Schindler 1978

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Limnol. Oceunoyr., 23(3), 1978, 47U-486@ 1978, by the American Society of Limnology and Oceanography, Inc.

Factors regulating phytoplankton production and

standing crop in the world’s freshwaters

D. W. SchindlerDepartment of Fisheries and the Environment, Freshwater Institute, 501 University Crescent,Winnipeg, Manitoba R3T 2N6

Abstract

A regression analysis of global data for freshwater phytoplankton production, chlorophyll,and various nutrient parameters revealed the following: A high proportion of the variance in

both annual phytoplankton production and mean annual chlorophyll could be explained by

annual phosphorus input (loading), once a simple correction for water renewal time was

applied. Good relationships were also found between phosphorus loading and mean totalphosphorus concentration, and between total phosphorus concentration and chlorophyll. The

slope of the regression of total phosphorus on phosphorus loading for stratified lakes was notsignificantly different from that for unstratified lakes, suggesting that the effect of stratificationon phosphorus concentration is insignificant compared to external sources of the element.

Nutrient input, which was unavailable in previous analyses, appears to be an important factorin controlling freshwater production. There is some evidence for a correlation between lati-tude and nutrient input, and it is possible that this may explain the good correlation between

latitude and production observed by earlier investigators.

In an earlier synthesis of IBP fresh-water primary production results, Brylin-sky and Mann (1973) and Brylinsky (inpress) concluded that variables related toenergy availability had a greater influ-ence on phytoplankton production than

those related to nutrient availability.They found that 57% of the variability inglobal primary production could be ex-plained by latitude alone. Brylinsky andMann, however, recognized the scarcityof good data for nutrient input to lakes inthe IBP data set. They suggested (p. 12)that some of the influence attributed toenergy might be due to its driving of cir-culation systems, so that nutrient avail-ability might be affected directly. Re-cently, more data on nutrients, including

input and output dynamics, have accu-mulated, chiefly as the result of investi-gations of the eutrophication of lakes.These data, plus our own experimentalstudies in lakes, suggested that nutrientsplayed a preeminent role in controllingphytoplankton production and standingcrop. Of all the variables which may con-trol aquatic production and standingcrop. only nutrients are amenable to con-trol by humans. It therefore seemedworthwhile to repeat Brylinsky andMann’s analysis, including this new in-formation (Schindler and Fee 1974).

The following analysis is highly biasedtoward glacial lakes in north temperateand subarctic regions, where most lim-nological activity has been concentrated.More complete data are sorely needed forwater bodies in tropical and arctic re-

gions, in the southern hemisphere, andin unglaciated areas before a definitiveglobal analysis of production and factorsaffecting it can be made.

Increases in the annual input of nu-trients (phosphorus in particular) havebeen found to cause corresponding in-creases in phytoplankton production andstanding crop, regardless of latitude (Vol-lenweider 1968, 1975, 1976; Vollenwei-der et al. 1974; Kalff and Welch 1974;Dillon 1975; Dillon and Rigler 1974;

Schindler 1976; Schindler et al. 1974).Indeed, the literature on eutrophicationincludes many high values for phyto-plankton production and standing crop atnorthern latitudes (Mathiesen 1971; Bin-dloss 1974; Ahlgren 1970; Wetzel 1966;Schindler and Comita 1972; Sakamoto1966; Barica 1975). The relationship be-tween nutrient supply and algal standingcrop and production has also been firmlyestablished by experimental studies inwhole lakes, at different latitudes (Schin-dler 1976; Schindler and Fee 1973; Pers-son et al. 1975).

478

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Freshwater phytoplankton production 479

Table 1. Comparison of maximum ranges of sites treated by Brylinsky and Mann (1973), Brylinsky (inpress), and this study. Data in columns 1 and 2 not given.in above papers wcrc supplied by Brylinsky(pers. comm.).

(2)Brylinsky(in mess)

(3)

PresentStudy

LatitudeArca, km2Mean depth, m

Production, kcal. rnp2* yr-’Water renewal time, year

0-75”N 10”N-7l”N 38”S-75”N

0.531,500 0.04-30,000 0.00283,3001.2-730 . 0.6-325 1.1-313

3&13,320 813,000 285,6000.01-130 0. l-l 18 0.09-247

E. Fee provided many discussions ofthis topic. M. Brylinsky and K. H. Mannprovided data from IBP lakes, as well as a

rigorous critique of the manuscript. K.Patalas also pointed out many flaws in theanalysis, some of which could be cor-rected. R. V. Schmidt and T. Ruszczynskicarried out the data analysis. Many sci-entific friends from around the world pro-vided unpublished data on their studies,for which I am grateful.

Methods

Data were gathered from severalsources, including the published litera-ture, manuscript reports, and personalcommunications from scientists involvedin the IBP, OECD-eutrophication, andother projects, and our own files. The fol-lowing data were tabulated: annual pro-duction per unit area by the 14C or lightbottle oxygen methods, annual mean con-centrations of chlorophyll and total phos-phorus, annual input of phosphorus andnitrogen, mean depth, and water resi-

dence times. Oxygen data were convert-ed to carbon by multiplying by 0.312.When data from such a variety of sources,collected by different methods and in-vestigators, are compared, large discrep-ancies are to be expected. Because all ofthe parameters studied spanned nearlythree orders of magnitude in total range,it was expected that even occasionallarge errors would not obscure relation-ships on the scale sought here. Net pro-

duction was used rather than gross, be-cause this is the value available forconsumption at higher trophic levels, andbecause results of the 14C method appear

to be closer to net than to gross produc-tion This seemed a more logical way ofcombining 14C and O2 light bottle results

than by using an unknown “fiddle factor”for relating respiration to 14C results. Re-cent analyses have shown that respirationin highly productive lakes is usually ahigh proportion of gross production be-cause the ratio mixing depth:depth of eu-photic zone is typically high in suchlakes. In many cases, respiration may be50% or more of gross production (e.g.Ganf and Home 1975). The proportionappears to vary greatly from lake to lake,

probably as a result of differences in mor-phometry, drainage basin characteristics,and types of consumer organisms, as wellas productivity differences, and thereseems to be no constant which could beused with validity to correct 14C data fromall sites. Relationships were tested byregression analysis, as in Brylinsky andMann’s studies.

Site description

The characteristics of sites analyzed indifferent IBP treatments are shown inTable 1. Our sites range from 38’S to75”N latitude, from 0.002 to 8.3 x lo4 km2in area, from 1.1 to 313 m in mean depth,and from 28 to 5,600 kcal * nw2* yr-’ in netproduction. At first glance, the data ana-lyzed in the different studies appear tobe similar. There are, however, severalimportant differences. I was unable toobtain nutrient data for most of the very

productive tropical sites treated by Bry-linsky, so that it was impossible to in-clude them. Only one tropical site, LakeGeorge, Uganda, had sufficient data

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480 Schindler

CAPRICORNmm-

EQUATOR

Fig. 1. Approximate locations of lakes and reservoirs in analysis. Numbers indicate several lakes insame locality.

available. On the other hand, I was able

to obtain more results from arctic regionsthan were used in the earlier summaries,plus data for one temperate site in thesouthern hemisphere (Fig. 1). The differ-ence in upper production values bc-twcen the analysts is probably not asgreat as it would first seem from Table 1.Brylinsky used gross production in hisanalysis, correcting 14C data for rcspira-tion by adding a constant proportion. Iused net production, defined as dis-

cussed above.

Results

Latitude and phytoplankton produc-tion-A correlation coefficient of only0.20 (not significant) was found betweennet production and latitude. To some ex-tent this is due to the abundance of datafrom productive north-tempcratc lakes,where studies of eutrophication are mostcommon, and the paucity of tropical lakes

with good data for nutrient input.Phosphorus and phytoplankton pro-

duction-one of the most popular in-dices of eutrophication has been annual

phosphorus input (Vollenweider 1968). If

production is truly a measure of eutro-phication, one would expect a good re-lationship between annual productionan d annual phosphorus input. Vollen-weider et al. (1974) found such a rela-tionship for the St. Lawrence GreatLakes. I did not find it for the lakes cx-amined here: the correlation coefficientof 0.23 was not significant.

In the treatment of lakes with drainagefrom the Precambrian Shield, Schindler

et al. (1978) found that two extremelysimple and logical equations could beused to relate phytoplankton standingcrop and production to phosphorus inputand water renewal. The first of these isthe steady state equation for a conserva-tivc clement:

C”,. = +,

0

where C*, is the steady state concentra-

tion of chemical (c) in the lake, I,. is theamount of chemical entering in a givenperiod, and V, is the outflow volume dur-ing the period. The second equation,

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-

ANNUAL PHOSPHORUSINPUT g/m2

20

15

BY WEIGHT

Fig. 2. Frequency distribution of nutrient loading for lakes studied.

c*c

= Mc + L (t>VL + v, (t)’

(2)

where M, is the mass of chemical in thelake at the beginning of the period, VL isthe lake volume, and t is the time periodunder examination, is a simple modifi-cation to incorporate lakes where nu-

trient inputs arc rapidly increased or re-duced. At steady state, the two equationsshould give equal results. Both equationsperformed well for Schindler et al.(1978). Both also worked very well here,but Eq. 2 clearly performed better, per-haps because of the fact that several lakeshad recently undergone rapid increasesor decreases in phosphorus input. For thesake of brevity I will therefore discussonly the results of Eq. 2.

Before using Eq. 2 to relate C*, (whereP is total phosphorus) and annual pro-duction, a second adjustment to the datawas made. One would not expect to find

a relationship between phosphorus andphytoplankton production when the ratioof nitrogen to phosphorus in input is ex-tremely low, i.e. where phosphorus is notthe limiting nutrient. Most algae seem torequire N:P at at least 1O:l by weight(Vallentyne I974), and a severe reductionin the ratio should cause the system to be

nitrogen limited. In a detailed study ofrelative nutrient requirements, Chian-dani and Vighi (1974) found phosphorusto be limiting at above 10: 1, nitrogen be-low 5:1, and a proportional relationshipin between these values. Schindler(1976, 1977) found that fixation of atmo-spheric N, would allow phosphorus-pro-portional development of phytoplanktonin lakes with ionic N:P ratios in input aslow as 5: 1. Only lakes with N:P ratios ininput greater than 5: 1 were therefore in-cluded in this analysis. The frequencydistributions of P loading and N:P ratiosencountered are given in Fig. 2.

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482 Schindler

OoL- ----- -- -2 3

LOG,, C*p

Fig. 3. Relationship between net primary pro-duction and C*p, as calculated from Eq. 1. Lakes

where N:P in input is <5: 1 are not included in anal-ysis. Correlation coefficient, T = 0.69, is highly sig-nificant. log PN = 0.83 log C*r + 0.56.

A linear regression of production onC*p explained a highly significant pro-portion of the variance (r = 0.59) but thiscould presumably be improved if moredata were available in the upper C*prange. Using a log-log plot improved thecorrelation to r = 0.65 (Fig. 3).

Inspection suggested that the relation-ship between production and C*p reachedsome upper limit, where production didnot increase as C*p got larger. This wouldbe expected logically: chlorophyll con-centrations in lakes with the highest C*pwere high enough to restrict severely thedepth of the eutrophic zone, so that lightshould have limited further increases inproduction, regardless of nutrient condi-tions. This apparent upper asymptote is

too roughly defined to treat in detail be-cause of the paucity of lakes with highC*p. It is also probable that the asymptoteof this relationship would be lower inlakes where light attenuation is causedlargely by tripton or dissolved material.Only further investigations in productivelakes can clarify this point.

Phosphorus and standing crop-Fromthe standpoint of managing eutrophica-tion, the concentration of the algal stand-ing crop supported is often of greater in-terest than the production. It thereforeseemed worthwhile to try to analyze nu-trient factors affecting standing crop di-

-T-----l 3

LOG,, C P, mg/m3

Fig. 4. Relationship between mean annual chlo-

rophyll concentration and mean annual concentra-tion of total phosphorus. Value for r (0.88) is highlysignificant. log [Chl] = 1.213 log [XP] - 0.848.

rectly, even though production andstanding crop must be related to somedegree.

Sakamoto (1966) and Dillon and Rigler(1974) have shown that the summer chlo-rophyll concentration of temperate lakesmay be predicted quite accurately fromthe concentration of total phosphorus(XP) at spring overturn. A similar treat-

ment was not possible for the lakes stud-ied here, because it was impossible toassign a “spring” value to tropical andarctic lakes. Instead, the relationship be-tween mean annual chlorophyll concen-tration and mean annual concentration oftotal phosphorus was examined (Fig. 4)and found to be as good as correlations inthe above-mentioned papers (r = 0.89).

In turn, our results show that the meanannual concentration of total phosphorus

could be quite accurately related to thephosphorus input corrected for water re-newal (r = 0.88, Fig. 5). In fact, when thechlorophyll-phosphorus relationship ofDillon and Rigler (1974), the PacificNorthwest Environmental Research Lab-oratory (1974), and this study are com-pared, there is no significant differencebetween them (Schindler 1976). This isof obvious interest to managers, becauseknowing either phosphorus input andwater renewal time or mean concentra-tion of P allows one to predict the meanphytoplankton standing crop quite accu-rately in the majority of cases, or, con-

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0 1 I I I0 I 2 3

LOG,, Cb

Fig. 5. Relationship between mean annual con-centration of total phosphorus and corrected annual

phosphorus input, C*p from Eq. 1. Correlation (T= 0.88) is highly significant. log [ZP] = 0.779 logC*p + 0.214.

versely if a certain reduction in standingcrop is desired, the necessary reductionin loading can be calculated and the fea-sibility of obtaining it by regulating phos-phorus input studied. Such a plan has re-

cently been suggested for lakes ofOntario by Dillon and Rigler (1975).Since there are good relationships be-

tween C*r and ZP, and between dP andchlorophyll, it follows that chlorophyllshould be predictable directly from C*r.This is shown in Fig. 6 (r = 0.76).

The effect of thermal stratification onphytopl&kto& production an-d standingcrop- Onelimnol

statement often debated byogists is whether shallow, holo-

mictic lakes are more nroductive than

stratified ones which circulate only pe-riodically (e.g. Richardson 1975). It wastherefore of interest to compare C*p vs.annual average 2P for stratified and un-stratified lakes. Presumably if “internalloading” (return from sediments) causedsignificantly more phosphorus to becomeavailable in the shallower lakes, theslope of EP on C *r would be greater thanfor deeper, stratified ones. The data weretherefore separated into a stratified and

an unstratified group and the regressionswere rerun. The difference detected(Fig. 7) was not significant, and we as-

I I I0 I 2 3

LOG,, Cb

Fig. 6. Relationship between C*p and mean an-nual chlorophyll concentration. Correlation (T =

0.76) is highly significant. log [Chl] = 0.968 log C*p- 0.620.

sume that for our purposes only externalloading of this element is of overwhelm-ing importance.

Nitrogen and primary production-Because we failed to ask contributors foraverage concentrations of total nitrogen,

it was impossible to calculate a C*N valuefor- water renewal-corrected nitrogenloading, as we did for phosphorus. Byusing the same rationale, i.e. by not in-cluding data where the N:P ratio inputwould render phosphorus limiting (> 10: 1according to Chiandani and Vighi 1974),we predict that good correlations be-tween production and nitrogen inputwould be found. Fewer data would, how-ever, be available, because many inves-tigators did not collect nitrogen input

data, and for many lakes the N:P ratio ex-ceeds the 1O:l critical value mentionedearlier.

Light and primary production-Thedifference in total annual light reachingChar Lake, the most northerly lake stud-ied here, and Lake George at the equator,was less than 50x, even when winterdarkness and attenuation by ice and snowwere accounted for. It therefore seemsunlikely that the much greater (1,000~)

range in production with latitude ob-served by Brylinsky was due to lightalone.

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484 Schindler

/UNSTRATIFIED ,’

O-W-----l I I

0 I 2 3LOG,, CT,

Fig. 7.*p into

Separation of regressions of total P onstratified and unstratified group. Lack of. - -

significant difference between slopes and asymp-

totes indicates that increased contact (and pre-sumed exchange) with sediments has little influ-ence on phosphorus concentration. O-Unstratified-lakes; O-stratified lakes.

The question then remains-why did

Brylinsky find a high correlation betweenproduction and latitude, if light is not ofprimary importance? A few scraps of evi-dence suggest a hypothesis which can besimply tested in a few years if the re-quired data are collected. When nutrientin rainfall is compared for the few siteswhere such data are available and wherecultural contamination is probably slight,there is a 100x increase in nutrient influxfrom polar regions to the equator (Schin-

dler and Fee 1974). Due to increasedamounts of precipitation, higher runoff,more organic and inorganic acids, morediverse and efficient communities of soildecomposers, longer period when soilsare not frozen, and higher temperature,one might also expect the nutrient inflowvia runoff and streamflow to be higher atmore equatorial latitudes. Latitude andinput of nutrients could therefore be cor-related, as well as latitude and light.

Data collected and analyzed from alarge number of sites would be neededto rigorously test the above hypothesis,due to geological, geographical, and cul-

tural factors. If controlling world aquaticproductivity is seriously contemplated,such a study must be undertaken. S.Oddn and T. Ah1 (pers. comm.) showed

that input of nutrients to north-temperateregions of Europe via precipitation is in-creasing rapidly due to the effects of in-dustry and agriculture. Outside Europe,such data are scarce and not usually col-lected and analyzed in comparable fash-ion.

Tailing (1975) doubts that the accuracyof any net production measurement isbetter than 250%. Measurement of nu-trient input is probably subject to even

larger errors, because many lakes havediffuse nutrient sources that are nearlyimpossible to estimate. The relationshipsfound here were possible only becausethe data treated embraced a range of 100to 1,000~ so that even quite large errorswould not obscure relationships if theyexisted.

When all data used arc obtained bysimilar methods, and when a relativelynarrow range of production and nutrientinput values are compared, the abovemethods give much more precise results(Schindler et al. 1978). A global standard-ization of methodology would probablyallow better interpretation to be made.

Discussion

It is obvious that work on lake produc-tivity and on eutrophication is really in-separable-the only difference is in theemphasis on the fate of the photosyn-

thesized material. Two variables, phos-phorus input and water renewal time,which have recently become central tointerpreting eutrophication problems,appear to serve equally well for inter-prcting production results and are thekey to managing a wide variety of aquaticproductivity problems.

It may not be a geochemical accidentthat production and standing crop in themajority of the world’s lakes are predict-able from phosphorus-based models,

even when ratios of C and N to P in inputare lower than those apparently favoredby plankton. Input calculations almost

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never take into account Nt fixation byboth phytoplankton and periphyton. At-mospheric contributions of CO2 can bequite large. Furthermore, once sedimen-

tation and outflow are subtracted from in-put, it is almost invariably found that ahigher proportion of incoming nitrogenthan of incoming phosphorus is retainedin the water column of the lake. Thesefactors appear to allow lakes to correctdeficiencies of nitrogen and carbon to thepoint where standing crop is proportionalto phosphorus (Schindler 1976, 1977;Persson et al. 1975). No such mechanismsappear to assist the phosphorus cycle,and while we do not have comparable in-vestigations of other elements, it seemsunlikely that they would be of primaryimportance in controlling the productionof natural systems.

M. Brylinsky (pers. comm.) performedcalculations on the precipitation datafrom IBP sites which partially supportmy hypothesis about latitudinal effects innutrient input. IIc found a significant cor-relation between latitude and amount ofprecipitation (r = 0.43, n = 89), but no

significant relationship between concen-tration of nutrients in precipitation andlatitude. He was unable to separate dif-ferences in the effects of cultural sourcesor collection techniques, while in ourmuch smaller analysis we were able tominimize such differences. Careful stud-ies of global precipitation chemistry arenecessary before the relationship be-tween latitude, cultural pollutants, andconcentration can be accurately assessed,and sllch knowledge is necessary before

a rational management strategy can bcdevised for production and cutrophica-tion in all climatic and geological set-tings.

The above treatment suggests generalstrategies for the management of waterbodies which should be widely applica-ble. However, when management of aspecific water body is discussed, light,temperature, hydrology, and morphologyas well as nutrients may play important

roles. For example, low light availabilityin very shallow lakes may be dlze to highwind-induced turbidity or to the inflow

of a large, highly turbid river. For thisreason Lake Chad, at only 13”N and pre-sumably with quite a high nutrient input,is as unproductive as most subarctic lakes

(Brylinsky and Mann 1973). Althoughone can devise predictive managementstrategies that will apply to the majorityof lakes, there will always be a small pro-portion of water bodies which will notconform to any generalized pattern.

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Submitted: 29 December 1975Accepted: 15 November 1977

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Schindler 1978