DEPENDENCIES OF FOOD WEB A ND NUTRIENT CYCLING DYNAM ICS ON
DISSOLVED ORGANIC MATTER (DOM) AND INORGANIC NUTRIENT
CONCENTRATIONS IN LAKE ENCLOSURES
by
Erinn Honor Radomske
B.Sc., Okanagan University College, 1999

THESIS SUBMITTED IN PARTIAL FULFILLMENT OF
THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
in
NATURAL RESOURCES A ND ENVIRONMENTAL STUDIES
(ENVIRONMENTAL SCIENCE)

THE UNIVERSITY OF NORTHERN BRITISH COLUMBIA
November 2004

© Erinn Honor Radomske, 2004

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Abstract
An autotrophic-allotrophic gradient was established in 12 lake enclosures across a natural
DOM concentration gradient. Phytoplankton were co-regulated by solar irradiance and
inorganic nutrient concentrations, whereas bacterioplankton were strongly dependent on
DOM in the reference enclosures. Nutrient scavenging in the reference enclosures was
limited by efficient biotic incorporation and recycling, across the full DOM gradient.
Nutrient enrichment stimulated a strong autotrophic response across the autotrophicallotrophic gradient due to increased phytoplankton productivity. Bacterioplankton
productivity was still strongly dependent on DOM, but bacterioplankton productivity also
increased either as a direct or indirect result o f nutrient enrichment. Carbon, nitrogen, and
phosphorus were effectively scavenged from the water column by incorporation into biomass
at high rates and then deposited in the sediments in the nutrient enriched enclosures,
producing nutrient-rich sediments. The data further suggest that at DOM concentrations
greater than 14 mg L '\ allotrophy would dominate regardless o f inorganic nutrient
enrichment.

11

Table of Contents
ABSTRACT..................................................................................................................................................ii
TABLE OF CONTENTS......................................................................................................................... iii
LIST OF TA BLES..................................................................................................................................... vi
LIST OF FIG U R ES................................................................................................................................. vii
ACKNOW LEDGM ENTS.....................................................................................................................viii
1.

LITERATURE REVIEW ................................................................................................................. 1
1.1.

General Introduction................................................................................................................. 1

1.1.1.
1.2.

O bjectives........................................................................................................................... 4

D O M ............................................................................................................................................ 6

1.2.1.
DOM Sources......................................................................................................................6
1.2.2.
DOM Properties................................................................................................................. 8
1.2.2.1.
Light Attenuation....................................................................................................9
1.2.2.2.
Nutrient Complexation.........................................................................................10
1.3.

Pelagic Microbial Community............................................................................................. 12

1.3.1.
1.3.2.

Phytoplankton.................................................................................................................. 13
Bacterioplankton..............................................................................................................15

1.4.

Elemental Stoichiometry........................................................................................................18

1.5.

Literature C ited....................................................................................................................... 20

2.
DEPENDENCIES OF PHYTOPLANKTON A ND BACTERIOPLANKTON
BIOMASS A ND PRODUCTIVITY ON DISSOLVED ORGANIC MATTER (DOM) AND
INORGANIC NUTRIENTS...................................................................................................................41
2.1.

Introduction.............................................................................................................................. 41

2.2.

Methods..................................................................................................................................... 43

2.2.1.
2.2.2.

Site Description................................................................................................................43
Enclosures......................................................................................................................... 44

111

2.2.3.
Sample Collection and Preparation............................................................................ 45
2.2.4.
Sample A nalyses.............................................................................................................46
2.2.4.1.
Water Chemistry................................................................................................... 46
2.2.4.1.1. Dissolved Organic Carbon............................................................................... 46
2.2.4.1.2. Total Dissolved Nitrogen................................................................................. 46
2.2.4.1.3. Total Dissolved Phosphorus............................................................................46
2.2.4.1.4. Dissolved Inorganic Carbon............................................................................47
2.2.4.1.5. pH ........................................................................................................................... 49
2.2.4.2.
Microbial B iom ass................................................................................................ 49
2.2.4.2.1. Chlorophyll a ...................................................................................................... 49
2.2.4.2.2. Bacterioplankton Abundance.......................................................................... 49
2.2.4.B.
Microbial Productivity and Respiration........................................................... 50
2.2.4.3.I. Phytoplankton Productivity and Community Respiration........................50
2.2.4.B.2. Specific Photosynthetic R a te...........................................................................51
2.2.4.5.3. Bacterioplankton Productivity........................................................................ 51
2.2.4.4.
Net Metabolism......................................................................................................52
2.2.5.
Statistical A nalyses........................................................................................................ 53
2.3.

Results........................................................................................................................................54

2.3.1.
2.3.2.
2.3.3.
2.3.4.
2.3.5.
2.3.6.
2.3.7.
2.4.

Water Chemistry............................................................................................................ 54
Phytoplankton................................................................................................................. 55
Bacterioplankton.............................................................................................................56
Net Enclosure Metabolism........................................................................................... 58
D issolved Inorganic Carbon........................................................................................59
Community Respiration................................................................................................ 60
GPP:R and GPP:BP R atios.......................................................................................... 60

D iscussion.................................................................................................................................61

2.4.1.
2.4.2.

Autotrophy-Allotrophy Gradient................................................................................61
Autotrophic Shift with NutrientEnrichment............................................................ 64

2.5.

C onclusion................................................................................................................................68

2.6.

Literature C ited........................................................................................................................68

3.
ELEMENT RATIOS OF SEDIMENTS PRODUCED FROM DOM AND
INORGANIC NUTRIENT DEPENDENT SCA V EN G IN G ......................................................... 89
3.1.

Introduction.............................................................................................................................. 89

3.2.

Methods..................................................................................................................................... 91

3.2.1.

Site Description............................................................................................................... 91

IV

3.2.2.
Enclosures.........................................................................................................................92
3.2.3.
Sample Collection and Preparation............................................................................. 93
3.2.4.
Sample A nalyses............................................................................................................. 94
3.2.4.1.
D issolved Organie Carbon...................................................................................94
3.2.4.2.
Total Dissolved Nitrogen..................................................................................... 94
3.2.4.3.
Total D issolved Phosphorus............................................................................... 94
3.2.4.4.
Seston and Sediment C, N , and P ...................................................................... 95
3.2.5.
C, N, and P Scavenging.................................................................................................95
3.2.6.
Mass B alance................................................................................................................... 95
3.2.7.
Mass Transfer Coeffieient and % Retention.............................................................96
3.2.8.
Element R atios.................................................................................................................97
3.2.9.
Statistieal A nalyses.........................................................................................................97
3.3.

Results.........................................................................................................................................98

3.3.1.
C, N , and P Enclosure Concentrations....................................................................... 98
3.3.1.1.
D issolved..................................................................................................................98
3.3.1.2.
Seston........................................................................................................................ 99
3.3.1.3.
Sediments................................................................................................................. 99
3.3.2.
C, N, and P Seavenging...............................................................................................100
3.3.2.1.
Carbon.....................................................................................................................100
3.3.2.2.
N itrogen................................................................................................................. 101
3.3.2.3.
Phosphorus............................................................................................................ 102
3.3.2.4.
Mass B alanee........................................................................................................103
3.3.3.
C:N, C:P, N:P Element R atios................................................................................... 104
3.3.3.1.
D issolved Element R atios................................................................................ 104
3.3.3.2.
Seston Element R atios........................................................................................105
3.3.3.3.
Sediment Element Ratios..................................................................................105
3.4.

D iseussion................................................................................................................................ 106

3.4.1.
3.4.2.
3.4.3.

4.

C, N, and P Scavenging.............................................................................................106
Element Ratios as Indicators o f Processes.............................................................. 108
Autotrophy-Allotrophy Convergence...................................................................... I l l

3.5.

Conclusions..............................................................................................................................I l l

3.6.

Literature C ited...................................................................................................................... 112

SUMMARY AND CONCLUSIONS....................................................................................... 130
4.1.

Literature C ited...................................................................................................................... 132

List of Tables
Table 2.1 Results o f significant simple regression m odels.............................................................80
Table 3.1 Initial total mass o f each component contributing carbon, nitrogen, and
phosphorus.......................................................................................................................................118
Table 3.2 Concentrations o f carbon, nitrogen, and phosphorus in the dissolved water
column, in the seston, and in the sediments............................................................................. 119
Table 3.3 Results o f significant simple regression m odels.......................................................... 120
Table 3.4 Carbon, nitrogen, and phosphorus mass transfer coefficients and percent sediment
retention.............................................................................................................................................121

VI

List of Figures
Figure 1.1. Autotrophy-allotrophy continuum graph...................................................................... 39
Figure 1.2. Comparison o f the autotrophic and allotrophic food w e b s ......................................40
Figure 2.1. Map o f site location........................................................................................................... 81
Figure 2.2. Schematic o f the lake enclosures used in this study...................................................82
Figure 2.3. Dependencies o f phytoplankton biomass, phytoplankton productivity, and
specific photosynthetic rate on DOC concentration and inorganic nutrient enrichment 83
Figure 2.4. Dependencies o f bacterioplankton biomass and productivity on DOC
concentration and inorganic nutrient enrichment...................................................................... 84
Figure 2.5. Dependencies o f p C O x concentrations on DOC concentration and inorganic
nutrient enrichment..........................................................................................................................85
Figure 2.6. Dependence o f DlC concentration on DOC concentration and inorganic nutrient
enrichment.......................................................................................................................................... 86
Figure 2.7. Dependence o f community respiration on DOC concentration and inorganic
nutrient enrichment..........................................................................................................................87
Figure 2.8. Dependencies o f GPP:R and GPP:BP ratios on DOC concentration and inorganic
nutrient enrichment..........................................................................................................................88
Figure 3.1. Map o f site location.......................................................................................................... 122
Figure 3.2. Schematic o f the lake enclosures used in this study................................................. 123
Figure 3.3. Carbon, nitrogen, and phosphorus scavenging dependence on DOC concentration
.....................................................................................................................................................
124
Figure 3.4. Sediment carbon, nitrogen, and phosphorus dependence on DOC concentration.
.............................................................................................................................................................125
Figure 3.5. Carbon and nitrogen mass balances and DOC concentration dependence plotted
with absolute errors calculated with a 95% confidence........................................................ 126
Figure 3.6. DOC dependence o f dissolved water column element ratios.................................. 127
Figure 3.7. DOC dependence o f seston element ratios..................................................................128
Figure 3.8. DOC dependence o f sediment element ratios............................................................129
Figure 4.1. Revised autotrophy-allotrophy continuum graph........................................................134

V ll

Acknowledgments
I would like to thank m y supervisors Dr. Ellen Petticrew and Dr. Jeff Curtis for their help and
guidance on m y masters thesis. Thanks to my committee member Dr. B ill M cGill for his
critical reviews and positive comments on m y thesis. And to my external examiner Dr. R olf
Vinebrook for taking the time to read my thesis and provide me with critical reviews.

Additional thanks to Dr. Sherry Schiff and Jason Venkiteswaran at the University o f
Waterloo for their help and support with sample collection and analysis at the Experimental
Lakes Area. Many thanks to Robert Bunn for his assistance in the field and in the laboratory.

An NSERC Discovery Grant awarded to Dr. Jeff Curtis and a Sigma-Xi, Grant-in-Aid o f
Research awarded to me, supported this study financially. Applied Environmental Research
Laboratory at Malaspina University College analysed the samples for total dissolved nitrogen
and Stephan Page o f the Experimental Lakes Area (ELA) provided us with the precipitation
data.

M y final thanks goes to Chad Luider for his ongoing support. Chad provided me with
statistical and analytical advice, critical reviews o f many drafts, and provided me with the
emotional support I needed.

vm

1. Literature Review
7.7.

General Introduction

Food web and nutrient cycling dynamics arc an integral part o f lake ecosystem function
(Elscr ct. al. 1998; Elscr and Foster 1998; Pace and Cole 2000; Elscr ct. al. 2000c). The
concept o f energy and nutrient transfers between biotic and abiotic components in lakes is
important in understanding lake ecology (Sterner et. al. 1992; DeAngelis 1992; Elscr et. al.
1995). Energy and nutrients are supplied to a lake ecosystem from the terrestrial
environment, atmospheric deposition, and internally through transformation processes. The
major energy and nutrient elements involved in biogeochemical cycling in lakes are carbon,
nitrogen, and phosphorus. Carbon, nitrogen, and phosphorus are important primarily because
o f their importance in cell growth and metabolism (Redfield 1958; Elscr et. al. 2000a; Sterner
and Elscr 2002). Therefore, food web dynamics influence nutrient cycling dynamics in lakes
by affecting the proportion o f energy and nutrients in each pool as w ell as the flux o f energy
and nutrients among pools (Stumm and Morgen 1995; Elscr et. al. 1998; Elscr et. al. 2000a;
Elscr et. al. 2000c; Hessen et. al. 2003). These pools include the dissolved and particulate
phases o f nutrients and nutrients deposited in the sediments.

The flux o f carbon, nitrogen, and phosphorus between the dissolved and particulate phases
and between inorganic and organic pools is dependent on the element ratios o f the organisms
and their environment as w ell as metabolic processes (Elscr et. al. 1995; Elscr et. al. 1998;
Elscr et. al. 2000c; Hessen et. al. 2003). Element ratios o f an organism and its environment
can help address the fate and flux o f carbon, nitrogen, and phosphorus among pools in lake

ecosystems (Elser et. al. 1995; Elser et. al. 1998). The fate o f nutrients includes
reincorporation into biomass, remineralization into the dissolved inorganic pool, or settling
out o f the water column to form sediments (Santschi 1988).

Element ratio requirements o f trophic levels as w ell as the primary metabolism driving lake
productivity can affect biogeochemical cycling o f energy and nutrients in lake ecosystems
(Sterner et. al. 1998; Elser et. al. 1998; Elser et. al. 2000c; Elser et. al. 2003). Phytoplankton
have flexible stoichiometric requirements, which often reflect the element ratios o f its
surrounding environment (Sterner et. al. 1997; Elser et. al. 2000b). Bacterioplankton are less
flexible than phytoplankton and have higher nutrient requirements (Vadstein et. al. 1988;
Makino et. al. 2003). Higher trophic levels, such as zooplankton, have rigid stoichiometric
requirements and high nutrient requirements (Elser et. al. 2000b), but graze on phytoplankton
with variable, and sometimes nutrient-poor, stoichiometry (Sterner et. al. 1992; Sterner et. al.
1998; Elser et. al. 2000c).

The majority o f research on lake ecosystem function has been conducted on autotrophic lakes
(Rich and Wetzel 1978; Currie 1990; Kirchman 1994). However, a trophic discontinuity
appears to exist between autotrophic and allotrophic lakes. The differences in food web
drivers (e.g. solar radiation and dissolved organic matter) between these lakes can result in
different nutrient cycling dynamics that reflect the primary metabolism o f the lake (Jones
1992; del Giorgio and Peters 1994; Jansson 1998; Jones 1998).

Autotrophic lakes are categorized primarily based on increasing inorganic nutrient
concentrations and increasing primary productivity, and they arc classified as cither
oligotrophic, mcsotrophic, or cutrophic lakes (Fig. 1). Oligotrophic lakes generally have low
inorganic nutrient concentrations and low primary productivity, whereas cutrophic lakes have
high inorganic nutrient concentrations and high primary productivity. Autotrophic systems
rely on phytoplankton production to mobilize energy to higher trophic levels (Birge and
Juday 1927; Vadstein et. al. 1989; Currie 1990; Hessen 1992; Cole et. al. 2000).

Allotrophic or dystrophic lakes do not fit within this continuum as they are characterized by a
high proportion o f dissolved organic matter (DOM) derived from terrestrial sources
(allochthonous), moderate to high nutrients concentrations, and low primary productivity
relative to the total inorganic nutrient concentrations (Birge and Juday 1927; Jackson and
Hecky 1980; M eili 1992; del Giorgio and Peters 1994; Jansson et. al. 1996).
Bacterioplankton are the primary drivers o f allotrophic food webs, and they are important in
mobilizing organically bound carbon to higher trophic levels (Tranvik 1989; Jones 1992;
Hessen 1998; Tranvik 1998). Therefore, the differences between autotrophic and allotrophic
lakes are the w ay nutrients are utilized and the primary microbial metabolism that drives the
system (Fig. 1.2) (Jansson 1998; Jansson et. al. 2000; Hakanson and Jansson 2002).

Current research indicates that the majority o f lakes worldwide are allotrophic, driven by
heterotrophic metabolism based on allochthonous organie matter (Kortelainen 1993; Cole et.
al. 1994). It has also been proposed that only extremely oligotrophic and extremely
cutrophic lakes are truly autotrophic systems (Baron et. al. 1991; del Giorgio and Peters

1993; del Giorgio and Peters 1994; Schindler et. al. 1997; del Giorgio et. al. 1999; Cole et. al.
2000; Jansson et. al. 2000). W hile allotrophic lakes may dominate our landscape the
biogeochemical processes driving these systems are far less understood than autotrophie
lakes.

The primary factors that appear to regulate lake metabolism and separate autotrophie lakes
from allotrophic lakes are natural dissolved organic matter loading, the availability o f solar
irradiance, and inorganic nutrient concentrations (Jones 1992; Tranvik 1998). Allochthonous
DOM provides bacterioplankton with a source o f carbon independent o f phytoplankton and a
source o f nutrients in allotrophic systems (Currie 1990; Jones 1992; Hessen 1992; Arvola et.
al. 1996; Arvola and Tulonen 1998). Therefore, natural allochthonous DOM can stimulate
bacterioplankton growth resulting in high bacterioplankton abundance and productivity in
allotrophic systems (Tranvik 1989; Hessen et. al. 1994; Jansson et. al. 1999). Furthermore,
allochthonous DOM has the ability to attenuate solar irradiance and to complex nutrients
(Francko and Heath 1982; de Haan et. al. 1990; Shaw 1994; Scully and Lean 1994; Morris et.
al. 1995). These properties o f DOM can create light and nutrient limiting conditions for
phytoplankton (Jackson and Hecky 1980; Jones 1998; Carpenter et. al. 1998). Thus,
allotrophic and autotrophic lakes may respond differently to allochthonous DOM and
nutrient loading and the availability o f solar irradiance.

1.1.1. Objectives
This research investigated the food web and nutrient cycling dynamics in systems with
variable natural DOM concentrations. These food web and nutrient cycling dynamic
dependences were investigated using a 2 x 6 enclosure design set up in the Experimental

Lakes Area (ELA) in northwestern Ontario. A gradient o f natural DOM concentration
(measured analytically as dissolved organic carbon, DOC), potentially representing an
autotrophic-allotrophic gradient, was established in two replicate sets o f six enclosures. One
set acted as a reference, and the other set was enriched with inorganic nutrients to stimulate
an autotrophic response across the autotrophic-allotrophic gradient.

This research is presented as two experimental chapters. Chapter 2 investigated the
dependencies o f phytoplankton and bacterioplankton on DOC and inorganic nutrient
concentration. The hypotheses tested in Chapter 2 were: 1. increasing DOC concentration
w ill shift the pelagic microbial community from autotrophic to allotrophic; and 2. nutrient
enrichment w ill prevent or dampen the shift o f the pelagic microbial community from
autotrophic to allotrophic.

Chapter 3 investigated the DOM dependence o f nutrient scavenging from the water column
and the DOM dependence o f the element ratios o f the sediments formed in the lake
enclosures. The null hypotheses tested in Chapter 3 were: 1. scavenging o f carbon, nitrogen,
and phosphorus from the water column is independent o f DOC concentration; 2. scavenging
o f carbon, nitrogen, and phosphorus from the water column is independent o f nutrient
enrichment; 3. element sediment ratios are independent o f DOC concentration; and 4.
element sediment ratios are independent o f nutrient enrichment.

1.2.

DOM

1.2.1. DOM Sources
Natural dissolved organic matter (DOM) originates from two sources: autochthonous and
allochthonous (McKnight and Aiken 1998; W etzel 2001). Autochthonous organic matter is
derived within lake systems from the hy-products o f photosynthesis, microhial activity,
leaching from macrophytes, and microbial and plant cell lysis (Lampert 1978; M eili 1992;
W etzel 1995). Autochthonous organic matter is less coloured than allochthonous organic
matter and typically exists in smaller concentrations in lake systems (M eili 1992; Münster
and de Haan 1998; Curtis 1998). This DOM is usually less absorbent and fluorescent, and it
is also considered biologically labile, or readily usable by microbes (McKnight et. al. 1994;
Tranvik 1998). Autochthonous DOM has a C:N element ratio o f approximately 14:1 and,
therefore, it is a nutrient-rich substrate for bacterioplankton (Wetzel 2001).

Allochthonous DOM is derived from decomposed plant material in the terrestrial
environment (Fukushima et. al. 1996; McKnight and Aiken 1998), and it is transported to
lake ecosystems via hydrologie pathways (Schindler et. al. 1997; Curtis 1998).
Allochthonous DOM is transformed by soil microbes as it is transported through a watershed
to a lake ecosystem, and as a result this DOM is generally considered recalcitrant, or resistant
to microbial degradation (Singer and Munns 1987; Manahan 1994). Approximately 70 to
80% o f allochthonous DOM consists o f recalcitrant humic substances (W etzel et. al. 1995),
which strongly absorb light, reducing the depth o f the photosynthetic zone as DOM
concentration increases (McKnight and Aiken 1998). Allochthonous DOM is nutrient-poor

with a C:N element ratio o f approximately 58:1 and, therefore, it is a poor organic substrate
for bacterioplankton (W etzel 1995; Wetzel 2001).

The recalcitrant allochthonous DOM results in lower assimilation rates, reduced
incorporation efficiency, and greater respiration rates by bacterioplankton (Hope et. al. 1996;
del Giorgio and Cole 1998). However, allochthonous DOM is a stable source o f carbon and
nutrients for bacterioplankton. Allochthonous DOM can support up to 90% o f
bacterioplankton productivity in allotrophic lakes, and it can result in 2 to 4 times greater
bacterioplankton biomass and productivity in allotrophic lakes than autotrophic lakes
(Tranvik 1989; Jansson et. al. 1996; Jansson et. al. 1999).

Climate, hydrology o f the watershed, catchment characteristics, and vegetation types can
influence the quantity and quality o f allochthonous DOM entering a lake (Rasmussen et. al.
1989; Curtis 1998). Significant alterations to the hydrology o f the watershed due to forest
harvesting, fires, flooding or other factors may influence the quantity and quality o f DOM
and the amount o f nutrients reaching lake systems (Jackson and Hecky 1980; Meyer and Tate
1983; Guildford et. al. 1987; Christensen et. al. 1996).

Global climate change may seriously affect allochthonous DOM loading. Currently there is a
concern that precipitation and natural DOM concentrations are decreasing in temperate North
American lakes (Schindler et. al. 1996; Schindler et. al. 1997; Schindler and Curtis 1997).
The opposite trend is occurring in Scandinavia (Forsherg 1992). In addition to the increasing

DOM loading, nitrogen and phosphorus loading are also inereasing in Scandinavia (Hessen
et. al. 1994). Changes in DOM and nutrient loading to lake systems w ill affect the
underwater light regime, nutrient availability, and ultimately the food web drivers and
nutrient cycling dynamics o f both allotrophic and autotrophic lakes.

Most temperate North American lakes have DOM concentrations ranging from 2 to 8 mg L '\
and they are primarily composed o f allochthonous DOM (Meili 1992; Kortelainen 1993;
Lean 1998). Autochthonous DOM often dominates lakes associated with watersheds with
low terrestrial biomass, such as alpine lakes. These lakes can have DOM concentrations < 3
mg L'^ (Baron et. al. 1991; Sommaruga et. al. 1999). In contrast, allotrophic lakes have
DOM concentrations ranging from 5 to 30 mg L'^ and are associated with high absorbance
and low transparency (Hessen 1998; Lean 1998). Regardless o f the source, no more than
20% o f the total natural DOM pool in lakes is ever biologically labile, but this fraction is
continually replenished from the refractory portion by photolysis and enzymatic hydrolysis
(Tranvik 1988; Münster et. al. 1992; Kroer 1993; Bushaw et. al. 1996; Tranvik 1998).

1.2.2. DOM Properties
Natural alloehthonous DOM has the ability to attenuate solar irradiance and to complex
nutrients, which creates an environment in allotrophic lakes that is structurally and
functionally different from autotrophic lakes (Salonen et. al. 1992; Jones 1992; Hessen 1998;
Jansson 1998; Jones 1998). The ability to attenuate solar irradiance can result in lower
phytoplankton photosynthesis, but photolytic by-products can stimulate bacterioplankton
productivity. Furthermore, DOM bound nutrients can result in nutrient limiting conditions

for phytoplankton, but can act as a source o f nutrients to bacterioplankton through
decomposition o f DOM by bacterioplankton (Blomqvist et. al. 2001 ; King 2002).

1.2.2.1. Light Attenuation
Natural allochthonous DOM attenuates solar irradiance in surface waters, and in moderate
concentrations DOM can protect organisms from harmful U V radiation (Scully and Lean
1994). Absorbance, a measure o f solar irradiance attenuation, increases as a function o f
increasing DOM concentration (Morris et. al. 1995; Bukaveckas and Robbins-Forbes 2000).
Researchers have shown that natural DOM concentrations can explain 85 to 92% o f the
among-lake variation in UV absorbance values, indicating a close relationship between DOM
concentration, lake water absorbance, and transparency (Morris et. al. 1995; Fee et. al. 1996).
Suspended particles are minor factors in solar irradiance attenuation in natural lake systems
as compared to oceans, but suspended particles become increasingly more important in
eutrified lake systems that typically support higher phytoplankton biomass (Fee et. al. 1996).

Availability o f solar irradiance directly affects photosynthetic processes by phytoplankton.
Photosynthesis increases as a function o f increasing irradiances at low levels, but at moderate
to high levels phytoplankton become light inhibited and primary productivity decreases
(Long et. al. 1994; Lampert and Sommer 1997). High irradiances in the water column o f a
lake often correspond to low allochthonous DOM loading and to high autochthonous DOM
loading, where autochthonous DOM is usually transparent in the photosynthetically active
wavelengths (Morris et. al. 1995).

The effective light attenuating properties o f DOM can suppress phytoplankton productivity
(Arvola et. al. 1996; Carpenter et. al. 1998; Jones 1998). Attenuation o f visible light and UV
radiation by high loading o f natural allochthonous DOM concentrations occurs within the
first few centimeters o f the water column (Lean 1998). More specifically, DOM can
successfully attenuate photosynthetically active radiation (PAR: 400-750nm), which is
extremely important for photosynthesis. DOM concentrations can account for 85% o f the
variation observed in PAR and 90% in U V attenuation (Bukaveckas and Robbins-Forbes
2000). Therefore, primary productivity is often light limited in allotrophic lakes (Arvola et.
al. 1996; Carpenter et. al. 1998).

The attenuating properties o f natural allochthonous DOM affect bacterioplankton in lake
systems. DOM is susceptible to photolysis, or the breakdown by U V radiation, which occurs
concomitantly with solar irradiance attenuation (Strome and Miller 1978; Stewart and Wetzel
1981). Photolysis can increase the labile fraction o f allochthonous DOM resulting in higher
bacterioplankton biomass and productivity than observed in autotrophic lakes (Lindell et. al.
1995; Wetzel et. al. 1995; Münster and de Haan 1998; Tranvik et. al. 2000). As a result,
bacterioplankton are often relieved o f their dependence on phytoplankton for their carbon
source due to the high allochthonous DOM concentrations present (Hessen 1998; Grover and
Chrzanowski 2000; Blomqvist et. al. 2001).

1.2.2.2. Nutrient Complexation
Natural allochthonous DOM complexes inorganic nutrients, therefore, reducing the inorganic
nutrient concentrations available to the pelagic microbial community (Jackson and Hecky
1980; de Haan et. al. 1990; Jones 1992; Shaw 1994). Nitrogen and phosphorus are often

10

transported from watersheds to lakes bound to allochthonous DOM, therefore, systems
dominated by allochthonous DOM loading may have lower biologically available inorganic
nutrient concentrations than autotrophic lakes (Jansson 1998; Wetzel 2001). DOM can also
complex nutrients in the water column, removing nitrogen and phosphorus from the available
inorganic nutrient pool (de Haan et. al. 1990; Shaw 1994).

Phytoplankton productivity in high DOM systems is lower than that predicted from the high
nutrient concentrations (Jackson and Hecky 1980; M eili 1992). Complexation by
allochthonous DOM removes nitrogen and phosphorus from the available inorganic nutrient
pool creating nutrient limiting conditions for phytoplankton (Jackson and Hecky 1980).
Some phytoplankton, such as phagotrophic phytoflagellates, may assimilate DOM directly or
consume bacterioplankton to obtain the necessary nutrients for productivity in allotrophic
lakes as an adaptive strategy and, therefore, may dominate the phytoplankton community
(Sanders and Porter 1988; Porter 1988; Isaksson et. al. 1999).

Bacterioplankton productivity is potentially limited by nutrients bound to DOM because o f
the recalcitrant nature o f allochthonous DOM. However, DOM degradation by photolysis
and bacterioplankton enzymatic hydrolysis are the two processes that can release nutrients
from their complexed state. Photolytic processes are shown to release labile nitrogen- and
phosphorus-rich organic substances from DOM (Francko and Heath 1982; Bushaw et. al.
1996; Kieber et. al. 1999; Tranvik et. al. 2000). These nutrient-rich substrates are rapidly
assimilated by bacterioplankton to drive productivity. Bacterioplankton decomposition o f
allochthonous DOM by enzymatic hydrolysis is slow, but it can still help support

11

bacterioplankton nutritional requirements (Münster et. al. 1992; W etzel 1995). Therefore,
high allochthonous DOM concentrations are an important nutrient source for
bacterioplankton in allotrophic lakes (de Haan et. al. 1990; Hessen et. al. 1994; Arvola and
Tulonen 1998).

1.3.

Pelagic Microbial Community

The pelagic microbial community includes but is not restricted to phytoplankton and
bacterioplankton that exist within the water column o f lakes, and they comprise a portion o f
the seston. Pelagic microbial productivity is defined by two trophic gradients driven by
separate energy sources. Microbial productivity along the autotrophic gradient is driven hy
solar energy, whereas microbial productivity along the allotrophic gradient is driven hy
allochthonous organic matter (Jones 1992). As a result o f these differences in microbial
drivers and productivity, a trophic discontinuity appears to exists between autotrophic and
allotrophic lakes.

The trophic discontinuity is the result o f differences in food web drivers and nutrient cyeling
dynamics in autotrophic and allotrophic lakes (Jones 1992; del Giorgio and Peters 1994;
Jansson et. al. 2000). Increasing inorganic nutrient concentrations and increasing
phytoplankton biomass and productivity characterize the autotrophic gradient. In contrast,
increasing allochthonous organic matter and increasing bacterioplankton biomass and
productivity characterize the allotrophic gradient (Cole et. al. 2000). Therefore, autotrophic
and allotrophic lakes differ in nutrient utilization, the primary microbial metabolism that

12

drives food web dynamics, and in the flux o f energy and nutrients (Jansson 1998; Hakanson
and Jansson 2002).

1.3.1. Phytoplankton
The microbial community o f autotrophic lakes is dominated by phytoplankton that mobilize
carbon to higher trophic levels. As primary producers in these systems, phytoplankton utilize
light energy to convert inorganic carbon to biomass through photosynthesis. Inorganic
carbon sources used by phytoplankton include carbon dioxide and bicarbonate. High rates o f
photosynthesis can result in the sequestering o f carbon dioxide directly from the atmosphere,
making the lake system a net sink for carbon dioxide (Schindler 1977; Stumm and Morgen
1995; Cole 1999; Hanson et. al. 2003).

In autotrophic lakes, dissolved inorganic nitrogen and phosphoms are used directly by
phytoplankton to aid metabolism. High concentrations o f inorganic nutrients can facilitate
high photosynthetic rates, which can deplete the inorganic carbon pool in an aquatic system
further increasing the need to sequester carbon from the atmosphere (Schindler 1977; Stumm
and Morgen 1995; W etzel 2001). However, phytoplankton are typically light or nutrient
limited rather than carbon limited because o f the large atmospheric source o f inorganic
carbon (Schindler 1977; Smith 1986; Sterner et. al. 1997).

Phytoplankton depend strongly on their environment for nutrients and can tolerate a wide
range o f solar irradiance and inorganic nutrient concentrations, which results in their flexible
element ratios that reflect their environment (Sterner et. al. 1997; Frost and Elser 2002). For

13

example, phytoplankton C:N, C:P, and N:P ratios can range widely from 6 - 15, 8 - 1340,
and 1 6 - 4 4 , respectively (Downing and M cCauley 1992; Coveney and W etzel 1995;
Hochstadter 2000; Mari et. al. 2001). The Redfield ratio (C:N = 6.6, C:P = 106, N:P = 16)
represents the optimal element ratio for marine phytoplankton (Redfield 1958; Buffle and De
Vitre 1994). Although freshwater phytoplankton ratios are typically more variable than
marine phytoplankton (Hecky et. al. 1993; Elser and Hassett 1994; Sterner et. al. 1997; Elser
et. al. 2000b), the Redfield ratio can serve as a useful comparison to lake phytoplankton or to
seston ratios (Uehlinger and Bloesch 1987; Buffle and De Vitre 1994).

Phytoplankton productivity is strongly suppressed in allotrophic lakes (Jackson and Hecky
1980; Blomqvist et. al. 2001; Klug 2002; Drakare et. al. 2002), which is likely due to the
strong light attenuating and nutrient complexation properties o f allochthonous DOM (de
Haan et. al. 1990; Jones 1992; Shaw 1994; Scully and Lean 1994; Morris et. al. 1995). The
suppression o f phytoplankton results in productivity levels that are insufficient to support the
other trophic levels and, therefore, phytoplankton are not the base o f the aquatic food web in
allotrophic lakes (Scavia and Laird 1987; Jansson et. al. 1996).

Adaptive strategies by phytoplankton have been identified by researchers to minimize the
effects o f high allochthonous DOM loading in allotrophic lakes. M obile phytoplankton can
regulate their position within the water column to maximize solar irradiance availability for
photosynthesis and, therefore, they dominate the phytoplankton community in allotrophic
systems (Jones 1998). Furthermore, phagotrophic phytoflagellates can consume
bacterioplankton and DOM directly and picophytoplankton, with high surface area to volume

14

ratios, can successfully compete with bacterioplankton for nutrients (Sanders and Porter
1988; Porter 1988; Nygaard and Tobiesen 1993; Jansson et. al. 1996; Isaksson et. al. 1999;
Drakare et. al. 2003).

1.3.2. Bacterioplankton
The primary role o f bacterioplankton in autotrophic lakes is decomposition o f organic matter.
As decomposers, bacterioplankton break down organic material and recycle nutrients back
into the system. Dissolved and particulate organic matter are decomposed primarily by
bacterioplankton in the water column making the nutrients bound to organic matter available
to phytoplankton for primary production (Wetzel 1995). As a result, phytoplankton depend
on bacterioplankton to remineralize organically bound nutrients (Azam et. al. 1983; Currie
and K alff 1984c).

Bacterioplankton are consumers o f organic matter, and they are an important component o f
the microbial loop in autotrophic lakes (Azam et. al. 1983). Bacterioplankton are typically
carbon limited and, therefore, they rely on phytoplankton for their organic carbon energy
source (Chrzanowski and Hubbard 1989; Coveney and W etzel 1995; Stumm and Morgen
1995). Bacterioplankton rapidly incorporate labile autochthonous organic matter into
biomass, which is transferred to higher trophic levels via the microbial loop (Azam et. al.
1983; Wetzel 1995; del Giorgio and Cole 1998). Therefore, a close coupling between
phytoplankton and bacterioplankton is often observed in autotrophic lakes (Sondergaard et.
al. 1988; Chrzanowski and Hubbard 1989; Coveney and Wetzel 1995).

15

In contrast to autotrophic systems, bacterioplankton in allotrophic lakes are not coupled to
phytoplankton (Jones and Salonen 1985; Hessen et. al. 1994; Jansson et. al. 1996; Jansson et.
al. 1999). The large pool o f allochthonous DOM in allotrophic lakes is a stable supply o f
carbon and nutrients for bacterioplankton metabolism, despite the recalcitrant state o f this
carbon source (Salonen et. al. 1983; de Haan et. al. 1990; Hessen 1992; Hessen et. al. 1994;
Wetzel 1995; Arvola and Tulonen 1998). Therefore, bacterioplankton are the base o f the
aquatic food web in allotrophic lakes by utilizing allochthonous organic carbon and nutrients
for biomass production (Tranvik 1989; Salonen et. al. 1992; Tranvik 1998; Grover and
Chrzanowski 2000).

Bacterioplankton in allotrophic lakes serve as a major pathway for carbon and nutrients to
higher trophic levels through grazing (Salonen and Jokinen 1988; Hessen 1992; Salonen et.
al. 1992; Arvola et. al. 1996; Kankaala et. al. 1996; Jansson et. al. 1999; Blomqvist et. al.
2001). Carbon flows through heterotrophic nanoflagellates (protozoans) and phagotrophic
phytoflagellates, the primary bacterivores, to higher trophic levels, such as zooplankton
(Porter 1988; Salonen and Jokinen 1988; Sherr et. al. 1992; Isaksson et. al. 1999). Typically
bacterioplankton are considered carbon limited in autotrophic systems, but this is unlikely in
allotrophic systems with high rates o f allochthonous DOM loading (Cotner and Wetzel 1992;
Grover 2000). Furthermore, nutrient enrichment studies o f allotrophic systems indicate that
bacterioplankton are nutrient limited rather than carbon limited (Vadstein et. al. 1988; Morris
and Lewis 1992; Morris and Lewis 1992; Hessen et. al. 1994; Chrzanowski et. al. 1995;
Jansson et. al. 1996).

16

Bacterioplankton can outcompete phytoplankton for the low available nutrient concentrations
in allotrophic systems (Currie and K alff 1984a; Currie and K alff 1984b; Currie and K alff
1984c; Chrzanowski et. al. 1995; Vadstein 2000). Bacterioplankton have high metabolic
demands for inorganic nutrient concentrations, and they can assimilate low nutrient
concentrations more efficiently than phytoplankton when they are not carbon limited (Ciurie
and Kalff 1984b; Vadstein et. al. 1988). These characteristics o f bacterioplankton can
contribute to the suppression o f phytoplankton growth in allotrophic systems (Jansson et. al.
1996; Grover 2000; Blomqvist et. al. 2001; Joint et. al. 2002; Drakare et. al. 2002).
Therefore, bacterioplankton abundance and productivity are generally high in allotrophic
lakes (Arvola et. al. 1996; Arvola and Tulonen 1998).

Decomposition o f allochthonous DOM by bacterioplankton enzymatic hydrolysis is slow, but
is an important nutrient recycling process in allotrophic systems (W etzel 1995; Münster and
de Haan 1998). Bacterioplankton can immobilize nutrients during decomposition o f DOM to
meet their high metabolic demands rather than recycling nutrients back to the inorganic
nutrient pool (Vadstein et. al. 1988; Tezuka 1990; Elser et. al. 1995). In contrast, nutrient
mobilization by bacterioplankton for phytoplankton productivity is important in autotrophic
systems (Sterner et. al. 1995). The immobilization o f nutrients by bacterioplankton can
further enhance the nutrient limited state o f phytoplankton in allotrophic lakes (Vadstein et.
al. 1988; Jansson 1998; Blomqvist et. al. 2001).

Nutrient immobilization by bacterioplankton results from the need to maintain elemental
stoichiometry (Vadstein et. al. 1989; Tezuka 1990; Hessen 1992; Vadstein et. al. 1993; Elser

17

et. al. 1995). Bacterioplankton have high metabolic nutrient requirements and less flexible
element ratios than phytoplankton (Vadstein et. al. 1988; Makino et. al. 2003). The C:N,
C:P, and N:P ratios for bacterioplankton reported in the literature ranges from 6 - 1 5 , 8 173, and 5 - 22, respectively (Coveney and Wetzel 1995; Chrzanowski et. al. 1996; Jansson
et. al. 2001).

Bacterioplankton incorporate nutrients and respire carbon during decomposition o f nutrientpoor substrates to meet their metabolic demands (Vadstein et. al. 1988; Hessen 1992).
Therefore, lakes that depend on bacterioplankton productivity generated from allochthonous
organic matter are typically net sources o f carbon dioxide (Salonen et. al. 1983; Hessen et. al.
1994). In contrast, autochthonous DOM generated by phytoplankton productivity is
assimilated more efficiently by bacterioplankton, resulting in lower respiration rates than the
primary productivity (del Giorgio et. al. 1997; del Giorgio and Cole 1998; del Giorgio and
Cole 1998; Hanson et. al. 2003). Therefore, autotrophic systems are generally net sinks for
carbon dioxide due to CO2 sequestering from the atmosphere by phytoplankton for
photosynthesis (Schindler et. al. 1997; Cole 1999; K elly et. al. 2001).

1.4.

Elemental Stoichiometry

Food web and nutrient cycling dynamics in autotrophic and allotrophic lakes are driven by
phytoplankton and bacterioplankton productivity, respectively. Elemental stoichiometry is a
method used to study the relationships between internal cycling processes and food web
dynamics within lakes (Elser et. al. 2000a; Elser et. al. 2000c; Sterner and Elser 2002). The
stoichiometric or element ratios o f an organism and its environment can help address the fate

18

and flu x o f carbon, nitrogen, and phosphorus in lake systems among pools (Elser et. al.
1998), which can help elucidate the different biogeochemical mechanisms that are occurring
in autotrophic and allotrophic systems (Elser et. al. 1995).

The element ratios o f the different biotic and abiotic pools represent nutrient availability,
metabolic processes, metabolic requirements o f organisms, and the nutritional quality o f food
sources (Elser et. al. 1998; Sterner and Elser 2002). The element ratios o f the dissolved and
particulate phases in the water column represent the balance o f available nutrients as w ell as
the nutrients scavenged from the water column (Stumm and Morgen 1995; Elser et. al.
2000a; Elser et. al. 2000c; Sterner and Elser 2002; Hessen et. al. 2003). Element ratios o f
recent sediments reflect the metabolic and nutrient scavenging processes occurring within the
water column o f a lake (Buffle and De Vitre 1994; Elser and Foster 1998; Elser et. al. 2000c;
Hakanson and Jansson 2002).

Nutrients are scavenged from the water column via three processes: incorporation,
adsorption, and coagulation (Santschi 1988). Incorporation o f carbon, nitrogen, and
phosphorus by organisms involves the assimilation o f these nutrients to form biomass.
Nutrients can also adsorb onto particles, and coagulation occurs between small particles that
combine to form larger particles. Coagulation is a less important scavenging process in soft
water lakes because dissolved organic matter can stabilize nutrients in solution, thereby
limiting coagulation (Weilenmann et. al. 1989). The fates o f scavenged nutrients include
remineralization into the dissolved inorganic pool, reincorporation into biomass, or settling
out o f the water column to form sediments.

19

The element ratios o f seston (i.e. suspended living and non-living organic matter) represent
the balance between carbon, nitrogen, and phosphorus hound in particulates. The ratios
reported in the literature for seston vary w idely (e.g. C:P ranges from 100 - 1632) (Sterner et.
al. 1997; Elser et. al. 1998; Elser and Foster 1998; Elser et. al. 2002). Element ratios o f
seston may represent the dominant organism comprising the pelagic microbial community,
the food quality o f the system, and or the importance o f nutrient-poor detrital particles (Elser
et. al. 2000a; Elser et. al. 2000c; Hessen et. al. 2003). Typically seston ratios are nutrient
deficient relative to the individual pelagic organisms, suggesting that detritus is a major
component o f seston (Uehlinger and Bloesch 1987; W etzel 1995).

1.5.

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38

Dystrophic

a

ou

o

Q

Oligotrophic

Eutrophic

Nutrients

Autotrophy

Figure 1.1. Autotrophy-allotrophy continuum graph (Hakanson and Jansson 2002).

39

A llo tro p h ic

A u to tro p h ic

Allocbtbonous DOM

Solar Radiation

Energy
Source

Energy
Mobilizers

I
Pbytoplankton

■■"■^►Bacteria

Bacteria

(microbial loop)

▼
Zooplankton

■Flagellates

Flagellates

Energy
Consumers

Fisb

Zooplankton

t

Fisb

Figure 1.2. Comparison o f the autotrophic and allotrophic food webs (Jansson et. al. 2000).

40

2. Dependencies of Phytoplankton and Bacterioplankton
Biomass and Productivity on Dissolved Organic Matter
(DOM) and Inorganic Nutrients

2.1.

Introduction

A trophic discontinuity appears to exist between autotrophic and allotrophic lakes due to
differences in food web drivers and nutrient cycling dynamics (Jones 1992; del Giorgio and
Peters 1994; Jansson et. al. 2000). Most researchers have assumed that lakes are primarily
autotrophic (Rich and W etzel 1978; Currie 1990), however, recent research indicates that the
majority o f temperate North American lakes are allotrophic and that the primary food web
drivers are allochthonous dissolved organic matter (DOM) and bacterioplankton productivity
(Hesslein et. al. 1980; Cole et. al. 1994; del Giorgio and Peters 1994).

Solar radiation and allochthonous DOM are the two energy sources that drive the autotrophic
and allotrophic gradients and determine pelagic microbial productivity. Solar energy drives
microbial productivity in autotrophic lakes, whereas allochthonous DOM drives microbial
productivity in allotrophic lakes (Jones 1992).

The autotrophic gradient is characterized by increasing inorganic nutrient concentrations and
increasing pbytoplankton productivity. Autotrophic lakes are clearwater lakes that are
typically undersaturated in carbon dioxide and, therefore, they are net sinks for CO 2 (Jones
1992; Schindler et. al. 1997). In contrast, the allotrophic gradient is characterized by
increasing allochthonous organic matter and increasing heterotrophic productivity.

41

Allotrophic systems are generally oversaturated in carbon dioxide due to decomposition o f
allochthonous DOM and, therefore, they are net sources o f CO 2 to the atmosphere (Salonen
et. al. 1983; Hessen et. al. 1994; Cole et. al. 1994).

Allotrophic or dystrophic lakes are characterized hy high proportions o f allochthonous DOM,
low primary productivity relative to the apparent nutrient availability, and high
hacterioplankton biomass and productivity (Jackson and Hecky 1980; Tranvik 1989; Jones
1992; Meili 1992; Tranvik 1998). Mechanisms hypothesized to cause dystrophy include
attenuation o f photosynthetically active radiation hy DOM and direct or indirect control o f
nutrient availability hy dissolved organic matter (Jones 1992; Jansson 1998; Jones 1998).

In allotrophic lakes, DOM probably competes with phytoplankton for available solar
irradiance resulting in light limiting conditions and low phytoplankton productivity (Jones
1992; Morris et. al. 1995; Arvola et. al. 1996; Carpenter et. al. 1998; Jones 1998). DOM also
has the ability to complex nutrients, which likely makes the nutrients unavailable to
phytoplankton for photosynthesis (Jackson and Hecky 1980; de Haan et. al. 1990; Shaw
1994; Jones 1998). Furthermore, hacterioplankton are not likely carbon limited in allotrophic
lakes because o f high allochthonous DOM concentrations (Cotner and W etzel 1992; Grover
2000). Photolysis o f DOM produces nutrient-rich organic substrates that stimulate
hacterioplankton growth (Francko and Heath 1982; W etzel et. al. 1995; Lindell et. al. 1995;
Bushaw et. al. 1996), and hacterioplankton can hydrolyse DOM releasing complexed
nutrients (Münster et. al. 1992; Münster and de Haan 1998). In addition, hacterioplankton
may outcompete phytoplankton for available nutrient concentrations, further suppressing

42

phytoplankton growth in allotrophic lakes (Currie and K alff 1984a; Currie and K alff 1984b;
Chrzanowski et. al. 1995; Joint et. al. 2002).

The objective o f this study was to investigate microbial food web dynamics as a function o f
DOM and inorganic nutrient concentrations. To meet this objective, two hypotheses were
tested: 1. increasing DOM concentration w ill shift the pelagic microbial community from
autotrophic to allotrophic; and 2 . nutrient enrichment w ill prevent or dampen the shift o f the
pelagic microbial community from autotrophic to allotrophic. Support for these hypotheses
w ill suggest that dystrophy is not a discrete trophie state as previously thought (Wetzel
2001), but is part o f a continuous distribution o f lake trophic states. The effect o f natural
dissolved organic matter (DOM) and inorganic nutrient concentrations on food web
dynamics were tested by determining the dependencies o f phytoplankton, hacterioplankton,
and inorganic carbon on DOM.

2.2.

Methods

2.2.1. Site Description
This study was conducted at the Experimental Lakes Area (ELA) in northwestern Ontario,
Canada (93°30’-94°00’W, 49°30’-49°45’N)(Fig. 2.1). The area ranges in elevation from 360
m to 380 m above sea level and is located on the south western region o f the Precambrian
Shield. The soils are poorly developed and underlain by granite, glacial sands, and gravels.
The vegetation is primarily boreal subclimax forest consisting o f jack pine (P in u s
b a n k sia n a ), black spruce (P ic e a m a ria n d ), trembling aspen {P o p u lu s tre m u lo id e s), and white

birch (B e tu la p a p y r ife r a ). The ELA mean annual temperatures range from 0.5 °C to 2.2 "C,

43

and the annual precipitation ranges from 500 mm to 750 mm (Brunskill and Schindler 1971;
Curtis and Schindler 1997). The lakes involved in this study were Lake 224 and Lake 225
and were chosen primarily because Lake 224 and Lake 225 represent the most extreme DOC
concentrations o f all active ELA lakes and, therefore, would provide an adequate DOC
concentration gradient. Furthermore, Lake 225 flows directly into Lake 224 making these
lakes hydrologically linked. Lake 224 has a surface area o f 25.9 ha, a drainage area o f 97.5
ha, and a mean depth o f 11.59 m. Lake 225 has a surface area o f 5.6 ha and a drainage area
o f 30.5 ha (Curtis and Schindler 1997).

2.2.2. Enclosures
Twelve, closed-bottom lake enclosures were randomized along a floating linear wooden
frame, and they were set up and remained in Lake 224 from July to September 2002. The
surface area and depths o f each enclosure was 0.84 m^ and 1.5 m, respectively. DOM
concentration gradients were established in two sets o f six enclosures by pumping water from
Lake 224 and Lake 225 into the enclosures in approximately 0%, 20%, 40%, 60%, 80%, and
100% proportions (relative to Lake 225)(Fig 2.2). These proportions potentially represent an
autotrophic-allotrophic gradient. Plankton were readily transferred into the lake enclosures
during pumping, but it is unlikely fish were transferred and none were observed in the lake
enclosures.

One set o f six lake enclosures acted as a reference (referred hereafter as reference
enclosures), and the other set was enriched with inorganic nutrients (referred hereafter as
nutrient enriched enclosures) to test the effects o f autotrophic stimulation on microbial
biomass and productivity along an autotrophic-allotrophic gradient. The nutrient enriched

44

enclosures were enriched with NaNOs and KH 2PO 4 at the beginning o f the experiment and
again 4 weeks later. The total amount o f nitrogen and phosphorus added to the enclosures
was 4500 mg N and 300 mg P, which elevated the concentrations by factors o f 10 and 7,
respectively.

2.2.3. Sample Collection and Preparation
Depth integrated water samples were collected w eekly from each o f the enclosures using a
1.5 m tube sampler and a bucket. Following each sample collection day, the enclosures were
mixed with an oar. Subsamples were taken from the integrated sample for analyses o f water
chemistry and hacterioplankton abundance and productivity. Samples collected for water
chemistry analyses were stored in 500 mL polyethylene bottles. From these samples, 100
mL aliquots were filtered through pre-ashed Whatman GF/C glass fibre filters and frozen.
One frozen filter from each sample was analysed for chlorophyll a. The filtrate was kept for
dissolved organic carbon (DOC; an analytical measure o f DOM), total dissolved nitrogen
(TDN), and total dissolved phosphorus (TDP) analyses. Bacterioplankton abundance and
productivity samples were stored in 60 mL tissue bottles and preserved with a final
concentration o f 3% glutaraldehyde buffered to pH 7 with 5N NaOH (Kepner and Pratt
1994). All water samples collected were stored and shipped at 4 "C.

Surface samples for dissolved inorganic carbon (DIG) and partial pressure o f carbon dioxide
{p C O j) were collected biweekly using headspace vials presalted with KCl to maintain pH

and to inhibit microbial activity between collection and analysis (Hesslein et. al. 1990; Kelly
et. al. 2001). These samples were analysed immediately following collection. In addition,
depth integrated samples for phytoplankton productivity and community respiration were

45

collected four times during the experiment. Analyses o f these samples were performed
immediately following collection and subsequent incubation.

2.2.4. Sample Analyses
2.2.4.1. Water Chemistry
2.2.4.1.1. Dissolved Organic Carbon
Filtered sample water was analysed for dissolved organic carbon (DOC) using a Shimadzu
TOC-5000A Total Organic Carbon Analyzer with a detection limit o f 0.05 mg L '\ A 40 mL
sample was acidified with 200 pL o f select grade HCl and sparged for 7 mins with oxygen to
volatilize and strip inorganic carbon from the sample. The sample was combusted to carbon
dioxide and measured with an infrared detector. This instrument was operated with a 2%
coefficient o f variation according to the instruction manual.

2.2.4.1.2. Total Dissolved Nitrogen
Total dissolved nitrogen (TDN) concentrations were determined on filtered samples using a
Shimadzu TNM-1 Total Nitrogen Analyzer with a detection limit o f 0.06 mg L '\ Samples
were combusted to nitrogen monoxide and nitrogen dioxide and then reacted with ozone to
create an excited state o f nitrogen dioxide. A chemiluminescence detector measured the light
emitted when the nitrogen dioxide returned to ground state.

2.2.4.1.3. Total Dissolved Phosphorus
Total dissolved phosphorus (TDP) concentrations were determined on filtered samples using
the persulphate digestion and ascorbic acid methods (Greenberg, Clesceri, and Eaton 1992).
The samples were digested with persulphate for 1 hr in an autoclave and then analysed on a

46

Milton Roy Spectrophotometer using a 5 cm pathlength. Sample absorbance was measured
at 885 nm. The detection limit o f this method is 0.01 mg L '\

2.2.4.I.4. Dissolved Inorganic Carbon
Surface water samples for analysis o f dissolved inorganic carbon (DIC) were measured to
determine the amount o f inorganic carbon available in the system. DIC samples were
acidified and then equilibrated with the headspace and analysed using a Varian Cbrompack
CP-3800 Gas Chromatograph. A criteria o f ±5% was used for reproducibility o f multiple
injections.

D IC =

+ HCO; + C O l

Eq 2.1

where, DIC concentration is the sum o f aqueous carbon dioxide (CO 2 ) and is
expressed as the partial pressure o f CO 2 (p C O i), bicarbonate (HCO 3'), and carbonate (COs^').
At pH < 9, the contribution o f carbonate is negligible, therefore, the equation becomes:

D I C = pC O ^ + H C O ;

Eq 2.2

The DIC concentration at atmospheric equilibrium (DICeq) was used as a reference point to
determine the utilization o f DIC in the enclosures, and it was calculated using the following
equations:

D IC ^ = p C O ,^ + H C O :

Eq. 2.3

47

Eq2.4

where, the suhseript x s stands for in excess, or oversaturation. The assumption that
HCOs'xs = HCOa'eq is made here because oversaturation o f CO 2 w ill affect the concentration
o f DIC, but w ill not significantly affect the concentration o f HCO 3 ". This assumption is not
valid when CO 2 is undersaturated because the equilibrium shifts to produce CO 2 and OH' in
Eq 2.5. The assumption becomes HCO 3 gq = HC 0 3 'unsat + OH' and OH' was not measured.

HCOi

CO; + O H -

Eq 2.5

Therefore, solving Eq 2.4 for HC 0 3 'xs and inserting it into Eq 2.3, w e get Eq 2.6:

D/C^ = D/C^ - ;,CO;^ + ;,CO;^

Eq 2.6

where, DICxs is measured DIC concentration in the reference enclosures in pM;
/ 7CO 2 XSis the measured partial pressure o f CO2 in the reference enclosures in pM, which was
determined to be close to or above equilibrium (see results); and pC O ieq is the measured
partial pressure o f CO2 at atmospheric equilibrium. Then ôDIC was calculated using the
following equation to determine if bicarbonate (HCO3 ) concentrations were changed in the
nutrient enriched enclosures as a result o f CO2 drawdown.

ÔD/C = D IC „ - D /C ,,

Eq 2.7

48

where, DICm is the measured DIC coneentration in either the reference or nutrient
enriched enclosures, and DICeq is the value calculated in Eq 2.6 for each reference enclosure
value.

2.2.4.I.5. p H
pH was measured on each o f the enclosure samples using a Beckman glass double junction
Ag-Ag/Cl pH electrode coupled with a Beckman 320 pH meter. The pH meter was
standardized using pH 4 and 7 buffers prior to each use.

2.2.4 2. Microbial Biomass
2.2.4.2.1. Chlorophyll a
Chlorophyll a, a surrogate for phytoplankton biomass (PB), was analysed by the technique
described by (W etzel and Likens 2000). Filters were left to extract for 24 hours in 10 mL o f
85% denatured alcohol. Analysis o f fluorescence at 660 nm with an excitation wavelength o f
436 nm was performed using a Shimadzu RF-1501 Spectrofluorophotometer. A stock
solution for the calibration standards was standardized using a Milton Roy
Spectrophotometer following the method o f (Wetzel and Likens 2000). A ll samples were
above the 4 pg L^ detection limit for this technique. Chlorophyll a was also converted to
units o f carbon using a conversion factor o f 50 pg C pg Chf^ (Coveney and W etzel 1995).
However, it is important to recognize that the proportion o f carbon in a plankton cell can
vary widely, especially under nutrient deficiencies and light limiting conditions (Hecky et. al.
1993).

2.2.4.2.2. Bacterioplankton Abundance

49

Bacterioplankton abundance, a surrogate for bacterioplankton biomass (BB), was determined
by epifluorescence direct counts (Hobbie et. al. 1977; Kepner and Pratt 1994). Samples were
stained with acridine orange to a final concentration o f 110 pg L'*, filtered onto 0.2 pm black
polycarbonate filters (Millipore ™), and counted at lOOOx magnification on an Olympus BH2 microscope. Minimums o f 200 cells were counted per filter. To prevent photobleaching,
the coverslips were mounted onto slides using non-drying immersion oil and 1,4diazabicyclo (DABCO, Triethylenediamine). Prepared filters were counted within 2 hours o f
staining. Bacterioplankton abundance was also converted to units o f carbon using a
conversion factor o f 0.121 pg C pm'^ and an average cell biovolume o f 0.06 pm^ (Hagstrom
et. al. 1979; Riemann et. al. 1984). The carbon per cell biovolume conversion factor is
variable (Newell and Christian 1981), but only the relative values were o f interest here.
Furthermore, applying an average cell biovolume is acceptable because bacteria exhibit a
small range in biovolume.

2.2.4.S. Microbial Productivity and Respiration
2.2.4.3.1. Phytoplankton Productivity and Community Respiration
Gross phytoplankton productivity (GPP) and community respiration (R) were measured as
changes in dissolved inorganic carbon (DIC) concentration during 4 to 7 hour incubations
(Hesslein et. al. 1990; K elly et. al. 2001). An integrated water sample from each enclosure
was transferred to three (initial, light, dark) 50 mL headspace vials making sure to fill from
the bottom and allowing the bottle to overflow. The bottles were capped to ensure no
bubbles. The initial CO 2 sample bottles were immediately fixed with 300 pL o f concentrated
phosphoric acid. The light and dark bottles were covered with a solar mesh to reduce light
intensity and incubated in Lake 239. Following the incubation, a 5 mL aliquot o f sample was

50

simultaneously removed from the bottles and replaced with N 2 gas, and then the sample was
fixed with phosphoric acid. DIC was analysed for CO 2 concentration in the headspace for all
bottles based on a precision o f ±5% using a Varian Cbrompack CP-3800 Gas
Chromatograph. The following equations were used to determine community metabolism;

Dark - Light = Gross primary production

Eq 2.8

Dark - Initial = Community respiration

Eq 2.9

2.2.4.3.2. Specific Photosynthetic Rate
The specific photosynthetic rate (SPR) was calculated to normalize gross primary
productivity per unit o f phytoplankton biomass using the following equation:

uçr

/-I

h~^

= ^ g C n g Chl-^ h-^

Eq 2.10

pg Chi L-'

where, the numerator is gross primary productivity, and the denominator is
chlorophyll a concentration.

2.2.4.3.3. Bacterioplankton Productivity
Bacterioplankton productivity (BP) was determined using the frequency o f dividing cells
(FDC) method (Hagstrom et. al. 1979). During bacterioplankton enumeration, dividing cells
(those cells showing invaginations but not separated) were also counted. This study used the
relationship between %FDC and specific growth rate established by (Riemann et. al. 1984).
An average bacterial cell biovolume o f 0.06 pm^ was used based on literature values

51

(Hagstrom et. al. 1979; Riemann et. al. 1984). Bacteria exhibit a small range in cell
biovolume, therefore, it is acceptable to use an averaged literature biovolum e when absolute
numbers are not required. The carbon per cell bio volume conversion factor o f 0.121 pg C
pm'^ is frequently reported in the literature and was used in this study (Riemann et. al. 1984;
Tranvik 1988). The carbon per cell biovolume conversion factor can range w idely from
0.087 pg C pm'^ to 0.380 pg C pm'^ (Newell and Christian 1981; Salonen et. al. 1992;
Friedrich et. al. 1999; Drakare et. al. 2002), but only the relative values are o f interest in this
study, therefore, the conversion factor w ill not affect the relative differences observed.

2.2A.4. Net Metabolism
Surface water samples for analysis o f dissolved inorganic carbon (DIC) and the partial
pressure o f CO 2 (pCOz) were measured to determine the amount o f inorganic carbon
available in the system and the net metabolism o f the enclosures, respectively. The p C 0 2 is
equal to C02(aq) in Eq 2.1, expressed as a partial pressure.

The p C O z samples were shaken to equilibrate the dissolved and gaseous phases with the
headspace. Henry's Law (Eq 2.11) was used to directly relate CO2 (aq) to p C O j , where Kh is
Henry's constant.

CO^^^)=Kfj^pCO^

E q2.11

Changes to CO 2 solubility were accounted for by correcting for the water temperature and
salt effects (Hesslein et. al. 1990; Kelly et. al. 2001). These samples were analysed using a

52

Varian Chrompack CP-3800 Gas Chromatograph and the data were assessed with a precision
o f ±5%.

The difference (ôpCOz) between the measured p C 0 2 (pCOzm) o f the water sample and the
atmospheric equilibrium value (pCOaeq), ranging from 12.5 pM to 14.8 pM, was used to
determine if the system was a net sink o f CO2 or a net source o f CO 2 .

ôpCOj =pCO^„ - p c o .

E q2.12

A negative value indicated that the system was a net sink for CO2 and CO 2 was sequestered
from the atmosphere. A positive value indicated that the system was a net source and excess
CO2 was released from the water into the atmosphere (Kelly et. al. 2001).

2.2.5. Statistical Analyses
A ll dependent variable data were integrated over the course o f the experiment and expressed
as a time weight average using the following equation (Eq 2.13):

(T o + T i )'

k +T2)

x (x , -X o ) +
w

k

- ^ 1)
y

V'

where, y is the measured parameter from day 0 to day n in cumulative days, and x is
the cumulative number o f days since the beginning o f the experiment from day 0 to day 61.

53

The initial DOC concentration for the enclosures was used as the independent variable, and
the reference and nutrient enrichment treatments were fixed factors. Data were analysed
using simple and stepwise multivariate regression analyses with SPSS 8.0 and assessed using
an alpha value o f 0.05. Simple regression analyses were used to determine the DOM
dependence o f the measured parameters and to compare between the reference and nutrient
enriched enclosures. The regression coefficients (slope and y-intercepts) were compared
between the reference and nutrient enriched enclosures to see if they were significantly
different using a homogeneity o f regression analysis. The homogeneity o f regression
analysis also determined whether the initial DOC concentration in the enclosures was a
significant covariate. Equal slopes between the reference and nutrient enriched enclosures
and DOC concentration as a covariate allowed an ANCOVA to be performed. ANCOVA
removed the effects o f the DOC covariate and assessed whether nutrient enrichment
significantly affected the measured parameter. Stepwise multivariate analysis was used for
exploratory purposes to better understand the relationships between parameters. M ANOVA
tested the effects o f nutrient enrichment on the measured parameters that were independent
o f DOM concentration.

2.3.

Results

2.3.1. Water Chemistry
The initial DOC concentrations in the both the reference and nutrient enriched enclosures
ranged from 3.6 mg L'^ to 11.4 mg L '\ The time weighted average TDN concentrations
ranged from 0.18 mg L'^ to 0.34 mg U ' and from 2.16 mg L'^ to 2.77 mg L'' in the reference

54

and nutrient enriched enclosures, respectively. The time weighted average TDP
concentrations were at or below the detection limit (0.01 mg L'^) in the reference enclosures
and ranged from 0.05 mg L'^ to 0.12 mg L'^ in the nutrient enriched enclosures. The time
weighted average pH values ranged from 6.0 to 6.4 in the reference enclosures and ranged
from 6.4 to 7.4 in the nutrient enriched enclosures.

2.3.2. Phytoplankton
Phytoplankton biomass (PB), measured as chlorophyll a concentration, increased as a
function o f increasing DOC concentration in the reference enclosures and ranged from 12 pg
L'^ to 48 pg L'* (r^ = 0.81; P < 0.01) (Table 2.1)(Fig. 2.3A). PB was independent o f DOC
concentration, but increased by one order o f magnitude as a function o f nutrient enrichment
in the nutrient enriched enclosures (P < 0.001). Chlorophyll a concentrations ranged from
239 pg U ' to 745 pg L'* in the nutrient enriched enclosures. Conversion o f chlorophyll a
concentrations to carbon units resulted in carbon biomass values ranging from 615 pg C L"'
to 2410 pg C L'^ in the reference enclosures and from 11900 pg C L'^ to 37200 pg C L'^ in
the nutrient enriched enclosures (Fig. 2.3A).

Gross primary productivity (GPP) was independent o f DOC concentration in the reference
enclosures and ranged from 8.10 pg C L'^ h'^ to 15.31 pg C L'^ h'^ (Fig. 2.3B). GPP
increased significantly in the nutrient enriched enclosures as compared to the reference
enclosures and ranged from 25.02 pg C L"' h'^ to 54.95 pg C L'* h ' (P < 0.001). GPP in the
nutrient enriched enclosures peaked between approximately 5.7 mg U* and 6.2 mg L'^ o f
DOC, but GPP was suppressed in the low DOC and high DOC nutrient enriched enclosures.
GPP did not correlate with chlorophyll a concentration in either o f the two sets o f enclosures.

55

The specific photosynthetic rate (SPR) decreased with increasing DOC concentration in the
reference enclosures ranging from 0.42 pg C pg Chl'^ h’* to 0.85 pg C pg Chl'^ h '\ but the
regression was non-significant (P > 0.05). SPR was independent o f DOC concentration in
the nutrient enriched enclosures and ranged from 0.20 pg C pg Chi'* h'^ to 0.39 pg C pg Chl'^
h'* (Fig. 2.3C). The SPR was significantly lower in the nutrient enriched enclosures than in
the reference enclosures (P < 0.001).

2.3.3. Bacterioplankton
Bacterioplankton biomass (BB), measured as bacterioplankton abundance, increased as a
function o f increasing DOC concentration in the reference enclosures and ranged from 3.51 x
10^ cells mU* to 9.34 x 10^ cells m U ' (r^ = 0.97; P < 0.001)(Table 2.1). BB increased with
increasing DOC concentration and ranged from 4.24 x 10^ cells m U ' to 6.56 x 10® cells m U '
in the nutrient enriched enclosures, but the regression was non-significant (P > 0.05)(Fig.
2.4A). The BB dependence on DOC concentration changed significantly as a function o f
nutrient enrichment, where BB in the low DOC nutrient enriched enclosures was
significantly higher than in the low DOC reference enclosures (P < 0.01). BB converted to
carbon biomass units ranged from 26 pg C L'^ to 68 pg C L’' in the reference enclosures and
ranged from 31 pg C L'^ to 48 pg C L'^ in the nutrient enriched enclosures (Fig. 2.4A).

Using DOC, chlorophyll a, TDP, and TDN concentrations as independent variables, stepwise
multivariate regression analyses showed that DOC concentration was the only variable that
significantly predicted BB in the reference enclosures (r^ = 0.97; P < 0.001). None o f these

56

other independent variables predicted BB in the nutrient enriched enclosures, suggesting that
some other variable, such as grazing, was regulating BB in these enclosures.

The dependence o f bacterioplankton productivity (BP) on DOC concentration was similar in
both sets o f enclosures, regardless o f nutrient enrichment, but BP was significantly higher in
the nutrient enriched enclosures (P < 0.05). BP was marginally dependent on DOC
concentration in the reference enclosures (r^ = 0.44; P = 0.09)(Fig. 2.4B) and ranged from
1.32 pg C L'^ h'^ to 3.01 pg C L’’ h '\ BP in the nutrient enriched enclosures was strongly
dependent on DOC concentration (r^ = 0.74; P< 0.05)(Table 2.1) and ranged from 3.13 pg C
L'^ h'* to 4.71 pg C L'^ h '\ The results from ANCOVA showed that nutrient enrichment
explained 84% o f the variation in adjusted BP values between the two sets o f enclosures (P <

0 .001).

DOC, chlorophyll a, TDP, and TDN concentrations were used as predictors for BP in a
stepwise multivariate regression analysis, but none o f these variables predicted BP separately
in the reference enclosures. Together, DOC, TDP, and TDN concentrations significantly
predicted BP in the reference enclosures (r^ = 0.99; P < 0.01), indicating that DOC and DOC
bound nutrients were the primary factors regulating BP in the reference enclosures.

DOC, TDP, and TDN concentrations all predicted BP in the nutrient enclosures separately,
but in a stepwise regression TDP was the only variable selected to predict BP (r^ = 0.89; P <
0.01). Together, TDP and chlorophyll a concentrations also significantly predicted BP in the
nutrient enriched enclosures, but chlorophyll a did not significantly increase the r^-value

57

obtained with TDP (r^ = 0.89; P < 0.05). The added phosphorus was important to
bacterioplankton growth and the bacterioplankton were likely P-limited. Phytoplankton
derived DOC may have also contributed to the increase in BP.

2.3.4. Net Enclosure Metabolism
The partial pressure o f carbon dioxide (p C O i) was marginally dependent on DOC
concentration and ranged from 12.1 pM to 21.4 pM in the reference enclosures (r^ = 0.55; P
- 0.056)(Table 2.1). The p C O i was strongly dependent on DOC concentration in the nutrient
enriched enclosures and ranged from 3.3 pM to 5.8 pM (r^ = 0.72; P < 0.05)(Fig 2.5A).
Nutrient enrichment did not change the dependence o f p C 0 2 on increasing DOC
concentration, but p C O i was significantly lower in the nutrient enriched enclosures than in
the reference enclosures (P < 0.05). ANCOVA showed that the nutrient enrichment
treatment explained 92% o f the variance in the adjusted p C 0 2 values between the two sets o f
enclosures (P < 0.001).

The Ô/JCO2 values for the reference enclosures were close to atmospheric equilibrium at low
DOC concentrations and then increased from equilibrium as DOC concentration increased,
indicating allotrophy at high DOC concentrations in the reference enclosures (r^ = 0.55; P =
0.056)(Table 2.1)(Fig 2.5B). The ô p C 0 2 values ranged from -1 .4 pM to 7.8 pM in the
reference enclosures. The Ô/7CO2 values decreased w ell below atmospheric equilibrium
ranging from -1 0 .3 pM to -7 .8 pM, but the d p C 0 2 increased towards equilibrium with
increasing DOC concentration (r^ = 0.72; P < 0.05). This suggests that the nutrient enriched
enclosures were approaching allotrophy at higher DOC concentrations.

58

2.3.5. Dissolved Inorganic Carbon
Dissolved inorganic carbon (DIC) concentrations decreased as a function o f increasing DOC
concentration in both the reference and nutrient enriched enclosures (r^ = 0.95, 0.88,
respectively; P < 0.01)(Table 2.1)(Fig 2.6A). The DIC concentrations ranged from 34.4 pM
to 100.8 pM in the reference enclosures and from 21.8 pM to 50.7 pM in the nutrient
enriched enclosures. The DIC concentration regression line in the reference enclosures did
not differ significantly firom the DICeq line (P > 0.05)(Eq 2.2), but the DIC dependence on
DOC concentration changed significantly as a function o f nutrient enrichment. DIC
concentration at low DOC concentration in the nutrient enriched enclosures was significantly
lower than at low DOC concentration in the reference enclosures (P < O.OI). The reference
and nutrient enriched regression lines would converge at a DOC concentration o f
approximately 13.8 mg L '\ indicating that at this point DOC becomes the primary factor
controlling the available DIC concentrations.

The ÔDIC concentrations were marginally dependent on DOC concentration in the reference
enclosures (r^ = 0.55; P = 0.056)(Tahle 2.1)(Fig 2.6B), and they were strongly dependent on
DOC concentration in the nutrient enriched enclosures (r^ = 0.83; P = 0.01). The ôDIC
values ranged from -1 .9 pM to 7.5 pM and from -4 8 .3 pM to -3 .3 pM in the reference and
nutrient enriched enclosures, respectively. The ÔDIC values were close to equilibrium at
high DOC concentrations, indicating that the enclosures were close to allotrophy at high
DOC concentrations in the nutrient enriched enclosures.

59

2.3.6. Community Respiration
Community respiration (R) was independent o f DOC concentration in the reference
enclosures (P > 0.05) and ranged from 7.12 pg C L'^ h’^ to 10.73 pg C L'^ h"\ R followed a
similar pattern as GPP in the nutrient enriched enclosures suggesting that respiration was
dependant on GPP (Fig 2.7). Respiration ranged from 11.40 pg C L"' h'* to 28.25 pg C L'^ h'
' in the nutrient enriched enclosures. R was significantly higher in the nutrient enriched
enclosures as compared to the reference enclosures (P < 0.01), but R was suppressed in the
low DOC and high DOC nutrient enriched enclosures. R correlated with GPP in the
reference enclosures at a P-value o f 0.1 (r^ = 0.73) and was correlated with GPP in the
nutrient enriched enclosures (r^ = 0.88; P < 0.05). Respiration did not correlate with BB or
BP in either the reference o f nutrient enriched enclosures.

2.3.7. GPP:R and GPP:BP Ratios
The phytoplankton productivity:community respiration ratios (GPPiR) were independent o f
DOC concentration in the reference and nutrient enriched enclosures and were not
significantly different between the reference and nutrient enriched enclosures (P > 0.05)(Fig
2.8A). The GPP:R ratios ranged from 0.40 to 1.9 in the reference enclosures and ranged
from 1.1 to 2.3 in the nutrient enriched enclosures.

The phytoplankton productivity:bacterioplankton productivity ratios (GPP:BP) were
independent o f DOC concentration in both the reference and nutrient enriched enclosures
(Fig 2.8B). These ratios were not significantly different between the reference and nutrient
enriched enclosures (P > 0.05), but the nutrient enriched enclosures had higher ratio values at

60

low DOC concentrations. The GPP:BP ratios ranged from 1.1 to 12 in the reference
enclosures and ranged from 6.2 to 74 in the nutrient enriched enclosures.

2.4.

Discussion

2.4.1. Autotrophy-Allotrophy Gradient
An autotrophic-allotrophic gradient was established across the natural DOM concentration
gradient in the reference enclosures, which supports hypothesis one. The shift from
autotrophy to allotrophy occurred at approximately 6 m g L'^ o f DOC. The dependences o f
p C 0 2 concentration and ô p C O j on DOC concentration suggested that CO 2 accumulated in

the water column o f the reference enclosures at DOC concentrations greater than 6 mg L'*.

At DOC concentrations o f at least 6 mg L '\ the 8 p C 0 2 data in the reference enclosures were
consistently greater than atmospheric equilibrium indicating that the enclosures were net
sources o f CO 2 and, therefore, were likely allotrophic (Hope et. al. 1996; D illon and Molot
1997; Duarte and Agusti 1998). These conclusions are consistent with findings from other
researchers who reported CO 2 supersaturation and phytoplankton productivity suppression at
DOC concentrations greater than 6 mg L'^ (del Giorgio and Peters 1994; Hope et. al. 1996;
Prairie et. al. 2002). Other researchers measured the shift from autotrophic to allotrophic at
10 mg L'^ o f DOC, but this higher DOC concentration is likely explained by higher total
phosphorus concentrations measured in those study lakes (Jansson et. al. 2000; Hanson et. al.
2003).

61

Carbon dioxide accumulation in the water column o f lakes is likely the result o f respiration
from the decomposition and subsequent assimilation o f organic matter by bacterioplankton
(Hessen 1992; del Giorgio and Peters 1994; Hope et. al. 1996; Prairie et. al. 2002), but may
also be from photochemical reactions (Graneli et. al. 1996). Results from research on five
Swedish oligotrophie lakes ranging from 4 mg L’* to 19 mg L'* o f DOC concentration
indicate that photooxidation o f DOC produces C0% and may contribute significantly to
supersaturation o f lakes (Graneli et. al. 1996).

Phytoplankton appeared eo-regulated by both solar irradiance and inorganic nutrient
concentrations in the reference enclosures. The direct dependence o f phytoplankton biomass
(PB) on DOC concentration in the reference enclosures was likely due to increased
chlorophyll a abundance by phytoplankton in response to increasing light limitation at higher
DOC concentrations. This conclusion is consistent with the independence o f phytoplankton
productivity (GPP) on DOC concentration and specific photosynthetic rate (SPR) data in the
reference enclosures. The SPR data shows that less carbon is actually produced per unit o f
chlorophyll a as DOC concentration increases. This conclusion is supported by researchers
who suggest DOM is an important indirect regulator o f phytoplankton growth by directly
regulating solar irradiance in aquatic ecosystems (Jackson and Hecky 1980; Lean 1998;
Carpenter et. al. 1998).

Phytoplankton growth in the reference enclosures was nutrient limited, which is supported by
the relative increase in GPP observed in the nutrient enriched enclosures. Therefore,
phytoplankton did not utilize organic nutrient sources, either directly or indirectly from

62

bacterioplankton decomposition to increase biomass at higher DOC concentrations in the
reference enclosures as suggested by other researchers (Sanders and Porter 1988; Porter
1988; Isaksson et. al. 1999). Bacterioplankton are more efficient assimilators o f low
available nutrient concentrations than phytoplankton and may have contributed to
phytoplankton nutrient limitation (Currie and K alff 1984a; Currie and K alff 1984b;
Chrzanowski et. al. 1995; Joint et. al. 2002).

In addition to solar irradiance and inorganic nutrient concentrations, low DIC (< 100 ^iM)
concentrations suggest that DIC may have also limited phytoplankton growth in the reference
enclosures. However, the large atmospheric source o f CO2 and quick dissolution o f CO 2 into
the water likely prevented inorganic carbon from limiting GPP (Schindler 1977; Wetzel
2001). The D ie concentrations in the reference enclosures were the same as DIG
atmospheric equilibrium concentrations, which suggests that biological activity within the
reference enclosures was insufficient to change the DIC concentration from atmospheric
equilibrium.

The direct dependence o f bacterioplankton biomass (BB) on DOC concentration in the
reference enclosures suggests the bacterioplankton were using the DOC for growth. This
result was supported by the direct dependence o f bacterioplankton productivity on DOC
concentration also observed in the reference enclosures. Results from other research support
the conclusion that bacterioplankton directly utilize allochthonous DOM for production o f
biomass (Tranvik 1988; McCauley et. al. 1989). Allochthonous DOM can act as a source o f
carbon independent o f phytoplankton and as a source o f nutrients for bacterioplankton.

63

especially at high DOC concentrations (Tranvik 1988; MeCauley et. al. 1989; de Haan et. al.
1990; Hessen 1992; Shaw 1994; W etzel 1995; Arvola et. al. 1996; Arvola and Tulonen
1998). Bacterioplankton typically rely on allochthonous DOM to support productivity
regardless o f the trophic state, however, the proportion assimilated w ill increase with
allotrophy (Chrzanowski and Hubbard 1989; Arvola et. al. 1996; Jansson et. al. 1999).

2.4.2. Autotrophic Shift with Nutrient Enrichment
Autotrophy appeared to be the dominant trophic state in the nutrient enriehed enclosures
across the natural DOM concentration gradient and supports hypothesis two. Nutrient
enrichment stimulated a strong autotrophic response across the autotrophic-allotrophie
gradient established in the referenee enclosures. The p C O i data suggested that the nutrient
enriched enclosures were undersaturated in carbon dioxide and, therefore, were autotrophic
systems (Schindler 1977; Sehindler et. al. 1997; Duarte and Agusti 1998; Carpenter et. al.
2001). The Ô/7CO2 data in the nutrient enriched enclosures were less than atmospheric
equilibrium for all DOC concentrations indicating that the enelosures were net sinks o f CO 2 .
These eonelusions are supported by results o f other studies that suggest highly eutrophic
systems are typically net sinks for carbon dioxide (del Giorgio and Peters 1993; Schindler et.
al. 1997; Jansson et. al. 2000).

The ô/?C02 dependenee on DOC concentration indicated that the nutrient enriched enclosures
would probably become net sources o f CO2 at DOC concentration values higher than used in
this study. This suggests that high nutrient availability cannot compete with significant
decreases in solar irradiance and in DIC concentrations due to high DOC concentrations and,
therefore, under these conditions the system would be allotrophic. This conclusion is

64

supported by results from research on systems with high allochthonous DOC loading, which
have low phytoplankton growth relative to the high nutrient availability (Jansson et. al. 2000;
Hanson et. al. 2003). Furthermore, these results provide support for the suggestion that
dystrophy is not a discrete trophic status (Fig 1.1), but rather is part o f a continuous
distribution o f trophic states, which are a function o f DOC concentration.

The DIC concentration data indicated that at a DOC concentration o f approximately 14 mg L"
\ DOC concentration was likely the primary regulator o f DIC concentration. DOC
concentration can inhibit or reduce the solubility o f carbon dioxide in water indicating that, at
high DOC concentrations and high nutrient availability, DIC concentration may limit
phytoplankton productivity (Wetzel 2001).

The available p C O i concentrations were likely fully utilized in the nutrient enriched
enclosures and additional carbon sources were required for photosynthesis, which is
supported by the larger ôDIC values than ôpCOa values. Phytoplankton in the nutrient
enriched enclosures likely consumed most o f the available p C O j in the nutrient enriched
enclosures and then relied on bicarbonate sources for photosynthesis. p C O i is preferentially
consumed by phytoplankton before other inorganic carbon sources (Gavis and Ferguson
1975; Wetzel 2001), but under high nutrient concentrations in the nutrient enriched
enclosures bicarbonate may also have been used. Alternatively, the low p C O i may have
resulted in an indireet drawdown o f bicarbonate by shifting the equilibrium towards CO 2
formation (Gavis and Ferguson 1975).

65

Phytoplankton in the nutrient enriched enclosures were no longer nutrient limited, which is
supported by the significant increase in gross phytoplankton productivity (GPP) observed.
GPP was suppressed in the nutrient enriched enclosures at low and high DOC concentrations,
which was likely due to light inhibition and light limitation, respectively. Low DOC
concentrations can offered little protection to phytoplankton from harmful UV damage
(Scully and Lean 1994; Lean 1998), which was amplified by the relatively shallow depth o f
the enclosures used in this study. High DOC concentration can limit productivity because
DOC competes with phytoplankton for available solar irradiance (Long et. al. 1994; Arvola
et. al. 1996; Carpenter et. al. 1998). Results from other research further supports the
conclusion that DOC concentration is an important indirect regulator o f phytoplankton by
regulating the availability o f solar irradiance (Morris et. al. 1995; Fee et. al. 1996; Jones
1998; Bukaveckas and Robbins-Forbes 2000).

BB was probably regulated by predation in the nutrient enriched enclosures. This conelusion
was supported by the direct dependence o f bacterioplankton productivity on DOC
concentration observed in the nutrient enriched enclosures. High bacterioplankton
productivity and low bacterioplankton biomass suggested that a high loss rate o f
bacterioplankton biomass was occurring in the nutrient enriehed enclosures. Predation is a
strong regulator o f bacterioplankton biomass and is enhanced in more productive ecosystems,
whereas oligotrophie systems tend to have low biomass insufficient to sustain large predator
populations (Currie 1990; Persson et. al. 1992; Pace and Cole 1996; Arvola and Tulonen
1998; Langenheder and Jurgens 2001).

66

The similar direct dependence o f bacterioplankton productivity (BP) on DOC concentration
in the reference and nutrient enriched enclosures suggested that allochthonous DOM was the
primary carbon source for bacterioplankton. Results from other studies show that 15-90% o f
bacterioplankton productivity is dependent on allochthonous DOM in a variety o f lake
systems (Chrzanowski and Hubbard 1989; Arvola et. al. 1996; Jansson et. al. 1999). The
added nutrients in the nutrient enriched enclosures also supported bacterioplankton growth
either directly or indirectly through phytoplankton productivity, which is supported by results
from other research (Currie 1990; Vadstein et. al. 1993; Hessen et. al. 1994; Coveney and
Wetzel 1995; Jansson et. al. 1996).

The community respiration (R), GPP:R ratios, and GPP:BP ratios provided no clear
demarcation between autotrophy and allotrophy in the reference and nutrient enriched
enclosures. The community respiration (R) data were independent o f DOC concentration in
both the reference and nutrient enriched enclosures and did not support the p C O i data. ^CO]
is a direct measure o f the amount o f CO 2 in the lake enclosures, whereas community
respiration is based on short term incubations and this technique may not have been sensitive
enough to detect changes in DIC concentrations (Davies et. al. 2003).

The GPP;R and GPP:BP ratios did not show clear trends or relationships with DOC
concentration or nutrient enrichment. Most natural systems with high DOM concentrations
are not associated with high inorganic nutrient concentrations, which could result in high
variability and masking o f trends. In addition, the lack o f trends may be the result o f using
very different techniques to measure GPP and BP.

67

2.5.

Conclusion

The data from this paper show that an autotrophic-allotrophic gradient was established across
the DOM concentration gradient in the reference enclosures. Phytoplankton were co­
regulated by both solar irradiance and inorganic nutrient concentrations, whereas
bacterioplankton were strongly dependent on DOM concentration.

Autotrophic stimulation on the autotrophic-allotrophic gradient was achieved with nutrient
enrichment. However, GPP appeared limited by solar irradiance at high DOC concentrations
and BP maintained a strong dependence on DOC concentration. Taken together this suggests
that allotrophy dominates at DOC concentrations higher than investigated in this study,
regardless o f inorganic nutrient concentrations, which suggests that allotrophy is a
continuous function o f DOC resulting in a continuous distribution o f trophic states.

2.6.

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79

Table 2.1 Results o f significant simple regression models. DOC is DOC concentration (mg
L'^), Chla is chlorophyll a concentration (mg L'^), BB is bacterioplankton biomass (10^
mL'^),/?C0 2 is partial pressure o f C 0 2 (pM), ^ C O z is the difference between the
measured p C O i value and atmospheric equilibrium value (pM), DIC is DIC concentration
(pM), ÔDIC is the difference between the measured DIC value and DIC at atmospheric
equilibrium (pM), and BP is bacterioplankton produetivity (pg C L'^ h'^).

DV

Model

r'

P-value

n

Reference Enclosures
Chla

4.60(DOC) + 9 .5 8 x 10'^

0.81

0.009

6

BB

0.755(DOC) + 0.956

0.97

0 .0 0 0

6

pC O i

0.998(DOC) + 9.695

0.55

0.056

6

Ô pC 02

0.997(DOC) - 3.894

0.55

0.056

6

DIC

-8.03(DOC) + 123

0.95

0 .0 0 1

6

ÔDIC

0.998(DOC) - 3.90

0.55

0.056

6

Nutrient Enriched Enclosures
BP

0.192(DOC) + 2.67

0.74

0.017

6

;)C 0 2

0.289(DOC) + 2.63

0.72

0 .0 2 0

6

^CO z

0 .2 8 8 (D O C )-II.O

0.72

0 .0 2 1

6

DIC

-3.94(DOC) + 66.22

0 .8 8

0.004

6

ÔDIC

5.06(DOC) - 58.6

0.83

0.008

6

80

Canada

Ontario

•ELA

Figure 2.1. Map o f site loeation. Experimental Lakes Area, northwestern Ontario, Canada.

81

Reference Enclosures

35

42

55

60

11 4

Nutrient Enriched Enclosures

Figure 2.2. Schematic o f the lake enclosures used in this study. The values in each o f the
enclosures indicates the initial DOC concentration in mg L"\

82

1000

cdl

I

-

10000

-

1000

100

g

is
II
m

10

60
Xj
o

I

B

50
40
30
20

1

10

o o

.jjjSSSSSJSSiS^^

O

O

0
1 .0

Us
M

ta
in u

I
8

A

0 .8

bO

0 .6

U

0 .4

D

0 .2

1

o o

0 .0

6

10

12

D O C (m g l ‘)

Figure 2.3. Dependencies o f phytoplankton biomass, phytoplankton productivity, and
specific photosynthetic rate on DOC concentration and inorganic nutrient enrichment.
A. Chlorophyll a and phytoplankton biomass plotted on a log scale. B. Phytoplankton
productivity measured as gross primary productivity. C. Specific photosynthetic rate.
The open circles represent the reference enclosures and the closed circles represent the
nutrient enriched enclosures. The solid black line represents a significant regression at
P < 0.05. The grey dashed lines represent non-significant regressions.

83

10
-

70

9

Il
i

- 60

8
7

- 50

I«3 ^bû

40

î f

6

t

il

pp 'S

5
- 30

4
3

-

II

“

a

20

2
5
4
i

u
s 5p
a 3

It
*
m ^

3

2

1

£

0

2

4

6

8

10

12

D O C (m g L'^)

Figure 2.4. Dependencies o f bacterioplankton biomass and productivity on DOC
concentration and inorganic nutrient enrichment. A. Bacterioplankton abundance and
biomass. B. Bacterioplankton productivity. The open circles represent the reference
enclosures and the closed circles represent the nutrient emiched enclosures. The solid
black lines represent a significant regression at P < 0.05. The grey dashed lines
represent non-significant regressions.

84

25

20
15
o

10
5

0

10
5

0
O
U
c»

5

10
2

4

6

8

10

12

D O C (m gL-l)

Figure 2.5. Dependencies o f p C 0 2 concentrations on DOC concentration and inorganic
nutrient enrichment. A. Direct p C 0 2 measures. B. The change in p C O z as calculated as the
difference between the measured p C 0 2 value and the atmospheric equilibrium value. The
open circles represent the reference enclosures and the closed circles represent the nutrient
enriched enclosures. The solid black lines represent significant regressions at P < 0.05. The
long grey dashed lines represent non-significant regressions, the short grey dashed line
represents atmospheric equilibrium, and the long black dashed line at 6 mg L"' o f DOC
represents the shift from autotrophy to allotrophy.

85

110

100

u

o

-10

-4 0
-5 0

2

4

6

8

10

12

DOC (mg L-1)

Figure 2.6. Dependence o f DIC concentration on DOC concentration and inorganic nutrient
enrichment. A. DIC concentration. B. The change in DIC as calculated as the
difference between the measured DIC value and the atmospheric equilibrium value. The
open circles represent the reference enclosures and the closed circles represent the
nutrient enriched enclosures. The solid black lines represent significant regressions at P
< 0.05. The long grey dashed lines represent non-significant regressions, the short grey
dashed line represents atmospheric equilibrium, and the long black dashed line at 6 mg
L"' o f DOC represents the shift from autotrophy to allotrophy.

86

30 1

2

4

6

8

10

12

DOC (mg L'3

Figure 2.7. Dependence o f community respiration on DOC concentration and inorganic
nutrient enrichment. The open circles represent the reference enclosures and the closed
circles represent the nutrient enriched enclosures. The grey dashed lines represent non­
significant regressions.

87

3.0
2.5

2.0
0

::

3

0.5

0.0
80

8

10

12

DOC(m gL'l)
Figure 2.8. Dependencies o f GPP:R and GPP:BP ratios on DOC concentration and inorganic
nutrient enrichment. A. Gross phytoplankton productivity:community respiration ratios.
B. Gross phytoplankton productivityibacterioplankton productivity ratios. The open
circles represent the reference enclosures and the closed circles represent the nutrient
enriched enclosures. The grey dashed lines represent non-significant regressions.

88

3. Element Ratios of Sediments Produced from DOM and
inorganic Nutrient Dependent Scavenging

3.1.

Introduction

Autotrophic and allotrophic lakes differ based on the primary energy source, the microbial
metabolism that drives the system, and nutrient utilization by the microbial community
(Jones 1992; del Giorgio and Peters 1994; Jones 1998; Jansson 1998). Autotrophic lake
microbial metabolism is driven by phytoplankton productivity based on solar irradiance,
whereas allotrophic lake microbial metabolism is driven by bacterioplankton productivity
based on allochthonous dissolved organic matter (DOM) (Currie 1990; Jansson et. al. 2000).
These differences in energy source and metabolism result in differences in nutrient cycling
(Sterner et. al. 1997; Sterner et. al. 1998).

Investigating biogeochemical processes may help to distinguish between autotrophic and
allotrophic lakes (Sterner et. al. 1992; Elser et. al. 1995). Biogeochem ical processes involve
the transfer o f energy and nutrients between living and non-living components. The primary
components o f a lake include dissolved nutrients, the seston, and the sediments. Elemental
stoichiometry is a method that can provide a better understanding o f food web and nutrient
cycling dynamics in autotrophic and allotrophic lakes by relating the energy and nutrient
requirements o f organisms to the element ratios o f their environment (Sterner et. al. 1998;
Elser et. al. 1998; Elser et. al. 2000c).

The most common element ratios are C:N, C:P, and N:P because carbon, nitrogen, and
phosphorus are important in cell growth and metabolism (Elser et. al. 2000a; Sterner and

89

Elser 2002). The distribution o f C, N, and P among components and the flux between
components w ill differ between autotrophic and allotrophic lakes and can be expressed by
element ratios. Comparison o f element ratios provides a measure o f organic matter quality
and nutrient availability to biota and can reflect the balance among C, N, and P scavenged
from the water column (Redfield 1958; Elser et. al. 2000a; Elser et. al. 2000c; Sterner and
Elser 2002; Hessen et. al. 2003). For example, the Redfield ratio (C:N = 6 .6 , C:P = 106, N:P
= 16) represents the optimal element ratio for marine phytoplankton (Redfield 1958).
Freshwater phytoplankton ratios are typically higher, and more variable than marine
phytoplankton (Elser and Hassett 1994; Sterner et. al. 1997; Elser et. al. 2000b), but the
Redfield ratio can serve as a useful comparison to lake seston ratios (Buffle and De Vitre
1994). Comparison o f the seston and sediment ratios can provide insight into metabolic and
scavenging processes occurring within the water column o f a lake (Elser and Foster 1998;
Elser et. al. 2000c; Hakanson and Jansson 2002).

Sediments are formed through scavenging o f dissolved nutrients, such as dissolved organic
carbon (DOC), nitrogen, and phosphorus, from the water column and the settling o f particles.
Nutrient scavenging can occur in three ways (Santschi 1988): 1. incorporation, 2. adsorption,
and 3. coagulation. Incorporation involves the assimilation o f nutrients by biota to generate
biomass. Nutrients can also adsorb onto particles and coagulation occurs between small
particles that combine to form larger particles. The fates o f scavenged nutrients include
remineralization into the dissolved inorganic pool, reincorporation into biomass, or settling
out o f the water column to form sediments.

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The objective o f this study was to investigate nutrient cycling dynamics as a function o f
DOM and inorganic nutrient coneentrations. To meet this objective four null hypotheses
were tested: 1 . scavenging o f carbon, nitrogen, and phosphorus from the water column is
independent o f DOC concentration; 2. scavenging o f carbon, nitrogen, and phosphorus from
the water column is independent o f nutrient enrichment; 3. element sediment ratios are
independent o f DOC concentration; and 4. element sediment ratios are independent o f
nutrient enrichment. Rejection o f these hypothesis w ill support the suggestion that
autotrophic and allotrophic lakes exists along the same continuum as opposed to existing as
discrete trophic states (Fig 1.1).

These hypotheses were tested by studying the DOM dependence o f nutrient scavenging from
the water column and the DOM dependence o f the element ratios o f the sediments formed
during a lake enclosure experiment. Scavenging was calculated as the difference between
initial and final concentrations in the water column, element ratios were calculated for the
dissolved, seston, and sediments, and a mass balance was calculated relative to phosphorus
because it is the conservative element among the three.

3.2.

Methods

3 .2 .1 . Site Description
This study was conducted at the Experimental Lakes Area (ELA) in northwestern Ontario,
Canada (93°30’-94°00’W, 49°30’-49°45’N)(Fig. 3.1). The area ranges in elevation from 360
m to 380 m above sea level and is located on the south western region o f the Precambrian
Shield. The soils are poorly developed and underlain by granite, glacial sands, and gravels.

91

The vegetation is primarily boreal subclimax forest consisting o f jack pine (P in u s
b a n k sia n a ), black spruce (P ic e a m a ria n a ), trembling aspen (P o p u lu s tre m u lo id e s), and white

birch (B etu la p a p y r ife r d ). The ELA mean annual temperatures range from 0.5 °C to 2.2 °C ,
and the annual precipitation ranges from 500 mm to 750 mm (Brunskill and Schindler 1971;
Curtis and Schindler 1997). The lakes involved in this study were Lake 224 and Lake 225
and were chosen primarily because Lake 224 and Lake 225 represent the most extreme DOC
concentrations o f all active ELA lakes and, therefore, would provide an adequate DOC
concentration gradient. Furthermore, Lake 225 flows directly into Lake 224 making these
lakes hydrologically linked. Lake 224 has a surface area o f 25.9 ha, a drainage area o f 97.5
ha, and a mean depth o f 11.59 m. Lake 225 has a surface area o f 5.6 ha and a drainage area
o f 30.5 ha (Curtis and Schindler 1997).

3.2.2. Enclosures
Twelve, closed-bottom lake enclosures were randomized along a floating linear wooden
frame, and they were set up in Lake 224 from July to September 2002. The surface area and
depths o f each enclosures was 0.84 m^ and 1.5 m, respectively. DOM concentration
gradients were established in 2 sets o f 6 enclosures by pumping water from Lake 224 and
Lake 225 into the enclosures in approximately 0%, 20%, 40%, 60%, 80%, and 100%
proportions (relative to Lake 225)(Fig 3.2). These proportions represent an autotrophicallotrophic gradient (Chapter 2). Plankton were readily transferred into the lake enclosures
during pumping, but it is unlikely fish were transferred and none were observed in the lake
enclosures.

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One set o f enclosures acted as a reference (referred hereafter as reference enclosures), and
the other set was enriched with inorganic nutrients (referred hereafter as nutrient enriched
enclosures) to test the effects o f autotrophic stimulation on microbial biomass and
productivity along an autotrophic-allotrophie gradient. The nutrient enriched enclosures
were enriched with NaNOa and KH 2 PO 4 at the beginning o f the experiment and again 4
weeks later. The total amount o f nitrogen and phosphorus added to the enclosures was 4500
mg N and 300 m g P, which elevated the concentrations by factors o f 10 and 7, respectively
(Table 3.1).

3.2.3. Sample Collection and Preparation
Depth integrated water samples were collected w eekly from each o f the enclosures using a
1.5 m tube sampler and a bucket. Following each sample collection day, the enclosures were
mixed with an oar. Samples were taken from the integrated sample for water chemistry
analyses in 500 mL polyethylene bottles. From these samples, 100 mL aliquots were filtered
through pre-ashed Whatman GF/C glass fibre filters, and then the filters were frozen for
seston carbon, seston nitrogen, and seston phosphorus. The filtrate was stored for dissolved
organic carbon (DOC; an analytical measure o f DOM), total dissolved nitrogen (TDN)
analyses, and total dissolved phosphorus (TDP) analyses. A ll water samples collected were
stored and shipped under refrigeration.

Non-quantitative sediment samples were collected from each o f the enclosures at the end o f
the experiment and then frozen. The fi*ozen sediment samples were freeze dried using a
Labconco Freeze Dry System/Freezone 4.5 and then homogenized using a mortar and pestle.

93

3.2.4. Sample Analyses
3.2.4.1. Dissolved Organic Carbon
Filtered sample water was analysed for dissolved organic carbon (DOC) using a Shimadzu
TOC-5000A Total Organic Carbon Analyzer with a detection limit o f 0.05 mg L '\ A 40 mL
sample was acidified with 200 pL o f select grade HCl and sparged for 7 mins with oxygen to
volatilize and strip inorganic carbon from the sample. The sample was combusted to carbon
dioxide and measured with an infrared detector. This instrument was operated with a 2%
coefficient o f variation according to the instruction manual.

3.2.4 2. Total Dissolved Nitrogen
Total dissolved nitrogen (TDN) concentrations were measured on filtered samples using a
Shimadzu TNM-1 Total Nitrogen Analyzer with a detection limit o f 0.06 mg L '\ Samples
were combusted to nitrogen monoxide and nitrogen dioxide and then reacted with ozone to
create an excited state o f nitrogen dioxide. A chemiluminescence detector measured the light
emitted when the nitrogen dioxide returned to ground state.

3.2.4 3. Total Dissolved Phosphorus
Total dissolved phosphorus (TDP) concentrations were measured on filtered samples using
the persulphate digestion and ascorbic acid methods (Greenberg, Clesceri, and Eaton 1992).
The samples were digested with persulphate for 1 hr in an autoclave and then analysed on a
Milton R oy Spectrophotometer using a 5 cm pathlength. Sample absorbance was measured
at 885 nm. The detection limit o f this method is 0.01 mg L '\

94

3.2AA. Seston and Sediment C, N, and P
Carbon (C) and nitrogen (N) concentrations o f the seston and sediment were analysed by a
PerkinElmer Series I I 2400 C H N S/0 Elemental Analyzer following the instruction manual.
The detection limit o f this method is 0.01 mg L'* for nitrogen and 0.11 mg L'* for carbon.
Seston and sediment samples analyzed for phosphorus (P) were pre-ashed and then digested
in 0.01 N HCl for 2 hrs at 85 °C . A suhsample o f the digested sample was diluted and
analyzed for phosphorus following the ascorbic acid method (Greenberg, Clesceri, and Baton
1992). The sample was analysed on a Milton Roy Speetrophotometer using a 5 cm
pathlength and absorbance was measured at 885 nm. The detection limit o f this method is
0.01 mg L '\

3.2.5. C, N, and P Scavenging
Scavenging o f C, N , and P from the water column was determined as the difference between
the initial and final measures. The initial nitrogen and phosphorus values included dissolved,
seston, and precipitation data, and the final values included the dissolved and seston data.
The initial and final organic carbon data included the dissolved and seston data. The
concentrations o f C, N, and P were converted to a total mass for the entire water column o f
the enclosures.

3.2.6. Mass Balance
Conservative estimates o f sediment generated in the enclosures were calculated from
phosphoms. Phosphorus is a non-volatile substance, therefore, it was assumed that the
amount o f phosphorus lost from the water column was gained in the sediments. Total carbon
and nitrogen concentrations in the sediments were calculated from this conservative estimate
o f sediment formed in the enclosures. Concentrations o f nitrogen and phosphorus in the

95

precipitation that fell during the experiment were also incorporated into the mass balance
(Table 3.1). Gains and losses o f gaseous carbon and nitrogen were not measured directly, but
based on the water column and sediment data, the amount o f C and N lost or gained to the
system could be determined. The mass balance was calculated using the following equation:

^

= [i^ di + ^ s i +

+ ^ se d )J

Eq. 3.1

where, Xdi is the initial mass o f dissolved C, N, or P; Xg, is the initial mass o f seston
C, N , or P; X& is the mass o f N or P from precipitation and or from added nutrients; Xdf is the
final mass o f dissolved C, N, or P; Xgf is the final mass o f seston C, N , or P; Xged is the mass
o f C, N, or P in the sediments.

3.2.7. Mass Transfer Coefficient and % Retention
The mass transfer coefficients were calculated to represent the rate at which the C, N , and P
were removed from the water column.

^sed

Axt

fr l
where, Xged is the total mass o f C, N, or P in the sediments (mg), A is the area o f the
enclosures (0.84 m^), t is the length o f time o f the experiment (61 days), and [Xj] is the initial
concentration o f C, N, or P in the water column o f the enclosures (mg m'^).

Percent retention was calculated to represent the proportion o f C, N , or P retained in the
sediments relative to the initial mass in the water column. However, C and N have volatile

96

States and, therefore, this retention does not account for exchanges with the atmosphere. The
% retention o f C, N , and P were calculated using the following equation:

sed

Eq. 3.2

xlOO%

X,

where, Xsed is the total mass o f C, N, or P in the sediments (mg) and X, is the initial
mass o f C, N, or P in the water column o f the enclosures (mg).

3.2.8. Element Ratios
Element ratios o f C:N, C:P, and N:P were calculated for dissolved, seston, and sediment
carbon, nitrogen, and phosphorus. The element ratio is calculated by dividing mass by the
appropriate molecular weight.

3.2.9. Statistical Analyses
A ll dependent variable data were integrated over the course o f the experiment and expressed
as a time weight average using the following equation (Eq 3.3):

(to + y i )

w

k -^ o ) +
y VV

k

( t „-i + T „ ) '

- ^ 1)
y

w

where, y is the measured parameter from day 0 to day n in cumulative days, and x is
the cumulative number o f days since the beginning o f the experiment from day 0 to day 61.

97

The initial DOC concentration for the enclosures was used as the independent variable and
the reference and nutrient enrichment treatments were fixed factors. Data were analysed
using simple regression analyses with SPSS 8.0 and assessed using an alpha value o f 0.05.
Simple regression analyses were used to determine the DOM dependence o f the measured
parameters and to compare between the reference and nutrient enriched enclosures. The
regression coefficients (slope and y-intercepts) were compared between the reference and
nutrient enriched enclosures to see i f they were significantly different using a homogeneity o f
regression analysis. The homogeneity o f regression analysis also determined whether the
initial DOC concentration in the enclosures was a significant covariate. Equal slopes
between the reference and nutrient enriched enclosures and DOC concentration as a covariate
allowed an ANCOVA to be performed. ANCOVA removed the effects o f the DOC
covariate and assessed whether nutrient enrichment significantly affected the measured
parameter. M ANOVA tested the effects o f nutrient enrichment on the measured parameters
that were independent o f DOM concentration.

3.3.

Results

3.3.1. C, N, and P Enclosure Concentrations
3.3.1.1. Dissolved
The initial DOC concentrations in both the reference and nutrient enriched enclosures ranged
fi-om 3.6 mg L"' to 11.4 mg L '\ The time weighted average TDN concentrations ranged
from 0.18 mg L'^ to 0.34 mg U ' in the reference enclosures and ranged from 2.16 mg L'^ to
2.77 mg L'^ in the nutrient enriched enclosures. The time weighted average TDP
concentrations were at or below the detection limit o f 0 . 0 1 mg L'^ in the reference enclosures

98

and ranged from 0.05 mg L'^ to 0.12 mg L'* in the nutrient enriched enclosures (Table 3.2).
The total initial mass o f the dissolved C, N , and P in the enclosures is shown in Table 3.1.

3.3.1.2. Seston
The time weighted average seston carbon concentrations ranged from 0.17 mg L'^ to 0.75 mg
L'^ in the reference enclosures and ranged from 0.93 m g L"' to 1.48 mg L'* in the nutrient
enriched enclosures. The time weighted average seston nitrogen concentrations ranged from
0.02 mg L'^ to 0.10 mg L"' in the reference enclosures and ranged from 0.14 mg L'* to 0.24
mg L'^ in the nutrient enriched enclosures. The time weighted average seston phosphorus
concentrations were at or below the detection limit o f 0 . 0 1 mg L'^ in the reference enclosures
and ranged from 0.05 mg L'^ to 0.08 mg L"' in the nutrient enriched enclosures (Table 3.2).
The total initial mass o f the seston C, N , and P in the enclosures is shown in Table 3.1.

3.3.1.3. Sediments
The sediment carbon concentrations ranged from 340 mg g'^ to 370 mg g'^ in the reference
enclosures and ranged from 430 mg g'^ to 490 mg g'^ in the nutrient enriched enclosures.
The sediment nitrogen concentrations ranged from 26 mg g'^ to 30 mg g'^ in the reference
enclosures and ranged from 43 m g g'^ to 62 mg g'^ in the nutrient enriched enclosures. The
sediment phosphorus concentrations ranged from 0.34 mg g'* to 0.89 mg g"' in the reference
enclosures and ranged from 1.5 mg g'^ to 6.1 mg g'^ in the nutrient enriched enclosures
(Table 3.2).

99

3.3.2. C, N, and P Scavenging
3.3.2.1. Carbon
The change in total carhon (ôTC) in the water column o f the lake enclosures showed that
carbon was gained in all enclosures except at high DOC concentrations in the reference
enclosures (Fig 3.3A). The 8 TC increased with increasing DOC concentration in the
reference enclosures, hut this regression was non-significant (P > 0.05), which supports
hypothesis one. The 5TC ranged from -1900 m g to 820 mg in the reference enelosures. The
5TC depended directly on DOC concentration in the nutrient enriched enclosures (r^ - 0.82;
P < 0.01)(Tahle 3.3) and ranged from -5300 mg to -1100 mg, which were significantly
greater increases in carhon than in the reference enclosures (P < 0.001) and does not support
hypothesis two. Nutrient enrichment explained 78% o f the variation in ÔTC values adjusted
for covariate effects o f DOC concentration between the two sets o f enclosures (P < 0.001).
The two regression lines would converge at approximately 14 mg L'^ o f DOC (Fig 3.3A).

The total mass o f carhon sedimentation in the reference enclosures was independent o f DOC
concentration and ranged from 1300 mg to 6300 mg (Fig 3.4A). The mass o f carbon
sedimentation in the nutrient enriched enclosures was directly dependent on DOC
concentration (r^ = 0.70; P < 0.05)(Tahle 3.3) and ranged from 26000 mg to 79000 mg. The
mass transfer coefficients o f carbon ranged from 4.2 mm d'^ to 27 mm d'^ in the reference
enclosures and ranged from 87 mm d"' to 190 mm d'^ in the nutrient enriched enclosures
(Table 3.4). The proportion o f carbon retained in the sediments ranged from 17% to 110% in
the reference enclosures and ranged from 350% to 790% in the nutrient enriched enclosures
(Table 3.4).

100

3.S.2.2. Nitrogen
The change in total nitrogen (ôTN) in the water column o f the lake enclosures showed that
nitrogen was scavenged detectahly from all o f the reference and nutrient enriched enclosures
except one (Fig 3.3 B). The ôTN was independent o f DOC concentration in the reference
enclosures and ranged from -5 .0 mg to 250 mg, which supports hypothesis one. The 5TN
was inversely dependent on DOC concentration in the nutrient enriched enclosures (r^ = 0.77;
P < 0.05)(Table 3.3) and ranged from 3200 mg to 4700 mg. More nitrogen was scavenged
from the water columns in the nutrient enriched enclosures than in the reference enclosures
(P < 0.001), which does not support hypothesis two.

The total mass o f nitrogen sedimentation in the reference enclosures was independent o f
DOC concentration and ranged from 110 mg to 520 mg. The mass o f nitrogen sedimentation
in the nutrient enriched enclosures increased with increasing DOC concentration in the
nutrient enriched enclosures, but this regression was non-significant (P > 0.05)(Fig 3.4B).
The total nitrogen sedimentation ranged from 3300 mg to 7900 mg in the nutrient enriched
enclosures and was greater than sedimentation in the reference enclosures (P < 0.001). The
mass transfer coefficients o f nitrogen ranged from 0.63 mm d'^ to 2.8 mm d"' in the reference
enclosures and from 14 mm d'^ to 31 mm d'* in the nutrient enriched enclosures (Table 3.4).
The proportion o f nitrogen retained in the sediments ranged from 2.6% to 12% in the
reference enclosures and ranged from 56% to 120% in the nutrient enriched enclosures
(Table 3.4).

101

3.3.2.S. Phosphorus
The change in total phosphoms (ôTP) in the water column o f the lake enclosures showed that
phosphoms was scavenged from all o f the reference and nutrient enriched enclosures. The
ÔTP depended directly on DOC concentration in the reference enclosures (r^ = 0.59; P <
0.05)(Table 3.3) and ranged from 2.3 mg to 11 mg, which does not support hypothesis one.
The ÔTP decreased with increasing DOC concentration in the nutrient enriched enclosures,
but this regression was non-significant (P > 0.05)(Fig 3.3C). The ÔTP ranged from 230 mg
to 370 mg in the nutrient enriched enclosures and more phosphoms was scavenged from the
water columns in the nutrient enriched enclosures than in the reference enclosures (P <
0 .0 0 1 ), which does not support hypothesis two.

The total mass o f phosphoms sedimentation in the reference enclosures depended on DOC
concentration in the reference enclosures (r^ = 0.59; P < 0.05)(Table 3.3) and ranged from 2.3
m g to 11 mg. The mass o f phosphoms sedimentation decreased with increasing DOC
concentration in the nutrient enriched enclosures, but this regression was non-significant (P >
0.05)(Fig 3.4C). The total phosphoms sedimentation in the nutrient enriched enclosures
ranged from 230 mg to 370 mg, which was greater than the phosphoms sedimentation in the
reference enclosures (P < 0.001). The mass transfer coefficients o f phosphoms ranged from
0.20 mm d'^ to 0.94 mm d'^ in the reference enclosures and from 16 mm d“' to 23 mm d'* in
the nutrient enriched enclosures (Table 3.4). The proportion o f phosphoms retained in the
sediments ranged from 0.83% to 3.8% in the reference enclosures and ranged from 54% to
84% in the nutrient enriched enclosures (Table 3.4).

102

3.S.2.4. Mass Balance
Phosphoms is a conservative substance with no volatile state, therefore, phosphoms was
neither lost nor gained from the lake enclosures. Thus, the phosphoms scavenged from the
water column was sedimented, and it was used to calculate the carbon and nitrogen mass
balances.

The carbon mass balance showed that carbon was gained in all o f the lake enclosures (Fig
3.5 A). The carbon mass balance was independent o f DOC concentration in the reference
enclosures ranging from 2300 mg ± 3900 mg to 6800 mg ± 28000 mg. The error associated
with the reference enclosures was high and suggests that carbon could have been either
gained or lost from these enclosures. The carbon mass balance in the nutrient enriched
enclosures depended on DOC concentration (r^ = 0.62; P < 0.05)(Table 3.3) and ranged from
29000 mg ± 5400 mg to 79000 mg ± 15000 mg. The amount o f carbon gained in the nutrient
emiched enelosures was one order o f magnitude greater that the amount o f carbon gained in
the reference enclosures.

The nitrogen mass balance showed that nitrogen was gained in all o f the enclosures except
three (Fig 3.5B). The nitrogen mass balance was independent o f DOC concentration in the
reference enclosures, but dependent on DOC concentration in the nutrient enriched
enclosures (r^ = 0.71; P < 0.05)(Table 3.3). The total gain in nitrogen ranged from -2 2 0 mg
± 380 mg to 290 mg ± 320 mg in the reference enclosures and ranged from -1 1 0 0 mg ± 240
mg to 4700 mg ± 1100 m g in the nutrient enriched enclosures. The amount o f nitrogen
gained at high DOC concentrations in the nutrient enriched enclosures was one order o f

103

magnitude greater that the amount o f nitrogen gained at high DOC concentrations in the
reference enclosures.

3.3.3. C:N, C:P, N:P Element Ratios
3.3.3.1. Dissolved Element Ratios
The dissolved C:N element ratios o f the water column in the reference and nutrient enriched
enclosures both depended on DOC concentration and ranged from 26 to 38 in the reference
enclosures and from 2.7 to 5.2 in the nutrient enriched enclosures (r^ = 0.91, 0.94,
respectively; P < 0.01)(Fig 3.6A)(Table 3.3). The C:N ratios o f the water column o f the
nutrient enriched enclosures were significantly lower than the C:N ratios in the reference
enclosures (P < 0.001).

The dissolved C:P element ratios o f the water column in the reference enclosures directly
depended on DOC concentration and ranged from 950 to 2600 (r^ = 0.99; P < 0.001)(Table
3.3). The C:P ratios were independent o f DOC concentration in the nutrient enriched
enclosures and ranged from 240 to 450 (Fig 3.6B)

The dissolved N:P element ratios o f the water column in the reference enclosures depended
on DOC concentration and ranged from 36 to 69 (r^ = 0.99; P < 0.001)(Table 3.3). The N:P
ratios decreased with increasing DOC concentration in the nutrient enriched enclosures, but
the regression was non-significant (P > 0.05)(Fig 3.6C). The dissolved N;P ratios in the
nutrient enriched enclosures ranged from 62 to 160.

104

3.3.3.2. Seston Element Ratios
The seston C:N element ratios were independent o f DOC concentration in both the reference
and nutrient enriched enclosures (Fig 3.7A). Seston C:N ratios ranged from 7.9 to 11 in the
reference enclosures and tfom 6.8 to 7.9 in the nutrient enriched enclosures.

The seston C:P and N:P element ratios depended on DOC concentration (r^ = 0.74, 0.69,
respectively; P < 0.05)(Table 3.3) in the reference enclosures and ranged from 43 to 164 and
from 5.6 to 19, respectively. The C;P and N:P ratios were independent o f DOC
concentration in the nutrient enriched enclosures and ranged from 42 to 56 and from 5.3 to
8.1, respectively (Fig 3.7).

3.3.3.3. Sediment Element Ratios
The sediment C:N element ratios decreased with increasing DOC concentration in the
reference enclosures (Fig 3.8A), but the regression was non-significant (P > 0.05), which
supports hypothesis one. The C:N ratios o f the sediments ranged from 14 to 16 in the
reference enclosures. The C:N ratios directly depended on DOC concentration in the nutrient
enriched enclosures (r^ = 0.63; P < 0.05) (Table 3.3) and ranged from 8.9 to 12, which were
significantly lower than the reference enclosure ratios (P < 0.001) and does not support
hypothesis two.

The sediment C:P and N:P element ratios decreased with increasing DOC concentration in
the reference enclosures (Fig 3.8), but the regressions were non-significant (P > 0.05), which
supports hypothesis one. The sediment C:P and N:P ratios in the reference enclosures ranged
from 980 to 2800 and from 64 to 180, respectively. The C:P and N:P ratios were directly

105

dependent on DOC concentration in the nutrient enriched enclosures (r^ = 0.78, 0.77,
respectively; P < 0.05)(Table 3.3) and ranged from 190 to 730 and from 22 to 63,
respectively, which were significantly lower than the reference ratios (P < 0.01) and does not
support hypothesis two.

The regression models o f the sediment C:N, C:P, and N:P element ratios in the reference and
nutrient enriched enclosures would all converge at a DOC concentration range between 14
mg L'* and 16 mg L'^ (Fig 3.8).

3.4.

Discussion

3.4.1. C, N, and P Scavenging
Carbon (C) and nitrogen (N) scavenging under low nutrient conditions in the reference
enclosures were independent o f DOC concentration, which supports hypothesis one.
Phosphoms (P) scavenging was dependent on DOC concentration and does not support
hypothesis one. This suggests that either more P was scavenged from the water column at
higher DOC concentrations or different scavenging mechanisms are affecting the different
elements.

Nutrient recycling within the water column by biota (biota includes zooplankton,
phytoplankton, and bacterioplankton) was an important mechanism preventing scavenging o f
nutrients to sediments in the reference enclosures. Results from another study showed that
recycled nutrients were an important source o f nutrients to both phytoplankton and
bacterioplankton (Sterner et. al. 1995). Scavenging o f C, N , and P from the water columns

106

o f the reference enclosures was low compared to the nutrient enriched enclosures, which was
consistent with the low mass transfer coefficients and proportions retained in the sediments
as w ell as the low concentrations o f C, N, and P deposited in the sediments o f the reference
enclosures.

Scavenging o f C, N, and P in the nutrient enriched enclosures was greater than the reference
enclosures. The higher mass transfer coefficients in the nutrient enriched enclosures suggest
that C, N, and P were rapidly scavenged from the water columns and deposited in the
sediments o f the nutrient enriched enclosures resulting in a higher proportion retained than in
the reference enclosures. These results suggest that nutrient scavenging and nutrient
sedimentation were greater with eutrophication and autotrophy in the nutrient enriched
enclosures. Results from another study reported greater annual sedimentation o f organic
carbon, nitrogen, and phosphorus fi'om a eutrophic lake than from a mesotrophic lake in
Switzerland (Bloesch et. al. 1977).

The carbon and nitrogen mass balances in the reference enclosures indicate net positive gains
in C and N, but were independent o f the autotrophic-allotrophie gradient established in the
reference enclosures (Chapter 2). The excess carbon and nitrogen were likely from
atmospheric sources and sequestered from the atmosphere to drive photosynthesis (Schindler
1977; Carpenter et. al. 2001). Data presented previously (Chapter 2) suggested that the
reference enclosures at high DOC concentrations were net CO2 producers, which does not
directly support the result that C and N were sequestered for photosynthesis. However,
phytoplankton productivity in the reference enclosures was limited by inorganic nutrients and

107

D ie concentrations were low (<100 |xM), therefore, it is possible that phytoplankton needed
atmospheric C and N for photosynthesis. An additional explanation for the observed C and
N sequestering in the reference enclosures is that w e could not detect the mass balance
changes at these levels due to the large errors associated with the mass balance. Phosphorus
occurred in lower concentrations than carbon or nitrogen in the reference enclosures, and
resulted in large errors when the mass balance was calculated (see Fig 3.5).

Net positive gains in earbon and nitrogen were observed in the mass balance o f the nutrient
enriched enclosures and indicate that carbon and nitrogen were sequestered from the
atmosphere. C and N scavenging to the sediments likely resulted in sequestering from the
atmosphere for photosynthesis by phytoplankton (Schindler 1977; Carpenter et. al. 2001).

3.4.2. Element Ratios as Indicators of Processes
The element ratios o f DOM in the reference enclosures indicate that the organic matter was
nutrient-poor. The element ratios o f the water eolumn in the reference enclosures were
extremely nutrient-deficient relative to the seston suggesting that biota rapidly incorporated
and recycled nitrogen and phosphorus into biomass in the water column, thereby removing
most o f the nutrients from the dissolved pool (Tezuka 1990; Currie 1990; Elser et. al. 1995).
The element ratios in the nutrient enriched enclosures showed that the dissolved organic
matter in the water columns was nutrient-rich. The dissolved organic matter element ratios
indicate that the water column was likely a stable source o f nutrients to biota (Elser and
George 1993).

108

The nutrient-rich seston ratios in hoth the reference and nutrient enriched enclosures suggest
that incorporation was the primary scavenging mechanism o f C, N , and P. This conclusion is
supported by results from another study that looked at fifteen lakes ranging in trophic status,
which found seston C:N ratios that ranged from 6 to 13 to represent phytoplankton (Baines
and Pace 1994). Seston element ratios in the enclosures were similar to the Redfield ratio
(C:N = 6.6, C:P = 106, N:P = 16) and to ratios representing biota as reported in the literature,
therefore, these seston ratios likely reflected biotic ratios (Uehlinger and Bloesch 1987;
Hochstadter 2000). The seston ratios deviated from the Redfield ratio at high DOC
concentrations in the reference enclosures and were probably the result o f the high element
ratios o f the dissolved organic matter in the water column. Other researchers have also found
no relationship between seston ratios and trophic state (Uehlinger and Bloesch 1987) because
similar seston ratios may actually be a product o f different growth rates under different
environmental conditions. For example, phytoplankton grow slow ly under high solar
irradiance, and they exhibit low C:P ratios (Xenopoulos et. al. 2002). Phytoplankton can also
have low C:P ratios when growth rate and P concentrations are high (Hochstadter 2000).

The sediment element ratios typically became more enriched in nitrogen and phosphorus at
high DOC concentrations in the reference enclosures, which does not support hypothesis
three. This result suggests that more nitrogen and phosphorus were scavenged from the
water column at higher DOC concentrations, which was supported by the phosphorus
scavenging data. The nitrogen scavenging data did not support this conclusion directly, but
the mass balance indicated that atmospheric sequestering occurred and the scavenging
calculation did not account for atmospheric fluxes. Results from other studies using lake

109

enclosures at the ELA showed that DOM can either decrease or increase scavenging o f trace
metals from aquatic systems (Santschi 1988; Curtis 1993).

Although scavenging likely occurred in the reference enclosures by incorporation, the high
element ratios o f the sediments suggested that the nutrients were not readily scavenged into
sediments. Therefore, a nutrient-poor water column produced nutrient-rich seston and
nutrient-deficient sediments, which indicates that nutrient recycling in the water column o f
the reference enclosures was more efficient than in the nutrient enriched enclosures (Currie
1990; Kroer 1993; del Giorgio and Peters 1993; Sterner et. al. 1995; Cotner and Biddanda
2002). This result is in contrast to results from another study o f 20 temperate lakes,
representing a wide trophic gradient, that found that lower P concentrations did not result in
higher nutrient cycling efficiency (Hudson et. al. 1999).

Scavenging in the nutrient enriched enclosures was likely dominated by incorporation by
biota based on the nutrient-rich seston ratios. Less nutrient recycling occurred in the water
column o f the nutrient enriched enclosures producing nutrient-rich sediments. Furthermore,
the higher mass transfer coefficients and nutrient retention in the sediments suggests that
biotic sedimentation rates were higher under eutrophic conditions in the nutrient enriched
enclosures, resulting in nutrient-enriched sediments, which is supported by results from other
studies (Bloesch et. al. 1977; del Giorgio and Peters 1993). Another study has shown that
sedimentation o f primary productivity is less in eutrophic systems, but the relative amounts
lost to the sediments from eutrophic systems as compared to oligotrophic systems were 5
times higher, producing low C;N ratios in the sediments (Baines and Pace 1994).

110

3.4.3. Autotrophy-Allotrophy Convergence
DOC concentrations greater than 14 mg L'^ would likely result in allotrophy, regardless o f
inorganic nutrient coneentrations. Autotrophy was observed in the nutrient enriehed
enclosures across the DOC eoncentration gradient (Chapter 2), but a common convergence,
at approximately 14 m g L '\ was observed in the change in total earbon o f the water column
(ÔTC) and the sediment element ratios. Furthermore, these convergences are consistent with
the interpretation o f the DlC eoneentration convergence observed at approximately 14 m g L'*
o f DOC (Chapter 2). At the eonvergenee point, inorganie nutrient concentrations had no
effeet on ÔTC or on the element ratios o f the sediments. Furthermore, the 6TC and sediment
element ratio values resemble the values predieted under low nutrient conditions in the
reference enclosures. Therefore, these results suggest that DOC concentration can be a
primary driver o f nutrient cyeling dynamics (Currie 1990; Sterner et. al. 1992; Chrzanowski
et. al. 1996; Sterner et. al. 1997; Chrzanowski and Grover 2001). More importantly, these
transitions to allotrophy further indicate that dystrophy is a continuous function o f DOC
concentration rather than a discrete trophie state (Fig 1.1).

3.5.

Conclusions

Seston element ratios indicated that incorporation by biota was likely an important C, N, and
P seavenging mechanism in the reference enclosures, but the sediment element ratios indicate
that the nutrients were retained within the water columns under low nutrient conditions.
Therefore, nutrient seavenging and subsequent sedimentation in the reference enclosures was
limited by efficient biotic incorporation and recycling along the autotrophic-allotrophie
gradient.

Ill

The autotrophic stimulation o f the autotrophic-allotrophie gradient resulted in greater
scavenging than observed in the reference enclosures and nutrient-enriched sediments.
Carbon, nitrogen, and phosphorus were effectively scavenged from the water column by
incorporation into biomass followed by rapid sedimentation. However, nutrient enrichment
o f water having DOC concentrations higher than used in this experiment would likely not
stimulate an autotrophic response. Thus, allotrophy is likely a continuous function o f DOC
concentration and, therefore, dystrophy is not a discrete trophic state.

3.6.

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del Giorgio, P. A. and R. H. Peters. 1993. Balance between phytoplankton production and
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Elser, J. J., T. H. Chrzanowski, R. W. Sterner, J. H. Schampel, and D. K. Foster. 1995.
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Elser, J. J., T. H. Chrzanowski, R. W. Sterner, and K. H. Mills. 1998. Stoichiometric
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Elser, J. J., R. W. Sterner, E. Gorokhova, W. F. Fagan, T. A. Markow, J. B. Cotner, J. F.
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Elser, J. J., R. W. Sterner, A. E. Galford, T. H. Chrzanowski, D. L. Findlay, K. H. M ills, M.
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Hessen, D. O., T. Andersen, P. Brettum, and B. A. Faafeng. 2003. Phytoplankton
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Hochstadter, S. 2000. Seasonal changes o f C:P ratios o f seston, bacteria, phytoplankton and
zooplankton is a deep, mesohumic lake. Freshwater Biology. 44: 453-463.

Hudson, J. J., W. D. Taylor, and D. W. Schindler. 1999. Plankton nutrient regeneration and
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Jansson, M. 1998. Nutrient limitation and bacteria - phytoplankton interactions in humic
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Jansson, M., A. K. Bergstrom, P. Blomqvist, and S. Drakare. 2000. Allochthonous organic

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Jones, R. I. 1992. The influence o f humic substances on lacustrine planktonic food chains.
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Jones, R.I. 1998. Phytoplankton, primary production and nutrient cycling, p. 145-175. In
D.O. Hessen and L.J. Tranvik [eds.], Aquatic Humic Substances: Ecology and
Biogeochemistry. Springer-Verlag.

Kroer, N. 1993. Bacterial growth efficiency on natural dissolved organic matter. Limnology
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Redfield, A. C. 1958. The biological control o f chemical factors in the environment.
American Scientist. 46: 205-221.

Santschi, P. H. 1988. Factors controlling the biogeochemieal cycles o f trace elements in fresh
and coastal marine waters as revealed by artificial radioisotopes. Limnology and
Oceanography. 33: 848-866.

Schindler, D. W. 1977. Evolution o f phosphorus limitation in lakes. Science. 195: 260-262.

Sterner, R. W. and J. J. Elser. 2002. Ecological Stoichiometry: The B iology o f Elements
from Molecules to the Biosphere. Princeton University Press.

Sterner, R. W., J. J. Elser, and D. O. Hessen. 1992. Stoichiometric relationships among
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Sterner, R. W., T. H. Chrzanowski, J. J. Elser, andN . B. George. 1995. Sourees o f nitrogen
and phosphorus supporting the growth o f bacterio- and phytoplankton in an oligotrophic
Canadian shield lake. Limnology and Oceanography. 40: 242-249.

Sterner, R. W., J. J. Elser, E. J. Fee, S. J. Guildford, and T. H. Chrzanowski. 1997. The
light:nutrient ratio in lakes: The balance o f energy and materials affects ecosystem structure
and process. The American Naturalist. 150: 663-684.

Sterner, R. W., J. Clasen, W. Lampert, and T. W eisse. 1998. Carbon: phosphorus
stoichiometry and food chain production. E cology Letters. 1: 146-150.

Tezuka, Y. 1990. Bacterial regeneration o f ammonium and phosphate as affected by the
carbon : nitrogen : phosphorus ratio o f organic substrates. Microbial Ecology. 19: 227-238.

Uehlinger, U. and J. Bloesch. 1987. Variation in the C:P ratio o f suspended and settling
seston and its significance for P uptake calculations. Freshwater Biology. 17: 99-108.

Xenopoulos, M. A., P. C. Frost, and J. J. Elser. 2002. Joint effects o f U V radiation and
phosphoms supply on algal growth rate and elemental composition. Ecology. 83: 423-435.

117

Table 3.1 Initial total mass o f each component contributing carbon, nitrogen, and
phosphorus. Nadd and Padd are the total mass o f N and P added to the nutrient enriched
enclosures. H alf o f the total mass was added July 13, 2002 and the other h alf was added
August 2 2 ,2 0 0 2 . Nppt and Pppt are the total mass o f N and P contributed to the enclosures
from precipitation during the experiment.

DOC Seston C TON
(mg)
(mg)
(mg)

4600
5600
7200
7800
10000
14000
4400
5300
6900
7500
9400
14000

29
77
31
510
440
990
31
150
410
220
570
1000

Seston N
(mg)

Seston P
(mg)

Padd
(mg)

Pppt
(mg)

2500
2200
2000
2400
2500
2200

Reference Enclosures
51
n/a
180
110
180
72
n/a
86
180
20
n/a
66
140
n/a
180
94
180
130
n/a
78
210
n/a
180
41

45
63
76
94
100
130

n/a
n/a
n/a
n/a
n/a
n/a

5.5
5.5
5.5
5.5
5.5
5.5

220
210
380
270
310
420

Nutrient Enriched Enclosures
39
4500
180
13
72
4500
180
13
180
4500
13
89
180
76
4500
13
110
4500
180
13
180
190
4500
13

13
13
13
13
15
21

300
300
300
300
300
300

5.5
5.5
5.5
5.5
5.5
5.5

Nadd
(mg)

Nppt
(mg)

TDP
(mg)

118

Table 3.2 Concentrations o f carbon, nitrogen, and phosphorus in the dissolved water
column, in the seston, and in the sediments. Values o f TON, TDP, and Seston C, N , and P
are time weighted averages.

Initial
TDN
TDP
Seston C Seston N Seston P Sediment
DOC (mg L ') (mg L ') (mg L"') (mg L'^) (mg L"')
C
(mg L ')
(mg g ')

Sediment
N
(mg g ')

Sediment
P
(mg g ')

370

29

370
340

27
26

0.40
0.34
0.89
0.64
0.49

Reference Enclosures
3.48
4.22

0.18
0.19

0.01

0.06

0.01

5.50

0.21

5.98
7.47
11.41

0.24
0.26
0.34

0.19

0.03
0.04

<0.01
<0.01

0.01

0.27

0.05

<0.01

0.01

0.06
0.04

<0.01
<0.01

370

0.01

0.27
0.17

350

30
27

0.01

0.68

0.11

0.01

360

30

0.63
4.5

Nutrient Enriched Enclosures
3.67
4.48

2.25

0.05
0.07

5.75

2.17

6.24
8.04
11.32

2.34

OjW

0.05
0.05

440
480

57
62

4.8

0.06

1.25
1.06

0.16
0.24
0.19

0.06

460

59

6.1

2.50

0.08

1.38

0.26

0.08

470

61

4.4

2.64
2.77

0.09
0.12

1.47
0.87

0.27
0.17

0.07
0.06

490
430

61
43

3.4
1.5

119

Table 3.3 Results o f significant simple regression models. DOC is DOC concentration (mg
L-1); ÔTC, ÔTN, and ÔTP are the change in total concentration in the water column (mg);
Dissolved C:N, C:P, N:P are element ratios from dissolved C, N, and P in the water
column; Sediment C, N , and P are the total amount deposited in the sediments (mg).

DV

Model

r2

P-value

n

Reference Enclosures
ÔTP

0.889(DOC) + 0.511

0.59

0.045

6

Sediment P

0.889(DOC) + 0.511

0.59

0.045

6

Dissolved C:N

1.58(DOC) + 21.3

0.91

0.002

6

Dissolved C:P

214(DOC) + 192

0.99

0.000

6

Dissolved N;P

4.12(DOC) + 22.3

0.99

0.000

6

Seston C:P

14.1(D 0C ) - 24.9

0.74

0.018

6

Seston N;P

1.61(D 0C ) + 1.46

0.68

0.026

6

Nutrient Enriched Enclosures
ÔTC

608(DOC) - 7460

&82

0.008

6

ÔTN

-184(D 0C ) + 4790

0.77

0.013

6

Sediment C

4980(DOC) + 6870

0.70

0.024

6

C Mass Balance

4370(DOC) + 14300

0.62

0.038

6

N Mass Balance

588(DOC) - 2650

0.71

0.023

6

Dissolved C:N

0.303(DOC) + 1.72

0.94

0.001

6

Sediment C:N

0.371 (DOC) + 7.06

0,63

0.037

6

Sediment C:P

64.0(DOC) - 75.5

&78

0.013

6

Sediment N:P

4 .87(D 0C ) + 3.14

0.77

0.014

6

120

Table 3.4 Carbon, nitrogen, and phosphorus mass transfer coefficients (MTC) (mm d'^) and
percent sediment retention.

Initial DOC

CM TC

(mg L'*)

%C

NM TC

Retention

%N
Retention

PM T C

%P
Retention

Reference Enclosures

148

2Z3

918

1.8

7.3

0.37

1.5

4.22

27.5

111.8

10.5

0.48

2.0

5.50

7.0

216

2.6
&89

0.48

2.0

198

4.2

17.3

0.63

3.6
2.6

0.20

0.8

7.47

14.5

S&2

2.6

10.4

0.70

2.9

11.41

10.1

41.1

2.8

11.5

0.94

3.8

Nutrient Enriched Enclosures
3.67

202

718.9

19

67.7

23

83.2

4.48

156

546.2

18

64.0

22

76.4

5.75

88

307.2

14

47.6

21

73.2

6.24

115

407.3

19

68.0

21

72.7

8.04

139

500.0

28

101.2

23

83.7

11.32

127

426.0

31

102.6

16

54.0

121

Canada

Figure 3.1. Map o f site location. Experimental Lakes Area, northwestern Ontario, Canada.

122

Reference Enclosures

; ' 1 1
180 m gN
5.5 mgP

42

55 J
1

60

4

114

\

Nutrient Enriched Enclosures

i ' l l
180 m gN
5.5 mg P

Figure 3.2. Schematic o f the lake enclosures used in this study. The values in each o f the
enclosures indicates the initial DOC concentration in mg
The contribution o f N
and P from precipitation and the amount o f added N and P are also shown.

123

1000
0
-1000
-2000
-3000
-4000
-5000
5000
4000
M

3000

2000
1000
0

issssa»

400

I
PL,

300

200

H

to

100
0
8

10

12

D O C (m g L'^)

Figure 3.3. Carbon, nitrogen, and phosphorus scavenging (initial - final) dependence on
DOC concentration. A. The change in total carbon in the water eolumn (6TC). B. The
change in total nitrogen in the water column (ôTN). C. The change in total phosphorus
in the water column (5TP). The open circles represent the reference enclosures and the
closed circles represent the nutrient enriched enclosures. The solid black lines represent
a significant regression at P < 0.05. The long grey dashed lines represent non­
significant regressions. The short grey dashed lines represent the zero or no change
value.

124

&
u

1
0)

c/3

80000
70000
60000
50000
40000
30000
20000
10000
0

&

<L>
C/3

•O

8000
7000
6000
5000
4000
3000
2000
1000
0

B

400
M)
Ph

......

300

i

200

a

100
0

-O O 0 0

=0-

& -r

8

10

12

DOC (mg U^)

Figure 3.4. Sediment earbon, nitrogen, and phosphorus dependenee on DOC eoneentration.
A. Sediment earhon (mg). B. Sediment nitrogen (mg). C. Sediment phosphorus (mg).
The open eireles represent the referenee enelosures and the closed circles represent the
nutrient enriched enelosures. The solid hlaek line represents a significant regression at
P < 0.05. The grey dashed lines represent non-significant regressions

125

100000
80000 "S
B

GOOOO -

^
o

40000 ■

% 20000

-

U

-20000

■

6000 1
5000 ^

4000 -

^

3000 ■

S
00

2000 -

I

1000 -

°

-1000

-

-2000
2

4

6

8

10

12

D O C ( m g L ')

Figure 3.5. Carbon and nitrogen mass balances (the gain or loss from the water column o f
the lake enclosures) and DOC concentration dependence plotted with absolute errors
calculated with a 95% confidence. A. Carbon (mg). B. Nitrogen (mg). The open
circles represent the reference enclosures and the closed circles represent the nutrient
enriched enclosures. The solid black line represents a significant regression at P < 0.05.
The long grey dashed lines represent non-significant regressions. The short grey dashed
lines represent the zero or no change value.

126

40
35
30
25
20

15
10

5
2500
2000
1500
PLh
ü

1000

500
160
140
%
0

1
eu

%

120
100

80
60
40
6

8

10

12

DOC (mg L'^)

Figure 3.6. DOC dependence o f dissolved water eolumn element ratios. A. C:N element
ratios. B. C:P element ratios. C. N:P element ratios. The open circles represent the
referenee enclosures and the closed circles represent the nutrient enriched enclosures.
The solid black lines represent a significant regression at P < 0.05. The grey dashed
lines represent non-significant regressions.

127

w

I
%

u

12
11
10
9

o

8

c>

o

4

6

o

7
6

5
4

l/l

%

S
pLn

Ü

w

I
PU|

%

160
140
120
100
80
60
40
18
16
14
12
10
8
6

2

8

10

12

DOC(mgL’^)
Figure 3.7. DOC dependence o f seston element ratios. A. C:N element ratios. B. C:P
element ratios. C. N:P element ratios. The open circles represent the reference
enclosures and the closed circles represent the nutrient enriched enclosures. The solid
hlack lines represent a significant regression at P < 0.05. The grey dashed lines
represent non-significant regressions.

128

18
16
M
O

14

0^

12

U

10

O
O

8

6

3000 1
2500

O

1000 ■

500
200
150
100

10

12

DOC(mgL')
Figure 3.8. DOC dependence o f sediment element ratios. A. C:N element ratios. B. C:P
element ratios. C. N:P element ratios. The open circles represent the reference
enelosures and the closed circles represent the nutrient enriched enelosures. The solid
black lines represent a significant regression at P < 0.05. The grey dashed lines
represent non-significant regressions.

129

4. Summary and Conclusions
Autotrophic lakes dominate our understanding o f food web and nutrient eycling dynamics,
whereas allotrophic lakes are far less understood, but they may represent a greater proportion
o f North American temperate lakes (Currie 1990; Cole et. al. 1994; Kirchman 1994).
Autotrophic and allotrophic lakes differ with respect to the microbial metabolism that drives
the system and the way nutrients are utilized (Jones 1992; Jansson 1998; Jansson et. al. 2000;
Hakanson and Jansson 2002). D issolved organic matter (DOM) and its ability to attenuate
light and complex inorganic nutrients appears to be the primary mechanisms that differentiate
these lake types (Jackson and Hecky 1980; de Haan et. al. 1990; Jones 1992; Shaw 1994;
Scully and Lean 1994; Morris et. al. 1995; Bukaveckas and Robbins-Forbes 2000).
Therefore, the objective o f this research was to investigate the dependencies o f food web and
nutrient cycling dynamics on DOM and inorganic nutrients using lake enclosures.

The food web and nutrient cycling dynamics in the reference and nutrient enriched
enclosures differed with DOM concentration and nutrient enrichment. A shift from
autotrophic to allotrophic was observed in the reference enclosures across the DOM
concentration gradient at approximately 6 mg L'^ o f DOC, whereas autotrophy dominated in
the nutrient enriched enclosures for all DOM concentrations.

Phytoplankton were likely light and nutrient limited in the referenee enclosures and,
therefore, bacterioplankton could outcompete phytoplankton for available nutrient
concentrations. Bacterioplankton could also effectively access additional nutrients to drive
productivity through the decomposition o f organic matter. DOM stimulated bacterioplankton

130

growth by acting as a source o f both carbon and nutrients. Furthermore, nutrients were
recycled rapidly within the water column o f the reference enclosures by biota resulting in
nutrient deficient sediments.

Phytoplankton were the dominant producers in the nutrient enriched enclosures. Nutrient
enrichment stimulated both phytoplankton and bacterioplankton growth, but bacterioplankton
also depended on phytoplankton for labile autochthonous DOM production. High biomass
turnover rates o f both phytoplankton and bacterioplankton and rapid settling resulted in high
retention o f carbon, nitrogen, and phosphorus in the sediments. Sediments then acted as a
source o f nutrients to the water column.

Allotrophy likely becom es the dominant trophic state at DOM concentrations greater than the
gradient established in this lake enclosure experiment, regardless o f inorganic nutrient
enrichment. Despite the food web and nutrient cycling differences observed in this study,
DOM concentration becomes the primary factor regulating the dynamics at concentrations
above 14 m g L '\ Phytoplankton become limited by availability o f solar irradiance and
possibly inorganic carbon availability at high DOM concentrations. In contrast,
bacterioplankton maintained a strong dependence on DOM in the nutrient enriched
enclosures. Thus, the transition to allotrophy is a continuous function o f DOC concentration,
which supports the suggestion that dystrophy is not a discrete trophic state as previous
thought (Fig 1.1). Therefore, most lakes likely fall along a continuous distribution o f trophic
states that are a function o f DOC and nutrient concentrations (Fig 4.1).

131

4.1.

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133

Allotrophy

14

Autotrophy

High

Low
Nutrients

Figure 4.1. Revised autotrophy-allotrophy continuum graph.

134