophic lakes aredominated by organic matter with a prevalence ofhumic particles originating from terrestrial sources(dy). The term dystrophic can be more easily accom-modated with our current understanding of theselakes if associated with dy, rather than with defectivenourishment.of low productivity, a plausible reason for the term405

  • color scale, such as the platinum units (expressed asmg Pt l1), through the use of a solution containing abrown platinum salt. The two measurements corre-late closely, and they also correlate with the totalconcentration of dissolved organic carbon (DOC) inthe water, at least where the DOC concentration oflakes is under strong control from the watershed(Figure 1). They can thus be used interchangeably asindicators of dystrophic conditions. The ratio of colorto the amount of organic carbon reflects the relativeimportance of humic substances in the pool of totaldissolved organic carbon (organic compounds otherthan humic substances are not typically colored).The DOC concentration of lakes ranges from less

    than 1mg l1 in ultraoligotrophic lakes at high alti-tudes and high latitudes to several 100mg l1 but thedistribution is highly skewed towards lower values.Only few lakes have concentrations above about30mg l1. In a global analysis of dissolved organiccarbon (DOC) in 7500 lakes, the median concentra-tion of DOC was close to 6mg l1, a concentration atwhich the brown color of the water is often visible.Assuming that the surveyed lakes are representative

    ern boreal zone is rich in dystrophic lakes. In particu-lar, flat topography favors accumulation of organic

    406 Biological Integration _ Dystrophyof lakes on earth, a globally typical lake has weakbut detectable dystrophic traits. In a recent nationalanalysis of about 3000 lakes in Sweden, the averageDOC concentration was 11mg l1, and a survey ofabout 1000 Finnish lakes in 1987 showed a medianconcentration of 12mg l1. These are concentrationsat which the water is markedly brown, and theecological conditions typical for dystrophic lakes pre-vail. The classical dystrophic lakes of Fennoscandia

    0

    1

    2

    Abso

    rban

    ce42

    0nm

    , 5c

    m

    Total organic carbon, mg C liter 10 20 40 60 80

    Figure 1 The concentration of total organic carbon (TOC) andhumic color, measured as absorbance at 420 nm, in the water ofabout 2800 Swedish lakes (from http://info1.ma.slu.se/db.html).

    The concentration of organic carbon in the water is correlated to

    the concentration of humic, colored organic substances. The

    relationship reflects that terrestrially derived humic substancesare a major component of the organic carbon in lake water.layers and peat, because of thicker soil layers andhigher extent of water-logged soils. This explains theabundance of humic lakes in some northern borealforest regions, e.g., Finland and Sweden. Also in trop-ical climates, the concentration of humic matter insurface waters may be high, as exemplified by theAmazon basin, which has some lakes and rivers(blackwater rivers), such as Rio Negro, highlystained by humic substances.

    Chemical Effects of Humic Substancesin Lake Water

    Humic substances are complex mixtures of heteroge-neous organic compounds of biotic origin that haveundergone extensive transformations since they werefirst produced by plants. Lignin is probably an impor-tant precursor, and based on solubility, humic sub-stances can be classified into humic acids (insolublebelow pH 2), fulvic acids (soluble at any pH), andhumin (insoluble in water). Because of the complexityand irregularity of humic substances, and of the path-ways of their formation, they should not be consid-ered as strictly defined molecules, but can rather becharacterized by average properties. Among the mostimportant of these properties are (1) prevalence ofaromatic structures, which absorb light, induce avariety of photochemical reactions, and are involvedin adsorption and aggregation; and (2) presence ofionic structures, including carboxylic and phenolicgroups, which affect solubility of humic matter, andare acidic, and have low buffering capacity and a lowcontent of inorganic ions. This is probably a commonfeature of dystrophic waters worldwide, but not aprerequisite. There are also examples of dystrophiclakes with high concentrations of inorganic dissolvedsolids, e.g., in calcareous watersheds.The global data on lakes mentioned reveals that

    properties of the drainage area (watershed) of lakesare important regulators of DOC concentration in thelake water. Thus, high amount of soil carbon andratio of carbon to nitrogen in soils are positivelycorrelated to DOC in lakes. In the Arctic, permafrostand barren watersheds limit the export of DOC fromsoils, but large areas with extensive peat layers harborhighly humic lakes and ponds.In cold and temperate climates, soils and wetlands

    accumulate large amounts of organic matter, becauseof high input of detritus from the vegetation in com-bination with relatively slow microbial degradation.These habitats are an important source of DOC in thesurface waters. Accordingly, the circumpolar north-

  • light at short wavelengths affects the underwater

    with the high concentration of organic matter suscep-tible to bacterial degradation and concomitant con-

    biopolymers such as carbohydrates, the overalldegradability of dissolved organic matter in lakewater appears to be weakly coupled to the relativecontribution of humic matter to the total dissolvedorganic matter. About 10% of the dissolved organicmatter is degradable by bacteria in bioassay experi-ments lasting about one week, regardless of the rela-tive contribution of humic substances. Accordingly,the high concentration of dissolved organic carbon inhumic waters is a source of energy for bacteria.Shortly after the first use of epifluorescence micros-

    copy to count bacteria in samples taken from lakes,cross-system comparisons of lakes demonstrated apositive correlation between the color and the bacte-rial abundance of lake water. It was suggested that thehigher bacterial abundance in humic lakes was due to

    Biological Integration _ Dystrophy 407light climate; light of long wavelength (orange, red)penetrates more deeply than light of shorter wave-length (violet, blue), than would be the case in lakeswith low concentrations of dissolved humic matter.The rapid attenuation of light in the water column ofdystrophic lakes may lead to decreased primary pro-duction, when compared with corresponding lakeswith lower concentrations of humic substances. Onthe other hand, since the incoming solar radiation isefficiently absorbed in the upper layers of the watercolumn of a dystrophic lake, the surface water warmsup rapidly and a stable stratification may be formedwith a shallower epilimnion than would be formed inan oligohumic lake, in particular in small, shelteredhumic lakes (Figure 2). A shallow epilimnion maycreate a favorable light climate for algae in theupper mixed layer. Also, flagellated algae that canuse locomotion to actively stay in the photic zone(in particular chrysophytes and cryptophytes) arecharacteristic of humic lakes.The strong thermal stratification of dystrophic

    lakes creates an effective barrier against movementcause complexation of metals and other substances.Humic substances are weak buffers, which take overfrom the carbonate system between pH 4 and 5.Hence, dystrophic waters typically are naturallyacidic, but less sensitive to anthropogenic acidifica-tion than oligohumic waters.The complexation properties of humic substances

    are important in several ways. Binding of persistenthydrophobic organic contaminants to humic sub-stances decreases their bioavailability, and thus theirtoxicity. Chelation of toxic metals (e.g., copper)greatly reduces their toxicity. Chelating by humiccompounds can also enhance the availability of ironto phytoplankton by preventing the iron from preci-pitating as iron oxides or it being adsorbed on particlesurfaces, which would make it unavailable for uptakeby phytoplankton. At high concentrations of dis-solved humic matter, however, overchelation mayoccur, hampering bioavailability of metals. Likewise,free phosphate can become immobilized by humicsubstances and thereby become unavailable tophytoplankton.

    Light, Thermal Stratification, andPhytoplankton

    A striking characteristic of dystrophic lakes is theirbrown water color, which reduces light penetration.The dissolved humic substances not only absorbstrongly the UV-B and UV-A, but also compete withphytoplankton for the photosynthetically availablelight (400700 nm). The selective attenuation ofsumption of oxygen, the strong stratification ofdystrophic lakes frequently results in oxygen deple-tion in the hypolimnion and sediments, both duringsummer stratification and winter stratification.

    Bacterioplankton and Food WebStructure

    Humic substances are traditionally regarded highlyresistant to biological degradation, which impliesthat they can reside in the environment for longperiods of time. Although they are clearly more re-calcitrant than monomers (e.g., glucose) or simpleof nutrients and gases from deeper layers. Thus, keynutrients (N, P) may become scarce in the epilimnion.Flagellated algae (e.g., Cryptomonas) may circumventnutrient scarcity in the epilimnion by crossing the ther-mocline during diel migration, which allows them toretrieve nutrients in the hypolimnion at night, and tophotosynthesize in the epilimnion during the day. Also,

    Dep

    th

    Dystrophic lake Clearwater lake

    Light Temperature

    Figure 2 Light penetration and thermal stratification indystrophic and clear, nondystrophic waters. The colored water of

    dystrophic lakes attenuates incident radiation more strongly thanthe water of clear lakes, resulting in rapid heat accumulation near

    the lake surface and a more stable and shallower thermal

    stratification, when compared with clearwater lakes.

  • matter. This was an extension of the previous view

    sedimentwater interface. The sediment is dominatedby humic colloids derived from terrestrial vegetation,with only limited contribution from autochthonousorganic matter. Rates of microbial metabolism in the

    Phytoplankton

    Bacterioplankton Protozooplankton

    Metazooplankton Fish

    Metazooplankton Fish

    DOC

    Bacterioplankton Protozooplankton

    Bacterioplankton Protozooplankton

    DOCPhytoplankton

    Methanotrophs

    CH4Methanogens

    Oxic water

    Anoxic water

    (a)

    (b)

    (c)Figure 3 Schematic view of energy transfer in lacustrine foodwebs (a) with no dissolved organic carbon (DOC) subsidy from the

    watershed, and (b) with substantial DOC originating from the

    watershed andusedbybacteria (dystrophic lake). In thedystrophic

    lake, energy and carbon fromDOCare transferred up the foodwebvia bacteria consumed by protozoan (flagellates, ciliates) and

    metazoan (cladocerans, copepods, rotifers) zooplanktons. The

    terrestrial subsidy in the dystrophic lake enhances the transfer ofenergy to heterotrophic organisms, as indicated by bold arrows. In

    anoxic waters and sediments, methane is an important end

    product organic matter that is metabolized by bacteria. When the

    methane reaches oxygenated water it is oxidized bymethanotrophic bacteria,which in turnare prey for consumers. The

    oxic/anoxic interface may be in the upper sediment or in the water

    column, and the methanotrophs may accordingly be fed upon

    either by benthic invertebrates or by zooplankton.

    408 Biological Integration _ Dystrophythat bacterioplankton are primarily a componentwithin a closed microbial loop, utilizing organic mat-ter released from phytoplankton and directing it intothe food chain via organisms that feed on the bacteria(Figure 3(a)). By using allochthonous organic matter,aquatic bacteria constitute a link between terres-trial primary production and aquatic food webs(Figure 3(b)).The presence of a substantial carbon source for

    the heterotrophic bacteria independent of the autoch-thonous primary production relieves the bacteriafrom complete dependence on phytoplankton. Hence,the bacteria are able to compete more strongly withalgae for limiting nutrients than they would in lakeswhere they depend entirely on the phytoplankton.Considering that the affinity for the nutrients ishigher in bacteria than in algae, the bacteria are in afavorable position in this competition. Some phy-toplankters can bypass the competition for nutrientsby mixotrophy. Mixotrophic algae are able to photo-synthesize as well as feed on organic particles, such asbacteria. In this way, they can obtain inorganic nutri-ents via ingestion of bacteria. Mixotrophy could be asuccessful algal strategy in dystrophic lakes becauseit allows the algae to thrive under low light condi-tions by feeding on bacteria, and to offset nutrientdepletion by using bacterial nutrients. Furthermore,algae are able to store excess phosphorus, whichallows them to grow during periods when they wouldotherwise be outcompeted by bacteria.The allochthonous organic carbon that enters the

    food web via bacteria can continue up the food webeither through ingestion by crustacean zooplankton,or through zooplankton predation on flagellates andother protozoa that eat bacteria. Several studies dem-onstrate that the production at higher trophic levels indystrophic lakes is not adequately sustained by algalproduction, implying that allochthonous organic car-bon is of importance. Recent experiments haveshown that zooplankton (Daphnia) received up tohalf of its carbon biomass from sources other thanthe algal production in a lake, probably from allo-chthonous organic matter.

    Sediments and Hypolimnetic Processesin Dystrophic Lakes

    Sediments of dystrophic lakes are rich in humicflocs, have the consistency of a gel, and a diffusebacterial utilization of allochthonous organic carbon.Experimental tests of the carrying capacity for het-erotrophic bacterial biomass in water from lakes ofdifferent humic content corroborated the idea thatwater column bacteria use allochthonous organicDOC Phytoplankton Metazooplankton Fish

  • In dystrophic lakes, heterotrophic bacteria are sus-

    Photochemical Transformations of

    Biological Integration _ Dystrophy 409tained not only by indigenous primary productionbut also by allochthonous organic carbon. Conse-quently more carbon dioxide is produced during res-piration by heterotrophs than consumed duringprimary production by autotrophs, i.e., net heterotro-phy (predominance of respiration over photosynthe-sis) prevails). The growth efficiency of bacteria usingnatural dissolved organic carbon is low (generally1020%). Hence, the fraction of the allochthonousorganic carbon that is passed up the food web viabacteria, as described above, is minor compared tothe fraction that is respired and released by bacteriaas carbon dioxide.The mineralization (decomposition) of allochtho-

    nous organic matter results in supersaturation oflake water with carbon dioxide, causing a net flowof carbon dioxide from the lake surface to the atmo-sphere. There is a positive relationship between netheterotrophy and the content of humic matter inlakes, which extends to a correlation between contentof humic matter and loss of carbon dioxide to theatmosphere. Most lakes on the global scale appear tobe net sources of atmospheric carbon dioxide. Thus,lakes commonly show some of the traits that areespecially pronounced in dystrophic lakes.sediment appear to be low, because of the recalcitrantnature of the organic matter and frequently anoxicconditions. Considering the rapid oxygen depletion inthe hypolimnion of stratified dystrophic lakes, how-ever, the idea of dystrophic sediments as sites of slowmetabolism may be in error. In general, the benthicfauna is scarce in the deep water sediments of dystro-phic lakes because of frequent anoxic conditionsand possibly also because the highly hydrated gel-like substratum gives limited physical support formacroinvertebrates.The high rates of bacterial mineralization in dystro-

    phic lakes along with strong thermal stratificationoften results in an anoxic hypolimnion and sediments.In these cases anaerobic degradation of organicmatterproduces reduced chemical forms including methane,which is transported to the atmosphere via ebullition(bubbling) and diffusion. Some of the methane is usedby methanotrophic bacteria when it reaches oxy-genated layers, either in surface sediments or in thewater column. These bacteria are a resource for bac-terivorous organisms, and it has been shown thatbenthic invertebrates (chironomids) as well as zoo-plankton may derive some of their carbon frommethanotrophic bacteria (Figure 3(c)).

    Net Heterotrophy and the Role ofDystrophic Lakes in Carbon CyclingDissolved Organic Matter

    Humic substances absorb strongly the UV and shortwavelength range of visible light. This absorption pat-tern provides protection against damage caused bysolar UV radiation for organisms living in humicwaters. In addition, energy from photons of shortwavelength causes chemical reactions directly in theabsorbing molecule, and the formation of reactivechemical species (e.g., hydroxyl radicals and superox-ide ions) can indirectly induce chemical reactions inorganic molecules, including those that do not absorblight. The photochemically induced reactions cause theloss (bleaching) of colored organic matter andthe complete oxidation of some of the organic matterinto carbon dioxide and accompanying consumptionof molecular oxygen. In addition humic matter isdegraded into a range of smaller organic moleculesthat are available to heterotrophic bacteria. Thus, pho-tochemical transformation of humic substances hasbeen shown to enhance the growth of bacteria. Attimes, these compounds can provide a substantialshare of the organic substrates utilized by heterotrophicbacteria in the epilimnion. Photochemistry thus play arole in the degradation of humicmatter, and at the sametime stimulates the mobilization of energy from humicmatter via bacteria into the aquatic food web.A high concentration of colored dissolved organicmatter in lake water is promoted by import of dis-solved humic substances from the watershed, butcounteracted by degradation of these substances inthe lake. Hence, in lakes with short hydraulic reten-tion time (less than a year), a substantial fraction ofthe imported colored organic matter remains in thewater column, while the water of lakes with longretention times (several years or more) usually is atmost moderately humic. Accordingly, aquatic humicsubstances are subject to loss processes, includingbiological and chemical degradation and aggregationinto particles that leave the water column by sedi-mentation. In the drainage area of 21major riverin Scandinavia covering 316 000km2 and includingabout 80 000 lakes, the calculated loss of dissolvedorganic carbon from the lakes, primarily as minerali-zation and carbon dioxide loss to the atmosphere,was similar to the total transport of organic carbonto the sea via rivers. Only a minor fraction of theorganic matter was of autochthonous origin in thislarge boreal area. Hence, about half of the dissolvedorganic matter carbon that entered the surface waterswas lost before the water reached the sea, and thefraction lost was positively related to the hydraulicretention time of the individual river systems.

  • Concluding Remarks

    Dystrophic waters are characterized by high concen-trations of colored dissolved organic matter (humicsubstances) that originate from the watershed. Thehumic substances attenuate light in the water column,thereby limiting the depth distribution of photosyn-thesis in the water column of the pelagic zone and thedepth distribution of aquatic plants in the littoralzone. Early limnologists perceived humic substancesprimarily as a constraint on the overall productivity

    system of study, e.g., phytoplankton and littoralaquatic plants in a lake. Autochthonous dissolvedorganic carbon absorbs little light, and has lessaromatic structures than allochthonous organicmatter.

    410 Biological Integration _ Dystrophyof lakes, and coined the term dystrophy, which sug-gests defective nourishment. Later research hasshown that the externally derived (allochthonous)dissolved organic matter is a substantial subsidy tolake biota, via its utilization by heterotrophic bacte-ria. In addition to the transfer of carbon up theaquatic food web, the bacterial utilization ofallochthonous organic matter gives rise to extensiverespiration followed by evasion of carbon dioxidefrom lakes to the atmosphere. These patterns wereidentified early in dystrophic lakes. It has laterbecome evident that most lakes on the global scaleare net sources of atmospheric carbon dioxide, andthat net heterotrophy sustained by allochthonousDOC is a likely major cause. Hence, patterns origi-nally considered specific to dystrophic lakes appear tobe ubiquitous phenomena. The term dystrophyshould be reserved for waters that are highly stainedby dissolved humic substances, even though net het-erotrophy caused by metabolism of allochthonousDOC occurs widely in lakes with only modestamounts of humic substances.

    Glossary

    Allochthonous organic carbon Organic carbon thathas its origin outside the system of study, e.g., ori-ginating from terrestrial primary producers in thewatershed of a lake. The dissolved colored organicmatter (humic substances) of lake water comprisesa large fraction of allochthonous organic carbon.

    Autochthonous organic carbon Organic carbon thatoriginates from primary production within theFurther Reading

    Findlay SEG and Sinsabaugh RL (eds.) (2003) Aquatic Ecosystems:Interactivity of Dissolved Organic Matter. Amsterdam: Academ-ic Press.

    Hessen DO and Tranvik LJ (eds.) (1998) Aquatic Humic Sub-stances: Ecology and Biogeochemistry. Berlin: Springer.

    Keskitalo J and Eloranta P (eds.) (1999) Limnology of HumicWaters. Leiden: Backhuys Publishers.

    Salonen K, Kairesalo T, and Jones RI (eds.) (1992) Dissolved or-

    ganic matter in lacustrine ecosystems: Energy source and system

    regulator. Developments in Hydrobiology, vol. 73. Dordrecht:Kluwer Academic Publishers.

    Sobek S, Tranvik LJ, Prairie YT, Kortelainen P, and Cole JJ (2007)

    Patterns and regulation of dissolved organic carbon: An analysis

    of 7,500 widely distributed lakes. Limnology andOceanography52: 12081219.

    Steinberg CEW (2003) Ecology of Humic Substances in Fresh-waters. Berlin: Springer.Mixotrophy In the case of phytoplankton, the termrefers to the ability to obtain energy not only byprimary production, but also by ingestion of bacte-ria and other organic particles. Flagellated algae,and primarily the division Chrysophyceae, com-monly have this ability.

    Net heterotrophy An ecosystem energy budget forwhich the amount of organic carbon oxidized byrespiration to make inorganic carbon is higher thanthe amount of autotrophy (removal of inorganiccarbon during the formation of organic carbon byprimary production). In dystrophic lakes, net hetero-trophy is largely explained by bacterial decomposi-tion of substantial amounts of externally derived(allochthonous) organic carbon, in addition to theorganic carbon provided by lacustrine primaryproducers.

    See also: Carbon, Unifying Currency; Color of AquaticEcosystems; Ultraviolet Light.

    DystrophyIntroduction and Historical OutlookOccurrence of Humic WatersChemical Effects of Humic Substances in Lake WaterLight, Thermal Stratification, and PhytoplanktonBacterioplankton and Food Web StructureSediments and Hypolimnetic Processes in Dystrophic LakesNet Heterotrophy and the Role of Dystrophic Lakes in Carbon CyclingPhotochemical Transformations of Dissolved Organic MatterConcluding RemarksGlossaryFurther Reading