TurbidityJ U Grobbelaar, University of the Free State, Bloemfontein, South Africa

ã 2009 Elsevier Inc. All rights reserved.

Introduction

In general terms, turbidity is a reduction in waterclarity because of the presence of suspended matterabsorbing or scattering downwelling light. However,all natural waters have suspended matter, but they areconsidered turbid only when the suspensoids or trip-ton (turbid materials) become visibly conspicuous(Table 1). Chandler (1942) already concluded thatturbidity and its variations may influence (1) thecomposition, size, and time of phytoplankton pulses,(2) the rate of photosynthesis at various depths,(3) position of the compensation point for macro-phytes and phytoplankton, (4) vertical distributionof the zooplankton, and (5) magnitude of commercialfish catches.In lentic waters, the sources of suspensoids could be

from either one or a combination of the followingfour sources: (1) internal production associated withprecipitation and the presence of oversaturated min-eral phases (e.g., whiting due to CaCO3 precipita-tion), (2) terrestrial inputs from fluvial erosion andinflows, (3) resuspension from deposited materials,and (4) atmospheric fallout, especially in arid andsemiarid regions (dust storms). As will be seen, theseinorganic particles not only influence light penetra-tion but they also form adsorption and desorptionsites for a variety of materials, including nutrients,dissolved organic matter (DOM), bacteria, and algae.

Fate of Light Energy Crossingthe Air–Water Interface

Refraction, due to light energy that passes through anair–water interface or because of different velocitiesin the different media, results in the light beam beingbent towards the vertical (Figure 1(a)). Turbidity,temperature, and salinity affect the degree of refrac-tion. It should also be noted that when a light beammoves from the water to the air, the angle will moveaway from the vertical (Figure 1(b)). The only differ-ence between the latter and light penetrating thewater surface is that when yw is >49�, all the lightwill be reflected back into the water.Disturbance of the water surface has a marked

influence on reflectance the closer the light beam isto vertical. For example, about 70% of vertical lightare reflected at a wind speed of 16m s�1. At lowersolar elevations, reflectance is actually lowered by the

waves than by smooth waters, due to an increase inthe angle between the light direction and the point ofpenetration.

Since a photon is a discrete packet of energy, there isa remote chance that it will be absorbed when it inter-acts with a molecule. The energy of the molecule mustincrease by an amount equal to the energy of the pho-ton. Photons within the visible range of the spectrumhave enough energy to cause a transition from oneelectronic energy level (e.g., the ground state) toanother higher level (an exited state). If the moleculeis chlorophyll a, we know that 8–10photons will pro-vide sufficient energy to cause the splitting of onewatermolecule with the production of oneO2. In the contextof primary production, it is therefore meaningful toexpress irradiance in photons per square meter persecond (previously as quanta m�2 s�1).

There is no rigorous definition of absorption orabsorbance (D), but it is commonly presented as ineqn [1]:

D ¼ log 10

I0I

½1�

where I0 is the light energy impinging on the surface ofan absorbing medium and I the light that is transmit-ted from the medium. In an aquatic system, this couldmean the light intensity at the surface (I0) and the lightintensity at a certain depth (Iz). The quantification oflight attenuation by suspended inorganic materialsremains problematic because of analytical limitationsdue to the disconnection between particles and theiroptical properties. The absorption of light energy isfrom the water itself, gilvin, suspended inorganicmaterial, phytoplankton, and possibly, by zooplank-ton. Generally, pure water absorbs little light in thevisible range and only becomes significant above600 nm where the absorption coefficient (k) is0.245m�1 and at 700 nm it is 0.65m�1. Gilvin (yel-low substances including humic acids) is a vast arrayof organic molecules derived mainly from the decom-position of plant materials. These substances vary inmolecular weight of a few hundred up to millions.They absorb light weakly in the red region and itincreases exponentially below 500 nm.

In general, the tripton or inorganic suspensoids donot absorb much light energy, but mainly scatters it.The scattered light energy may be rescattered by otherinorganic particles or it could be absorbed by an algalcell, since phytoplankton can capture light fromany direction. In highly turbid waters, the angular

699

θa θaθa

θwθw θw

Air

Water

(b)(a)

Figure 1 Refraction as a light beam passes from the air

through the air–water interface into the water (a) and from the

water to the air (b). The symbols are as per eqn [2].

Table 1 Criteria for classifying a watertype turbid due to

suspended inorganic materials

Attenuationcoefficient (m�1)

Secchi depth (m) Euphoticdepth 1% (m)

2.3 to >90 �2 �2.5

700 Light and Heat in Aquatic Ecosystems _ Turbidity

structure of the underwater light fields is virtuallyindependent of the surface incident irradiation.Therefore, the underwater angular structure in suchwaters is determined by the ratio of scattering toabsorption. Suspended clay particles tend to cause aspectral shift towards red light.The absorption coefficient of suspended inorganic

particles (tripton) increases exponentially below atabout 550 nm and overlaps with gilvin. However,total turbidity is seldom expressed as an absorptioncoefficient but rather in nephelometric turbidity units(NTU, explained later). The phytoplankton mainlyabsorbs in the wavelengths where the various pig-ments, such as the chlorophylls, carotenoids, andbiliproteins, absorb light energy. For example, thechlorophylls have maxima above 600 nm and below500 nm, while the carotenoids mainly absorb wave-lengths below 500 nm. Total absorption, expressed asthe absorption (attenuation) coefficient (k), is usuallyascribed to water (kw), gilvin (kg), tripton (kt), andphytoplankton (kp), according to eqn [2]:

ktot ¼ kw þ kg þ kt þ kp ½2�where the attenuation coefficient (k) is calculatedfrom:

Iz ¼ I0ekz ½3�

where z is the depth or optical cross-section.As mentioned earlier, scattering does not absorb

light energy, but redirects the path resulting in a zig-zag pattern and consequently diminishes the verticalpenetration depth. In fact, scattering can result in theupward direction of photons generally referred toas back scattering. When considering scattering in

turbid waters, the scattering is due to particle interac-tion. For particles larger than a few wavelengths oflight, diffraction by geometrical optics can explainmost scattering because of the reflections and refrac-tion processes. A nephelometric turbidity meter is infact a fixed angle light scattering meter, where in mostcases the scattered light is measured at an angle of 90�

to the beam of excitation light. Turbidity is thenexpressed as NTU where the samples are referencedagainst an artificial standard.

Turbidity and scattering is caused by both inor-ganic suspensoids and phytoplankton, and althoughthe latter can scatter significant quantities of pho-tons, this article will mostly deal with the inorganicparticles.

Inorganic Suspensoids and theirElectrical Charge

Several generic particle types are used to typify sus-pended matter. These are clay minerals, iron-,manganese-, and silica-rich particles, quartz, diatoms,and ‘other’ particles. In general terms, clay mineralsdominate followed by quartz, diatoms, and the cat-ionic particles. Although the Secchi disc is commonlyused to measure water clarity, its usefulness to mea-sure light penetration in waters with high inorganicturbidity has been questioned. This is because of thepresence of many different absorbing and scatteringparticles in such waters.

The electrical charge of the inorganic suspensoidsform adsorption and desorption surfaces for anions,cations, and all other charged materials. Sediments asa source of nutrients are well known, especially as asource of P, both for phytoplankton and macro-phytes. For example, it was accepted that the watersof the Amazon River and its tributaries were of thenutrient poorest in the world and had at most onlytraces of PO4–P. Bioassays with algae isolated fromsuch waters or a standard bioassay alga, such asSelenastrum capricornutum, showed appreciablequantities of biologically available adsorbed nutri-ents. These could be as high as 10mg PO4–P100 g�1 and the available fraction is roughly approxi-mated by an alkaline extraction. Ca-bound P is gen-erally unavailable for algal growth.

Suspended sediments can also attract algae andwater clearing has already been ascribed to theiradhesion to clay particles. Addition of P to waterswith high inorganic turbidity results in decreasedturbidity, probably due to the formation of P–clayaggregates that settle out. Montmorillonite causeshigher turbidities than does kaolinite in waterswhere similar concentrations of these two clay types

Light and Heat in Aquatic Ecosystems _ Turbidity 701

are added. Therefore, net community productivity,chlorophyll a, and algal densities are the lowestwhen montmorillonite is the major clay present.However, the interaction between nutrient availabil-ity and light limitation in highly turbid waters iscomplex and several anomalies exists, includingN limitation, N þ P limitation, or no limitation atall, and the role of a deep mixed layer compared tothe photic zone.Montmorillonite and kaolinite also absorbs large

quantities of dissolved organic materials (DOM)(>30mg leaf leachates per g clay). This dissolvedorganic fraction is available to bacteria, indicatingthat such clay–organic aggregates are important inthe transportation of terrestrial organic materialsinto aquatic ecosystems.

Phytoplankton Productivity in Waterswith High Inorganic Turbidity

The importance of phytoplankton primary produc-tion in aquatic environments is undisputed, also thatof the littoral and epiphytic communities. However,an important consideration is that only a fraction ofthe available light is used for photosynthesis and thatthis depends on the phytoplankton present, inorganicturbidity, and any other light absorbing substances,such as gilvin. Inorganic turbidity essentially causes a

� rapid attenuation of light,� change in the spectral quality of the light, and� change in the ratio of the euphotic depth (Zeu) tothe mixing depth.

The attenuation of light is directly dependent onthe concentration of suspended inorganic particlesand extinction coefficients of >12m�1 are oftenreported. Ephotic depths of a few centimeters to afew meters are common in turbid waters. Since allnatural waters contain some turbidity, the followingcriteria (Table 1) are proposed, where turbidity ismostly derived from inorganic suspended particles,in order to be considered turbid.The rapid attenuation of light implies that the

euphotic zone becomes compressed with a real possi-bility of missing the point at which maximum photo-synthesis (Pmax) occurs whenmeasurements aremade.A flask used formeasuring primary production,with adiameter of 50mm, could span a light variance of50% and more depending on the actual attenuationin highly turbidwaters. Such an estimate would in factrepresent an integral and the construction of depthprofiles of primary production, and photosynthesisagainst light intensity (P/I) would be impossible.Several modifications have been made, including the

use of horizontal tubes incubated at 50-mm depthintervals or vertically suspended tubes with an innerdiameter of about 50mm spanning at least the eupho-tic zone. Such vertical tubes give an integrated rateand contains no information about the P/I responses.

Phytoplankton primary productivity follows thesame pattern in turbid waters as in clear waters,including surface inhibition,Pmax, exponential decreasebelow Pmax with an exponential decrease in irradiance,midday surface inhibition, diurnal variations, light,temperature, and nutrient influences. Noteworthy isthat there is little difference in volumetric rates ofprimary productivity, when clear water systems arecompared with turbid waters. The major difference isevident when integral primary productivity is com-pared, being generally lower in turbid waters than inclear ones. As stated earlier, the overriding consider-ation is the fact that inorganic suspended materialscompresses the euphotic zone. The consequence ofthis is small euphotic–aphotic ratios. The large aphoticzone compared with the small euphotic zone, togetherwith the mixing depth (Zm), determines the relativetime spent by the phytoplankton in the light and dark.This has two major consequences for the phytoplank-ton, i.e., the average light per phytoplankton celldecreases the smaller the Zeu/Zm ratio becomes, andthe longer the cells remain in die dark, the more pro-nounced losses due to dark respiration becomes. Thedecrease in primary production is because of a decreasein the average available light energy with increas-ing mixing depth. The increased mixing depths alsoinfluence nutrient supply and sinking rates where itdecreased with an increase in the mixing depths.

The concept of the ‘critical mixing depth’ was intro-duced in the 1950s, which in effect is a water column’scompensation point, where primary productionequals respiratory and other losses. This was identi-fied as probably the most important factor that influ-ences phytoplankton productivity in turbid systems,and critical Zeu/Zm ratios of about 0.05 have beendetermined. The critical mixing depth has been ques-tioned where it was observed that spring phytoplank-ton blooms developed before these waters stratified,such as in Norwegian fjords with depths exceeding200m. Recently, there has also been a suggestion thatturbulence interacts with the criticalmixing depth andwhen the turbulence is less than the critical turbu-lence, phytoplankton growth will be unaffected byvertical mixing rates. Under such conditions, bloomswill develop irrespective of the mixing depth.

If the ratio Zeu/Zm determines overall phytoplank-ton productivity, then the role of nutrient concentra-tions become secondary in such systems. A furthercomplication is that the smaller the Zeu/Zm ratiothe lesser is the average light availability per

702 Light and Heat in Aquatic Ecosystems _ Turbidity

phytoplankton cell. This leads to light acclimation,and the smaller the ratio the more dark-acclimated thecells will become. There are major physiological differ-ences between light- and dark-acclimated phytoplank-ton and they have developed several mechanisms tocope with changes in the quality and intensity of light.In essence, the aim of a plant is to balance and optimizethe light and dark photosynthetic reactions. The quan-tity of light harvesting pigments per cell increases underlight limiting conditions, implying an increase in thenumber of photosynthetic units and the size of the lightharvesting antennae. Also, a decrease in the accessorypigments, b-carotene and zeaxanthin, is seen underlight-limiting conditions, which is a characteristic oflow light-acclimated cells. The opposite is true forcells exposed to high light intensities. Such high light-acclimated cells typically have less photosyntheticunits, lower chlorophyll a, and high concentrations ofaccessory pigments. The time scales within which thealgal cells photoacclimate range from seconds to hours,depending on the parameters measured. Paradoxically,it appears as if the tendency is for algae to favor the lowlight-acclimated state, which is typical in highly turbidwaters. The implication of this is that algae can effi-ciently utilize low light intensities, but on the otherhand, they often have to deal with excess energy.Mostly, the excess energy is handled in PS II througheither state transitions or dissipation, and these happenwithin seconds to minutes. Structural and biochemicalchanges, on the other hand, require longer time scales.Results from turbid waters clearly show that the phy-toplankton become dark-acclimated as the water massbecomes more turbid. Also, the carbon fixing capacityin terms of chlorophyll a concentration increases withincreasing turbidity, as well as the light utilizationindex (LUI).Thus turbidity affects the capturing of impinging

light byphytoplankton and also alters the photobiologyof the algae. These findings need to be interpreted inview of the fact that inorganic suspended materialslimit light penetration, but as such mostly scatterslight, which extends the path length and increases theprobability that an algal cell might intercept it.

Phytoplankton Community Composition

Turbidity affects the phytoplankton composition andgenerally the number of phytoplankton taxa declinesas water bodies become more turbid. Major shifts inthe taxa also occur as waters become turbid; wherecyanobacteria often become dominant, the chloro-phytes decrease and the bacillariophytes are largelyunaffected. Combining nutrient enrichment with tur-bidity leads to cyanobacterial domination, especially

those (such as Anabaena, Microcystis, and Oscilla-toria species) that can regulate their buoyancy.Micro-cystis is particularly successful in highly turbid watersbecause of the gas vesicles that develop and increasestheir buoyancy. Dinoflaggelates are known to migratevertically during the diurnal cycle. This phototacticresponse essentially ensures that the organisms areexposed to optimal light conditions and it has beenshown in a few cases that turbid waters favor theselection for and domination of dinoflaggelates.

Clear succession trends are seen with changes inturbidity between submerged and floating macro-phytes, and phytoplankton. In general it can be statedthat submerged macrophytes and a diverse phyto-plankton community dominates clear waters, whilefloating macrophytes and cyanobacteria will domi-nate in turbid waters. Zooplankton grazing of thephytoplankton in clear waters and detritus in turbidwaters could impact on water clarity, which tends topromote growth of submerged macrophytes. Nutri-ent enrichment in most cases will lead to an eventualdomination of floating macrophytes.

Zooplankton Feeding and CommunityStructure

The influence of inorganic turbidity on zooplanktonabundance and community composition is open fordebate without any clear trend. In laboratory experi-ments, clays will reduce the efficiency of zooplanktonfeeding on algae, but the same effect has not beendemonstrated in nature. For example, Daphniaappears to be particularly sensitive to increased tur-bidity, while several other species show no influence.A possible explanation lies in the fact that claysabsorb organic materials that are available for zoo-plankton. The adsorbed carbon can be significant andin certain freshwaters it could be 10 times as much asthat which the zooplankton obtains from phyto-plankton. In fact, clays could be the sole source offood for cladocerans during periods of very high tur-bidity. Aggregates up to 65 mm in diameter oftenform, rendering them available for zooplankton. Ofsignificance is also the adsorption of bacteria to theclay particles and it has been shown that zooplanktoncan selectively graze on these adsorbed bacteria. Thebacteria also benefits from the adsorbed organicmaterials.

Accepting the fact that clays will influence feedingand that reference to zooplankton implies a diversegroup of organisms, it is to be expected that inorga-nic turbidity will also influence their communitystructure. Calanoid copepods and some cladoceransappear to better adapt to inorganic turbidity than do

Light and Heat in Aquatic Ecosystems _ Turbidity 703

crustaceans, and rotifers should replace cladocerans,possibly because of their ability to select algae fromclay particles. Also, rotifers selectively ingest algae,while cladocerans ingest both clay and algae.A consequence of this is that cladocerans are severelyaffected by suspended clay materials. Rotifers, there-fore, have a competitive advantage over cladoceransin turbid waters, explaining their dominance in suchwaters.Montmorillonite is much more potent than kaolo-

nite in reducing densities of crustaceans. The reasonfor this inhibiting affect of montmorillonite is openfor debate and it could be either its stronger adsorp-tion/desorption properties compared to kaolonite, orits negative affect on phytoplankton growth.

Turbidity, Fish, and Predation

Predator–prey interactions mostly rely on reactivedistances or energy spent versus energy gained. Reac-tive distance has been defined as the maximum dis-tance at which visual predators can detect their preyor the maximum distance of pursuit. In these complexinteractions, predator size, prey size, hunger, anddensities all determine strike and success rates, butthe presence of turbidity complicates all of these.Turbidity will reduce available light and the sus-pended particles will scatter light and it has beenshown that turbidity reduces predation and that it isunrelated to shading. Using human observers, it wasfound that the reactive distance is best described by apower function where it declined rapidly as the tur-bidity increased from low to moderate levels. Athigher turbidities, the reactive distances reachedasymptotic values. Noteworthy is that light intensityhad little impact on predation rates and on the reac-tive distances, while an increase in turbidity markedlyinfluences both.The overall influence of turbidity is reduced preda-

tion rates where the predator relies on visual locationof its prey, and consequently, a reduction in the fishpopulation with increased turbidity. High suspendedsediment loads also result in a decrease in size at firstmaturity and maximum size. Smothering throughblanketing may reduce the availability of benthicfood sources, and gillrakers and filaments maybecome clogged. However, at moderate turbidity,the growth and recruitment of fish larvae may bebenefited by providing additional protection againstpredation. Turbidity also has a marked impact on theareal distribution of fish and increased numbers arefound in the clearer littoral regions than in the pelagiczone. Fish also adapt to high turbidities, andGilchris-tella aestuarius have smaller eyes in turbid waters

than when they occur in clearer waters. The Africanclariid catfish Clarias gariepinus has an array of ana-tomical adaptation to survive in highly turbid waters,while the common carp Cyprinus carpio not onlyprefers turbid waters, but through their bottom feed-ing action they actually can transform a clear waterbody into a turbid one.

Applied Aspects of Increased InorganicTurbidity

The adsorption and desorption properties of sus-pended inorganic materials do have environmentalconsequences that could be beneficial. For example,zooplankton are sensitive bioindicators of environ-mental pollution and have been used in ecotoxicolog-ical studies. Turbidity mitigated lead toxicity tocladocerans of between 20% and 75%. As statedbefore, dissolved organic materials adsorb on sus-pended clay particles and form aggregates with bac-teria. In turn, these conglomerates form an importantsource of food for the zooplankton and eventuallysupport much higher fish yields than what could beproduced from the phytoplankton alone.

The presence of suspended inorganic materials alsoinfluences submerged macrophytes and there arestrong relationships between the composition anddensity of the aquatic vegetation and water transpar-ency. The presence of macrophytes is important forfish recruitment and preserving a high biodiversity.

Increased pollution and concentrations of inor-ganic suspensoids could react, mitigating the conse-quences of pollution. Gold-mining activities on theWest Coast of the South Island, New Zealand clearlyshowed the impact of increased clay loads on thewater quality, benthic primary production, and com-munity respiration rates of several streams. The opti-cal properties were severely influenced resulting in amarked reduction of the benthic primary productionas well as the quality of the epiphytic phytomass.Consequently, allochtonous inputs of organic materi-als from the catchments became an important sourceof organic materials. The fine clay particles that set-tled on the stream beds reduced the organic content ofthe epilithon and thus reduced the food quality for theinvertebrates. Macrophytes and periphyton normallyresponded first to an increase in inorganic turbidityand whole stream respiration finally decreases. Alter-ing the concentration of suspended inorganic matterin rivers usually result in a lag of 2–3 years before theresponses becomes evident.

Turbid waters require special treatment steps beforeit could be used for domestic purposes and it couldcause the clogging and compacting of soils when used

704 Light and Heat in Aquatic Ecosystems _ Turbidity

in agriculture because of the deposition of clays. Reser-voir capacities are adversely affected and sedimentationhas caused loss in storage capacity of impoundments inmany areas of theworld, especially in arid and semiaridzones. For example, the Welbedacht Dam, SouthAfrica, lost 38% of its storage capacity within the first3 years following completion.

Further Reading

Bruton MN (1985) The effects of suspensoids on fish. Hydro-biologia 125: 221–241.

Chandler DC (1942) Limnological studies of western Lake Erie: II.

Light penetration and its relation to turbidity. Ecology 23:41–52.

Cullen JJ and Lewis MR (1988) The kinetics of algal photoadapta-

tion in the context of vertical mixing. Journal of PlanktonResearch 10: 1039–1063.

Diehl S (2002) Phytoplankton, light, and nutrients in a gradient of

mixing depths: Theory. Ecology 83: 386–398.

Golterman HL (ed.) (1977) Interactions Between Sediments andFresh Water. The Hague: W. Junk B.V. Publishers.

Grobbelaar JU (1983) Availability to algae of N and P adsorbed on

suspended solids in turbid waters of the Amazon River. Archivfur Hydrobiologie 93: 302–316.

Grobbelaar JU (1985) Phytoplankton productivity in turbid waters.

Journal of Plankton Research 7: 653–663.

Grobbelaar JU (1992) Nutrients versus physical factors in deter-

mining the primary productivity of waters with high inorganicturbidity. Hydrobiologia 238: 177–182.

Jeppesen E, Jensen JP, S�ndergaard M, and Lauridsen T (1999)

Trophic dynamics in turbid and clearwater lakes with specialemphasis on the role of zooplankton for water clarity. Hydro-biologia 408/ 409: 217–231.

Kirk JTO (1994) Light and Photosynthesis in Aquatic Ecosystems,2nd edn. Cambridge: Cambridge University Press.

Kirk JTO (1994) Characteristic of the light field in highly turbid

waters: AMonte Carlo study. Limnology and Oceanography 39:702–706.

Lind OT and Davalos-Lind L (1991) Association of turbidity andorganic carbon with bacterial abundance and cell size in a large,

turbid, tropical lake. Limnology and Oceanography 36:

1200–1208.

Reynolds CS (1984) The Ecology of Freshwater Phytoplankton.Cambridge: Cambridge University Press.

Talling JF (1957) The phytoplankton population as a compound

photosynthetic system. New Phytologist 56: 133–149.Talling JF (1971) The underwater light climate as a controlling

factor in the production ecology of freshwater phytoplankton.

Mitteilungen Internationale Vereinigung fur Theoretische undAngewandte Limnologie 19: 214–243.

Van Nes EH, Scheffer M, van den Berg MS, and Coops H (2002)

Dominance of charophytes in eutrophic shallow lakes—When

should we expect it to be an alternative stable state? AquaticBotany 72: 275–296.

Relevant Website

http://dipin.kent.edu