Table Of ContentDissolved Organic Matter in Lacustrine Ecosystems:
Energy Source and System Regulator
Developments in Hydrobiology 73
Series editor
H. J. Dumont
Dissolved Organie Matter in Laeustrine
Eeosystems:
Energy Souree and System Regulator
Edited by
K. Salonen, T. Kairesalo & R. I. Jones
Reprinted (rom Hydrobiologia, vol. 229 (1992)
Springer Science+Business Media, B.V.
ISBN 978-94-010-5092-0 ISBN 978-94-011-2474-4 (eBook)
DOI 10.1007978-94-011-2474-4
Pril1led on acidjree paper
All Rights Reserved
© 1992 Springer Science+Business Media Dordrecht
Originally published by Kluwer Academic Publishers in 1992
Softcover reprint ofthe hardcover 1st edition 1992
No part 01' the material protected by this copyright notice may be reproduced or utilized in any
form or by any means, electronic or mechanical, inc1uding photocopying, recording, or by any
information storage and retrieval system, without written permission from the copyright owner.
v
Contents
Preface .......................................................................... . Vll
Origin and nature of DOM in lakes
Natural and man-caused factors affecting the abundance and cycling of dissolved organic sub
stances in precambrian shield lakes
by D. W. Schindler, S. E. Bayley, P. J. Curtis, B. R. Parker, M. P. Stainton & c. A. Kelly
Sources, concentrations and characteristics of organic matter in softwater lakes and streams of the
Swedish forest region
by M. Meili ................................................................. . 23
Leaching from vegetation of soluble polyphenolic compounds, and their abundance in temporary
ponds of the Dofiana National Park (SW Spain)
by L. Serrano ............................................................... . 43
Will an increased greenhouse impact in Fennoscandia give rise to more humic and coloured lakes?
by C. Forsberg .............................................................. . 51
Impacts of environmental changes on the biogeochemistry of aquatic humic substances
by H. De Haan .............................................................. . 59
DOM as an energy source
The influence of humic substances on lacustrine planktonic food chains
by R. I. Jones ............................................................... . 73
Extracellular dissolved organic carbon released from phytoplankton as a source of carbon for
heterotrophic bacteria in lakes of different humic content
by I. Sundh & R. T. Bcll ..................................................... . 93
Allochthonous dissolved organic matter as an energy source for pelagic bacteria and the concept
of the microbial loop
by L. J. Tranvik ............................................................. . 107
Dissolved organic carbon in a humic lake: effects on bacterial production and respiration
by D. O. Hessen ............................................................. . 115
Planktonic food chains of a highly humic lake. 1. A mesocosm experiment during the spring primary
production maximum
by K. Salonen, L. Arvola, T. Tulonen, T. Hammar, T.-R. Metsala, P. Kankaala& U. MUnster
125
Planktonic food chains of a highly humic lake. II. A mesocosm experiment in summer during
dominance of heterotrophic processes
by K. Salonen, P. Kankaala, T. Tulonen, T. Hammar, M. James, T.-R. Metsala & L. Arvola 143
Bacterioplankton in a small polyhumic lake with an anoxic hypolimnion
by P. Kuuppo-Leinikki & K. Salonen ........................................... . 159
Microbial control of dissolved organic carbon in lakes: research for the future
by J. E. Hobbie ............................................................. . 169
VI
DOM as a system regulator
Gradient-dominated ecosystems: sources and regulatory functions of dissolved organic matter in
freshwater ecosystems
by R. G. Wetzel. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 181
Littoral-pelagial interchange and the decomposition of dissolved organic matter in a polyhumic lake
by T. Kairesalo, A. Lehtovaara & P. Saukkonen .................................. 199
Extracellular enzymes in a polyhumic lake: important regulators in detritus processing
by U. Munster, P. Einio, 1. Nurminen & 1. Overbeck .............................. 225
Effects of different molecular weight fractions of dissolved organic matter on the growth of bacteria,
algae and protozoa from a highly humic lake
by T. Tulonen, K. Salonen & L. Arvola .......................................... 239
Vertical distributions of bacteria and algae in a steeply stratified humic lake under high grazing
pressure from Daphnia /ongispina
by L. Arvola, K. Salonen, P. Kankaala & A. Lehtovaara ........................... 253
Migrations of haemoglobin-rich Daphnia iongispina in a small, steeply stratified, humic lake with an
anoxic hypolimnion
by K. Salonen & A. Lehtovaara. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 271
Concluding remarks
by R. G. Wetzel .............................................................. 289
Hydrobiologia 229: vii, 1992.
K. Salonen. T. Kairesalo & R. I. Jones (eds.). vii
Dissolved Organic Matter in Lacustrine Ecosystems: Energy Source and System Regulator.
Preface
Dissolved organic matter (DOM) is quantitatively the most important pool of organic matter in most
lakes. Photosynthesis by the littoral and pelagic flora produces autochthonous DOM within lakes through
various secretion and decomposition processes. In addition, part of the production of the terrestrial
vegetation within the catchment area enters surface waters as allochthonous DOM. The two components
can be widely different in composition. Allochthonous DOM is largely composed of humic substances
which have already undergone a complicated series of modifications in soil. The fate of these humic
substances in water is poorly understood, but they are generally considered refractory to further rapid
microbial degradation. The role ofDOM in the food chains of water bodies has been controversial since
the beginning of the 20th century, and with few exceptions has been largely ignored. Only in the 1980's
did the importance of DOM become more widely accepted with the recognition of the 'microbial loop'
as a mechanism by which DOM can be utilised by higher trophic levels.
From the tropics to the northern coniferous forest zone, allochthonous DOM may produce a degree
of brown colouration in surface waters. In Finland, lakes are generally highly coloured because of the
high input of allochthonous humic substances from catchments with peaty soils. As a consequence,
awareness of the potential importance of DOM in lakes developed relatively early in Finnish limnology.
H. Jarnefelt, the first professor of limnology in Finland, took account of DOM in the 1930's while
developing his classification scheme for lakes. Subsequently, in the 1960's, his successor R. Ryhiinen laid
the foundations of Finnish research into humic waters. In 1986, the report of an international evaluation
of scientific research in hydrobiology in Finland, organised by the Academy of Finland, recommended
increased support for fundamental research on the limnology of humic lakes in Finland. Following that
recommendation, a three year research programme entitled "Food chains of humic lakes" was established
at Lammi Biological Station (University of Helsinki) with financial support from the Academy of Finland
and from the Maj and Tor Nessling Foundation. The main aim of the programme was to evaluate the
role of DO M in humic lakes, with detailed study of a polyhumic lake, Mekkoj arvi. The end of this project
provided a timely opportunity for a symposium to disseminate the results of the research and to discuss
them in the wider context of international research into ecosystem effects of DOM.
This volume contains the proceedings of that symposium, held at Lammi Biological Station in May
1990. We were happy to be able to gather together many of the most distinguished scientists in the field
to present their results and to discuss important recent developments, such as the role of bacteria
nanoflagellate food chains. The symposium highlighted the many kinds of effects which allochthonous
DOM can have in lacustrine ecosystems, and helped to clarify the needs and directions for future research
on the food chains of humic lakes . We hope that the publication of these proceedings will help to focus
attention on the importance of DOM in lakes as an energy source and system regulator.
K. SALONEN
T. KAIRESALO
R. I. JONES
Hydrobiologia 229: 1-21, 1992.
K. Salonen, T. Kairesalo & R.I. Jones (eds.),
Dissolved Organic Matter in Lacustrine Ecosystems: Energy Source and System Regulator.
© 1992 Kluwer Academic Publishers.
Natural and man-caused factors affecting the abundance and cycling of
dissolved organic substances in precambrian shield lakes
D. W. Schindler,l S. E. Bayley,t P. J. Curtis,l B. R. Parker/ M. P. Stainton2 & C. A. Kelly3
1 Departments of Zoology and Botany, University of Alberta, Edmonton, Alberta T6G 2E9, Canada;
Freshwater Institute, Fisheries and Oceans Canada, 501 University Crescent, Winnipeg, Manitoba R3T
2
2N6, Canada; 3 Department of Microbiology, University of Manitoba, Winnipeg R3T 2N2, Canada
Abstract
Effects of natural factors (drought and forest fire), and experimental perturbations (fertilization and
acidification) on dissolved organic carbon (DOC) concentrations and ratios to other nutrients in lakes
of the Experimental Lakes Area are examined using data obtained over a period of 20 years. DOC
concentration, and the ratio of dissolved iron to DOC in lakes of the area were strongly correlated with
the relative size of the catchment to the lake.
DOC in many lakes of the area declined over 20 years, due to increased water residence times caused
by increasing average temperature and decreasing precipitation. Inexplicably, Lake 382 was an excep
tion to this general observation. Acidification of Lake 302S to below pH 5.0 also caused DOC to de
crease. The lesser acidification of Lake 223 (min. pH 5.0) did not significantly affect DOC. Experimental
acidification of a small peatland also caused a temporary decline in DOC concentrations in bog pools.
Changes in DOC appear to affect the availability of mercury for methylation. Addition of aluminum to
a small acidic lake caused a two-fold decline in DOC.
Fertilization of Lake 227 caused a considerable increase in DOC, and in ratios of DOC to other carbon
fractions. New stable ratios did not occur for a decade after fertilization began. Lake 226N, fertilized
at a lower rate, showed similar but less pronounced increases in DOC, but the experiment was termi
nated after only eight years. Phosphorus fertilization caused a dramatic increase in the lability of the DOC
pool in Lake 226N, where the autochthonous carbon pool was labelled with DI14C. A large increase
in autochthonous production of DOC and increased microbial utilization of allochthonous DOC appear
to have occurred.
DOC concentrations in streams were higher after drought, but concentrations were unrelated to flow
volume during wet periods. Due to lower strearnfIows in drought years, annual yields of DOC from
streams were unaffected by drought.
Mesocosm experiments showed that DOC's primary effect on iron is to inhibit sedimentation, pos
sibly by suppressing flocculation reactions that are known to control the cycles of many metals.
The changes in DOC in lakes brought about by changes in water renewal, acidification, or other
perturbations can have major effects on the cycles of metals, lake transparency, and phytoplankton
production and standing crop.
Introduction webs (Wetzel et al., 1972). It also has important
effects on other elemental cycles (Stumm & Mor
Dissolved organic matter (DOM) is an important gan, 1981; Drever, 1988; Weilenmann et ai., 1989;
energy source for microbially-based aquatic food Curtis, 1991). In softwaters, high concentrations
2
of dissolved organic compounds with low pKa's real forest communities dominated by jackpine
can be a major source of acidity (LaZerte & Dil (Pinus banksiana) and black spruce (Picea ma
lon, 1984; Eshleman & Hemond, 1985; Korte riana). Small wetlands also occur in some of the
lainen & Mannio, 1987). A number of new meth catchments, causing major changes in DOC.
ods of study have rekindled interest in DOM Brunskill & Schindler (1971) give more detailed
among aquatic ecologists and geochemists. information on the watersheds.
In most cases, the index of DOM that is mea The period of record is one of climatic warm
sured in lakes is dissolved organic carbon (DOC). ing and drying. Average lake temperatures in
Our studies are no exception, and to be strictly creased by about 2.5 C, and water renewal times
0
correct, we shall refer to DOC throughout the rest for the lakes increased several-fold (Schindler
of this paper. et al., 1990). The warm, dry weather caused a
Curiously, methane has not been considered as high incidence of forest fires in the area. Of the
part of DOC, despite the fact that it is an ex lakes studied in their natural state, Lake 239
tremely important energy source for bacteria (re (L239) had over half of its watershed burned in
viewed by Rudd & Taylor, 1980). Recently, at 1974, and all of it burned in 1980. Lake 382 (L382)
tention has shifted to methane because of its had only one small fire in its catchment, so any
importance as a greenhouse gas (Lorius et al., changes should reflect the effects of drought alone.
1990). We shall follow the usual procedure, by These reference systems have been important in
excluding methane from our discussion of DOC, interpreting experimental results, for the increas
but its importance as an organic carbon pool ing water renewal times and water temperatures
should not be forgotten. have caused many changes in the physical, chem
More typically, the DOC pool is regarded as ical and biological properties of lakes in the area
containing humic and fulvic acids, plus smaller (Schindler, 1988; Schindler et at., 1990).
organic molecules that are excreted by organisms In addition, DOC and many other parameters
and are an important substrate for metabolism by have been monitored in lakes that have been ex
microorganisms. In this paper, we focus instead perimentally altered by adding nutrients, acids
on ecosystem-level changes in DOC in response or radiotracers. Lakes 227 (L227) and 226N
to various natural factors and experimental per (L226N) were fertilized with phosphorus and ni
turbations at the Experimental Lakes Area. These trogen. Carbon, as sucrose, was also added to
records reveal some characteristics of DOC and L226N. Lake 226S (L226S) received nitrogen and
its interactions with the cycles of other elements carbon, but no phosphorus. The two basins of
that cannot be easily studied by smaller-scale, L226 were fertilized from 1973 -1980, after which
short-term studies. they were monitored during recovery. Recent
summaries are provided by Schindler, 1990;
Description of the studies Schindler et at., 1987; Shearer et at., 1987; Find
lay & Kasian, 1987.
At the Experimental Lakes Area (ELA) in north Lake 223 (L223) and 302S (L302S) were acid
western Ontario, we have measured a number of ified with sulfuric acid. The former lake was acid
physical, chemical and biological variables in ified for eight years, reaching a pH of 5.0, after
lakes, streams and wetlands for over two decades, which it was allowed to recover slowly to a pH
during a period of climatic warming and lower of 5.8 in 1988. Lake 302S has been acidified to a
than average precipitation (Schindler, 1988; pH of 4.5, at which value it is currently being held.
Schindler et at., 1990). The lakes are small, soft Further details of these lake experiments are sum
water systems in catchments underlain by Pre marized by Schindler (1988; 1990), Rudd etal.
cambrian gneisses or granites. Catchments have (1990) and Schindler et al. (1991).
thin, sandy soils, usually under 1 m in depth. The Carbon-14 was added as carbonate to three
catchments are covered with typical pristine bo- lakes with differing DOC concentrations and
3
nutrient inputs (Hesslein et al., 1980; Bower & we shall use TDP in our examination of dissolved
McCorkle, 1980; Bower et al., 1987). These ex organic nutrient ratios.
periments offer unique opportunities to observe
differences in the patterns of transformation of
inorganic carbon into DOC, and in how DOC Observations on DOC in natural lakes and streams
interacts with the cycles of nutrients and trace at the Experimental Lakes Area and elsewhere in
metals. Further opportunities to observe the be the precambrian shield
haviour of DOC under a wide range of conditions
were offered by a comparative study of the iron In preliminary surveys, Schindler (1971 a) ob
cycle in lakes with over an order of magnitude served that water color was correlated with the
range in DOC concentrations (Curtis, 1991), a ratio of terrestrial drainage area (Ad) to lake sur
study of streams draining upland and wetland face area (AJ, suggesting that DOC was largely
areas (Bayley, unpubl.) and a study of the effects of terrestrial origin. This observation was tested
of artificial applications of sulfuric and nitric acids by Curtis (1991), who showed a close correlation
to wetland systems (Urban et al., 1989; Bayley between DOC concentration in lakes and Ad/ Ao.
et al., 1987, unpubl.). In all of the studies, chem Engstrom (1987) also found a strong relationship
ical analyses were done as described by Stainton between DOC and Ad! Ao for lakes of Labrador
et al. (1977). with small catchments, and Rasmussen et al.
The changes in ratios of carbon, nitrogen and (1989) provided detailed analyses of the DOC
phosphorus in the dissolved organic pool result watershed relationships in a variety oflakes. They
ing from various man-made or natural stresses found that catchment slope, lake size and depth
may change the availability of such compounds also had significant effects on DOC concentra
for metabolism. Much of the dissolved organic tions. Gorham et al. (1986) found that organic
fraction in a pristine oligotrophic lake consists of acidity accounted for a high proportion of the
relatively refractory residuals from biological pro acidity in Nova Scotia lakes, regardless of
cesses in the lake and its catchment. As we shall whether or not they received acidic precipitation.
show, lake fertilization causes DOC to increase, Schindler (1971 b) showed that the color of water
adding both refractory and labile compounds to was the major factor attenuating light in thc oli
the DOC pool. In addition, fertilization with gotrophic lakes at ELA, a conclusion which had
phosphorus seems to cause increased availability previously been reached by Birge & Juday (1934)
of DOC. As discussed by Munster et aI., 1991, for lakes in northern Wisconsin. Lakes with the
DOC residuals may represent 'capacitors' that highest concentrations of DOC (1500-1800 t1 M)
extend the nutrient reserves for algae and bacte also had maximum light penetration strongly
ria over longer time periods than would otherwise shifted toward yellow or orange wavelengths
be possible. Their availability may also depend (> 600 nm), while the clearest lakes of the area
on the nutrient sufficiency of bacteria (see also (which generally have DOC concentrations of
Jones, 1991 ). We shall therefore compare 240-400 JiM) had maximum penetration by blue
the ratios of DOC to DON (dissolved or to green wavelengths « 500 nm) (Schindler,
ganic nitrogen = TDN - (NH4 + N03 + N02) or 1971 b). Similar results were reported by Effier
to DOP (dissolved organic phosphorus), to see et al. (1985) and Watras & Baker (1988). Vertucci
whether the relative sizes of pools of nutrients in & Likens (1989) showed that DOC also had a
dissolved organic matter are affected by any of strong effect on the reflectance oflight from lakes.
the perturbations. Because our earlier experi DOC was positively correlated with reflectance of
ments have shown that for all practical purposes, wavelengths from 600-750 nm, but negatively
DOP = measured total dissolved phosphorus, i.e., correlated with visible wavelengths. Large spec
that inorganic P is below the limits of detection tral shifts were found for rather small changes in
(Levine & Schindler, 1980; Levine et al., 1986), DOC concentration. The euphotic zones in the
