integrating landscape carbon cycling: research needs for resolving organic carbon budgets of lakes

Integrating Landscape CarbonCycling: Research Needs

for Resolving Organic CarbonBudgets of Lakes

Paul C. Hanson,1* Michael L. Pace,2 Stephen R. Carpenter,1

Jonathan J. Cole,3 and Emily H. Stanley1

1Center for Limnology, University of Wisconsin, 680 N Park St, Madison, Wisconsin 53706, USA; 2Department of EnvironmentalSciences, University of Virginia, Charlottesville, Virginia 22904, USA; 3Cary Institute of Ecosystem Studies, Millbrook

New York 12545, USA

ABSTRACT

Based on empirical and synthetic research, lakes

make, store, and mineralize organic carbon (OC) at

rates that are significant and relevant to regional

and global carbon budgets. Although some global-

scale studies have examined specific processes such

as carbon burial and CO2 exchange with the

atmosphere, most studies of lake carbon cycling are

from single systems, focus only on a specific habi-

tat, and do not account for all of the major terms in

OC budgets. Hence, most lake OC budgets are

incomplete, leaving some key processes highly

uncertain. To advance the analysis of the role of the

inland waters in C-cycling, ecosystem science

needs a new generation of studies that confront

these shortcomings. Here we address research

needs and priorities for improving OC budgets. We

present ten key research questions and recommend

a framework for essential ecosystem-scale studies

of lake OC cycling. Answers to these ten questions

will not only improve carbon budgets but also

provide robust estimates of lake contributions to

global and regional carbon cycling. In addition,

studies of lake carbon budgets will provide relative

autochthonous and allochthonous carbon fluxes,

indicate sources and rates of carbon burial, improve

quantification of lake-atmosphere carbon ex-

changes, better integrate lakes with terrestrial and

lotic carbon dynamics, promote understanding of

how climate and land-use change will impact lakes,

and enable tests of ecological theory related to

subsidies and food web stability.

Key words: organic carbon; lake; budget;

reservoir; ecosystem; carbon cycling.

INTRODUCTION

Lakes are important sites for organic carbon (OC)

storage in sediments and for transfer of CO2 to the

atmosphere with annual global fluxes to these

reservoirs of petagrams of carbon (Cole and others

2007; Tranvik and others 2009; Raymond and

others 2013). The importance of lakes in OC cycling

has sparked arguments for revising the global C

cycle budget to explicitly include inland waters

(Battin and others 2009; Regnier and others 2013).

However, a dearth of complete, ecosystem-scale

budgets for lake OC creates uncertainty and limits

Received 28 May 2014; accepted 4 October 2014

Author contributions PCH, MLP, SRC, JJC, and EHS conceived of the

review and wrote the manuscript.

*Corresponding author; e-mail: [email protected]

EcosystemsDOI: 10.1007/s10021-014-9826-9

2014 Springer Science+Business Media New York

C-cycling assessments. Partly as a result, dissonant

views have emerged about both the processing of

catchment OC in lakes and the consequences of

catchment load for lake processes. For example,

although lakes store large quantities of OC (Stallard

1998; Einsele 2001), they also tend to be sources of

CO2 to the atmosphere (Cole and others 1994;

Sobek and others 2003; Roehm and others 2009);

the euphotic zone of a given lake may be net

autotrophic (Hanson and others 2003), whereas

the lake as a whole may be net heterotrophic

(Hanson and others 2004); the particulate fraction

of water column OC pool may be both of allo-

chthonous and autochthonous origin, whereas the

dissolved fraction is primarily allochthonous (Wil-

kinson and others 2013b); allochthonous OC is

assimilated by aquatic heterotrophs (Pace and

others 2004), but the extent of this assimilation and

whether or not it represents a subsidy to consumer

production is debated (Jones and others 2012; Cole

2013; Kelly and others 2014).

The complexity of OC cycling relates to lakes

dual roles as ecosystems that both fix inorganic

carbon (IC) through photosynthesis and mineralize

OC derived from both autochthonous and allo-

chthonous sources (Figure 1). OC inputs to lakes

arise from surface water, ground water, and

atmospheric deposition whereas OC losses are via

outflow and burial (Likens and others 1977;

Saunders 1980) (Figure 1). OC is created and de-

stroyed within lakes via the processes of primary

production, respiration, and photolysis. The bal-

ance of these processes along with input and out-

puts of IC determine whether there is net uptake or

net loss of CO2 relative to the atmosphere (Fig-

ure 1). Key problems in understanding lake OC

budgets are parsing autochthonous and allochtho-

nous sources, resolving spatial heterogeneity and

temporal dynamics in inputs and transformation,

and measuring critical processes such as burial of

OC at temporal scales suitable for resolving annual

budgets. Additionally, a critical problem is sepa-

rating the effects of processes such as sedimenta-

tion, resuspension, secondary production, and

heterotrophic respiration on allochthonous versus

autochthonous OC (Hanson and others 2011).

Current understanding of ecosystem-scale OC

budgets in lakes is remarkably incomplete. Al-

though the individual components of lake OC

budgets are often measured, rarely are all compo-

nents measured, and as a result, only a few lakes

have complete budgets (for example, Likens 1985;

Cole and others 1989; Wetzel 2001). By complete

budget, we mean measures of: (1) the major allo-

chthonous inputs from surface water, groundwa-

ter, and atmospheric deposition; (2) losses due to

outflow, sediment burial, and (3) autochthonous

primary production and ecosystem respiration.

These are the minimum fluxes needed for OC

budgets to place lakes in a larger landscape context.

A depiction of this type of budget is presented in

Hanson and others (2014, see Figure 1).

The methods used to estimate key OC fluxes in

lakes are diverse. In Table 1, we show examples for

the major components of lake OC budgets and the

associated fluxes. These methods are in common

use for lakes; however, rarely, if at all, are all the

techniques applied to a single system. If only some

terms are measured when compiling a budget, the

unmeasured terms are sometimes calculated by

difference and/or estimated based on prior studies.

Scaling from rate estimates made under highly

controlled conditions to ecosystems is a problem for

many methods. For example, bottle incubations

used for estimating lake metabolism have been

supplanted in many research programs by free-

water dissolved gas methods, which provide for

higher-frequency and more continuous sampling

protocols (Staehr and others 2010). As a conse-

quence, more metabolism estimates are available

for a greater variety of lake conditions, providing

opportunities to better understand controls over

these important fluxes in OC budgets (Solomon

and others 2013). In general, the advent of perva-

sive sensing techniques has begun to provide large

volumes of data relevant to estimating physical and

biological processes relevant to OC fluxes (Porter

and others 2009). Similar opportunities arise from

satellite remote sensing, which may provide

empirically based estimates of OC concentration

across broad geographies (Kutser and others 2005),

and stable isotopes, which allow for partitioning

OC between allochthonous and autochthonous

sources (Wilkinson and others 2013b). However,

with new technologies, managing, using, and

interpreting the extensive data are often difficult

and require new approaches (Porter and others

2011). Data analysis and management need to be

addressed before new measurements can be fully

incorporated into models of OC cycling. Applying

these observations to ecosystem-scale processes

requires integrative models that have not yet been

fully developed.

Given the limited number of complete OC lake

budgets, comparisons across a range of climate and

landscape conditions are currently limited. Further,

lack of complete budgets makes it difficult to de-

velop, calibrate, and compare general models of OC

dynamics. Ultimately, uncertainties related to OC

budgets, and models thereof, limit robust assess-

P. C. Hanson and others

Fig

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Balancing the OC Budget

ments of lakes in regional, continental or global C

cycles. For example, although there are global

estimates of CO2 fluxes from lakes to the atmo-

sphere (for example, Raymond and others 2013)

and of burial in sediments (Dean and Gorham

1998; Stallard 1998), these are not constrained by

similar estimates of inputs and other outputs.

Many factors make it difficult or expensive to

gather complete OC budgets for lakes. Inputs of

OC can be highly variable in time, with seasonal

or weather-related peaks that are difficult to

measure (Caverly and others 2013; Dhillon and

Inamdar 2013). In addition, diffuse inputs from

heterogeneous wetland and upland soils may be

difficult to measure (Hanson and others 2014).

Internal processes, such as primary production

and respiration, are also heterogeneous in space

and over annual cycles (Staehr and Sand-Jensen

2007; Van De Bogert and others 2007; Hoellein

and others 2013; Solomon and others 2013).

Heterogeneity in lake morphology and the physi-

cal structure and chemical composition of sedi-

ments also complicates estimation of OC storage in

sediments (Dean and Gorham 1998; Kortelainen

and others 2004; Kastowski and others 2011;

Ferland and others 2012). Nonetheless, with

appropriate sampling all of these problems can be

overcome and indeed have been overcome in

some studies. Thus, it is possible to develop the

network of OC budgets to understand variability

among lakes and the role of lakes in landscape C

cycles (Hanson and others 2014). In addition,

modern sensors enhance the opportunity to

overcome past measurement limitations and thus

make possible a new era of research.

Here, we provide a framework for advancing

understanding and quantification of lake OC cy-

cling. First, we review a few examples of lake car-

bon budgets that indicate the diversity of potential

OC loads and fates. We then pose ten questions

intended to guide research that ultimately will lead

to better estimates of OC loads to lakes, fluxes of C

between lakes and the atmosphere (source-

strength), and estimates of the long-term OC stor-

age (sink-strength) in lakes. Successful research in

these areas will result in more comprehensive

understanding of lake C-cycling, important insights

about OC cycling and aquatic food webs, and

opportunities for better integration of lakes in re-

gional and global carbon cycle analyses.

Table 1. Common Methods for Estimating OC Budget Components

OC budget component Flux Method Q

Import Precipitation Precipitation collector followed by chemical analysis 1

Dry deposition Surface trap followed by chemical analysis 1

Surface water flow Gaging station, event sampler, chemical analysis 1

Groundwater flow Seepage meter, piezometer, tracers (isotopes, unique

gases)

1

Internal process GPP Bottle incubations, radiocarbon or dissolved oxygen

Free-water dissolved oxygen, CO2 or pH 2

Ecosystem respiration,

including photo-oxidation

Bottle incubations, dissolved oxygen 5

Free-water dissolved oxygen, CO2 or pH 2, 5

Autotroph respiration Physiological studies, models 5

Heterotroph respiration Microbial metabolism studies, models 5

Generation and respiration of DOC Bottle experiments, physiological studies, stable

isotope tracers

7, 8

Fates of terrestrial OC Bottle experiments, stable isotope tracers 3

Sedimentation Sediment traps 6

Export Loss of CH4/CO2 to atmosphere Aqueous concentrations and gas exchange coefficient 2

Floating chambers with CO2 and other gas sensors

Surface water flow Gaging station, surface water chemistry

Groundwater flow Seepage meter, piezometer

Burial Dated sediment cores 6

The questions for which the methods are particularly relevant are identified in Q. Three questions depend on knowing most of the fluxes in the table: 4, 9, 10. In addition,there can be predation fluxes that are inputs or outputs. For example some fish actively seek and eat terrestrial prey. Anglers or ospreys remove OC when they harvest fish. Thesefluxes are probably small in comparison to the overall OC budget and are not included here.


Example Carbon Budgets

Figure 2 contrasts approximate OC budgets for five

example lakes with broad differences in area,

hydrologic residence time, and trophic state.

Although other budgets exist, this collection of

lakes indicates the diversity of relative load sources.

For example, oligotrophic Mirror Lake receives

nearly equal allochthonous inputs from surface

water (fluvial), groundwater, and atmospheric

sources, whereas Ortrasket, Dickie, and Donghu

lakes have allochthonous loads dominated by fluvial

inputs and Crystal Lake has no fluvial inputs

(Figure 2). Although allochthonous loads vary by

almost two orders of magnitude, the inclusion of NPP

reduces the range in OC inputs (inclusive of allo-

chthonous and autochthonous) to about one order

of magnitude (Figure 2). Emitted CO2 and fluvial

losses are major outputs for most lakes, whereas

methane emissions are a minor loss (Figure 2).

Burial is also an important fate with relative impor-

tance being >50% in oligotrophic Crystal Lake and

eutrophic Lake Donghu (Figure 2). The budgets in

Figure 2 do not illustrate the large internal fluxes of

OC due to gross primary production and autotrophic

respiration. The former flux leads to the production

of autochthonous OC, whereas the latter flux

(autotrophic respiration) destroys primarily autoch-

thonous OC (accounting for the possibility of some

heterotrophy by primary producers which is usually

a minor flux). The difference between these two

metabolic processes, is NPP and is depicted as a load

(new input) in Figure 2. It is important to note,

however, that both heterotrophic respiration and

photo-oxidation (combined for brevity as R), min-

eralize all sources of OC, including NPP. Therefore,

R is a fate. As we describe below, there are few lakes

where internal OC cycling is integrated with external

inputs and losses providing a full description of the

major OC budget fluxes.

Ten Unanswered Questions About LakeOC Budgets

There are many research fronts that need to be

addressed to advance our understanding of lake OC

cycling (Figure 3). We group these loosely into

major components of the OC governing equation

(Figure 1)inputs, outputs, and within-lake pro-

cessesand then place them within the context of

changing climate and land use. Advancing on these

fronts will require a variety of approaches, includ-

ing long-term observations, cross-lake compari-

sons, process measurements, and modeling studies.

Lakes at the Interface (Inputs, Outputs)

Q1: What are the Allochthonous Loads to Lakes,How are They Partitioned Among Sources, and Howare Loads Driven by Events? For many lakes,

Figure 2. Approximate OC budgets for five example

lakes with broad differences in area, hydrologic residence

time (RT), and trophic state. Loads are simplified as in-

flow from surface water, atmospheric (for example, leaf

litter), net primary production (NPP), and other, such as

precipitation and groundwater. The respiration wedge

includes microbial respiration and photo-oxidation.

Animal movements may add and remove organic matter,

and we have assumed that the net flux is small. Fates are

assumed to equal loads, and exploded terms in the

budgets are not included in the respective studies, but are

approximated by proportion from data from similar lakes

and are estimates for the purpose of illustration only. For

example, most budgets do not include NPP as a source or

methane (CH4) efflux as a fate. High DOC lakes (A) have

high inputs and short residence times. Smaller lakes with

long residence times (B) tend to have substantial pro-

portion of inputs as atmospheric, whereas lakes with

shorter residence times (CE) have large fluvial inputs.

Little is known about overall balance in E eutrophic

lakes. Sources: 1Jonsson and others (2001), 2Hanson and

others (2014) and NPP from North Temperate Lakes

LTER database, 3Likens (1985), 4Dillon and Molot

(1997), 5Yang and others (2008) (values include OC and

IC); NPP for Dickie and Donghu lakes estimated from

Wetzel (2001) values for mesotrophic and eutrophic

lakes, respectively.


fluvial loads are the dominant OC flux (for exam-

ple, Figure 2A, C, D, E). Because surface-waters in

many catchments are flashy, loading curves (hys-

teretic relationships of loads with the rise and fall of

hydrographic fluxes) need to be well characterized

(Lambert and others 2013). Loading curves, how-

ever, may shift as a function of antecedent condi-

tions such as recent floods or droughts. Changes in

land use and climate may alter loading relation-

ships. Further, loading curves may not capture

episodic inputs such as extreme storms where a few

hours or days may account for most of the annual

load. If these events are missed then the load is

underestimated. Depending on load pathways,

more intensive measurements may be required to

capture episodes of high loading or new methods

may need to be developed.

For atmospheric inputs, methods for estimating

load as a function of vegetation type and proximity

would be useful. Although some atmospheric loads

have been measured for lakes (Gasith and Hasler

1976; Preston and others 2008), more extensive

studies of atmospheric inputs to streams indicate a

wide range of loads (Hanson and others 2014, and

references therein). In small lakes with a large

perimeter to area ratio, this flux may prove espe-

cially important as is the case for OC inputs in

relatively small Crystal and Mirror lakes (Fig-

ure 2B, C).

Groundwater that passes through organic-rich

soils may pick up substantial DOC just before

entering aquatic ecosystems (Schindler and Krab-

benhoft 1998). Depending on lake hydrology, these

relatively diffuse input sources are difficult to ob-

serve directly, and add substantial uncertainty to

load estimates. Accounting for groundwater loads,

especially in flowpaths that are shallow or that pass

through adjacent wetlands, is a primary need for

OC budget closure and comparison. Full hydrology

(that is, a complete water budget) is rarely included

Figure 3. Balancing the lake OC budget will require addressing a number of research fronts using a variety of approaches

(Carpenter 1998). Long-term observations and cross-lake comparisons will provide contrasts representative of important

gradients and will be more valuable if they involve complete budgets. Process rate studies need to consider non-linear

events, such as storm-driven transport as well as gas fluxes and other phenomena affecting OC degradation. Modeling will

enable estimation of key unknowns, quantification of sensitivities and uncertainties that will inform further observational

studies, and balancing budgets at multiple time scales. Advancing on these research fronts will require collaboration

among multiple disciplines and will result in better integration of lake ecosystems in global carbon budgets.


explicitly in lake OC budgets mainly because of the

difficulty in measuring groundwater flux (but see

Winter and Likens 2009; Hanson and others 2014).

Q2: How does Control over Gas Exchange Vary byLake and What are the Underlying Physical FactorsGoverning the Differences? Mineralization ofOC to CO2 is a dominant fate in many lakes

(Figure 2AD), leading to net efflux of CO2 to the

atmosphere when the concentration is supersatu-

rated (Cole and others 1994). Fluxes to the atmo-

sphere are estimated from gas partial pressures and

the atmospheric exchange piston velocity (k).

Improving understanding and calculation of gas

exchange requires application of modern methods

in physical limnology in a broad range of lakes. For

example, the main control of k likely shifts from

convective- to wind-driven dominance as lake area

increases (Read and others 2012). Data typically

used in estimating gas exchange are partial pres-

sures of gas within the lake water column; how-

ever, gas partial pressures are driven by a variety of

processes, including metabolism, internal mixing

and advection, chemical conditions, as well as gas

exchange. The consequences of other variables for

k are not yet well quantified. Hence, partial pres-

sure data need to be supplemented with other

observations, such as floating chamber or eddy

covariance techniques to better evaluate alterna-

tive gas exchange models for k (MacIntyre and

others 2010; Vachon and others 2010; Huotari and

others 2011). Improved measures of gas exchange

would reduce uncertainties and constrain the rest

of the carbon budget.

Q3: How Does the Source of Allochthonous OC Thatis Loaded (That is, Fluvial OC, Leaf Fall, PeatPore Water, and So on) Determine Its Fate inLakes? Differing materials degrade at differingrates. Most studies of lakes are restricted to studies of

the degradation of bulk surface water DOC (but see

Gudasz and others 2012). In controlled laboratory

experiments these rates vary by about 20-fold

(Hanson and others 2011). Applying these DOC loss

rates to OC budgets is problematic, because lakes

have heterogeneous light and temperature, which

are two key drivers of degradation. Exposure of OC

to conditions that promote or inhibit degradation

will depend in part on mixing patterns and residence

times, as well as the particle size and molecular

weight (Amon and Benner 1996). Furthermore, the

presence of more labile forms of OC has been found

to enhance mineralization of refractory OC (Hotch-

kiss and others 2014), suggesting interactions that

may confound simplifying assumptions of first order

decay rates for OC mineralization. Additional study

of how differing materials degrade under these

varying conditions is warranted. One approach to

better understanding degradation rates is studying

lakes that span large gradients in environmental

conditions as well as the types of OC loads. Extensive

parallel work in lotic and coastal marine ecosystems

should serve as a guide for the most effective ap-

proaches (Tank and others 2010; Fichot and Benner

2014).

Internal Cycling and Lakes as Sinks (Within-Lake Pro-

cesses)

Q4: Do the Estimated Fates for Allochthonous OCMatch Estimates of External Loads? Addressingthis question will require quantifying the fates (or

sinks) of OC as mineralization, export down-

stream, storage in sediments, and incorporation

into the food web. There are a number of proxies

for these fates. For mineralization, studies tend to

track changes in metabolic gases (dissolved O2 and

CO2) (Staehr and others 2010). However, rarely are

these dissolved gases observed and modeled

throughout the ecosystem (for example, including

surface-waters, deep waters, and sediments) as well

as through time (for example, including all sea-

sons). CO2 emission from lakes has been used as an

index of allochthonous C load (Cole and others

1994; Sobek and others 2003; Roehm and others

2009), but this approach is incomplete because the

relative fractions of IC and OC in the load are not

accounted for (Striegl and others 2001; Hanson and

others 2004; McDonald and others 2013). More-

over, without the export and burial terms to com-

plete the suite of sinks, fates cannot be allocated to

check for balance with measured loads. Differences

in precision among measurements for the sinks

influence interpretation as well. For example, dis-

solved gases are relatively easy to measure at short-

time scales during ice-free seasons with automated

instruments (Staehr and others 2010). As a result,

there are many estimates for rates of primary pro-

duction and respiration (that is, metabolism).

Contrast the data available for metabolism with

sparse measurements of permanent burial in sedi-

ments. Long-term burial rates are estimated from

sediment cores; however, because of a lack of

precision, it is difficult to quantify burial at rela-

tively short-time scales. Thus, quantifying sinks

is scale-dependent. Studies of OC budgets should

strive to reconcile inputs with outputs in the con-

text of both short (seasonal to annual) and long


(decadal to century) time scales to analyze the

balance between load and the various fates of al-

lochthonous OC.

Q5: What are OC Respiration Rates for Lake Ecosys-tems? There are estimates of open water respira-tion for a large number of lakes (Pace and Prairie

2005; Solomon and others 2013). Recent studies

have also synthesized old observations and pre-

sented new observations of sediment respiration

especially in relation to temperature (Gudasz and

others 2012; Cardoso and others 2014). Neverthe-

less, it is difficult to determine whole-lake respira-

tion of OC because few studies include all lake

depths (for example, mixed layer and hypolimnion)

and habitats (for example, open water and littoral

zone). Further studies are needed to differentiate

respiration of autochthonous and allochthonous

OC, determine how allochthonous OC sources

influence respiration, and understand how physical

factors, such as sunlight and temperature, alter

respiration as well as photolysis. Temperature scal-

ing of respiration is a special case, because predic-

tions through thermal strata, seasons, and under

changing climate are based on these relationships.

One recommendation is to estimate respiration

across a wide temperature range, both within and

between ecosystems. Respiration may also have an

important spatial component (Van de Bogert and

others 2012). Additionally, estimates of respiration

would benefit from synoptic measurements in

multiple habitats during stratified periods. These

could be confined to mixed surface layer. The

hypolimnion, which tends to be more stable and

absent of primary productivity in most lakes, could

be characterized by fewer measurements through

time. Although there are measures of hypolimnetic

oxygen deficits for a number of lakes including

some multi-year studies (for example, Matthews

and Effler 2006), these oxygen deficits are rarely

used for of budgeting lake-wide OC losses. Further,

in lakes with anoxic hypolimnia, the use of alter-

nate electron acceptors needs to be integrated into

estimates of respiration (Mattson and Likens 1993;

Houser and others 2003). Longer time series that

encompass surface and deep waters as well as

shallow and profundal sediments would improve

estimates of ecosystem rates. Also with long time

series, factors may emerge that help identify scales

most important to determining variability in rates

(for example, Solomon and others 2013).

Q6: What Controls Burial Rates of OC, and Whatare the Origins of Buried OC? As noted above, OCstorage in sediments is difficult to quantify and

reported rates vary by 23 orders of magnitude

(Kastowski and others 2011; Ferland and others

2012). Control over long-term burial rates has been

attributed to human activity, temperature, and

catchment features (Kastowski and others 2011).

Burial rates change through time and differ among

lakes. Highly eutrophic systems may have burial

rates that are as much as two orders of magnitude

greater than non-eutrophic lakes (Downing and

others 2008). The efficiency of burial (burial di-

vided by the sum of burial and sediment respira-

tion) is hypothesized to be inversely related to

oxygen exposure time and allochthonous input

(Sobek and others 2003; Cole 2013). In addition,

sorptive protection of OC on clay and mineral

surfaces as observed in marine systems is likely

important (Cole 2013). Thus, analysis of these

factors will be necessary to account for the OC

stored in lakes and for predicting how future

changes in burial alter the influence of lake eco-

systems on long-term landscape-scale carbon

dynamics.

Q7: What are the Relative Concentrations of OCDerived from Internal Net Primary Production(NPP) Versus Allochthonous OC Loading to Budgetsand to Aquatic Consumers? Whole-lake manipu-lations and natural abundance stable isotope stud-

ies indicate that terrestrial OC supports aquatic

consumers in many low to moderate productivity

lakes (Carpenter and others 2005; Karlsson and

others 2012; Wilkinson and others 2013a; Berggren

and others 2014). However, this evidence has been

challenged on the basis of low food quality of ter-

restrial OC (Taipale and others 2014), low inputs of

allochthonous OC relative to autochthonous pro-

duction (Brett and others 2012), and difficulties

with isotopic studies (Francis and others 2011).

These arguments are evaluated elsewhere (Cole

2013), but further studies of lake OC budgets are

needed to identify lakes where allochthonous re-

source use is important. One approach to unrav-

eling the relative importance allochthonous and

autochthonous OC in supporting aquatic food webs

is to determine source proportions of lake DOM

and POM. Differences in isotope ratios of sources

(especially hydrogen isotopes) provide one means

for evaluating this question (Wilkinson and others

2013b; Berggren and others 2014) as do targeted

isotope addition studies (for example, Wilkinson

and others 2014). However, additional studies of

OC loads in relation to lake NPP are needed to

better understand how allochthonous and autoch-

thonous organic matter cycle and contribute to

food webs in lakes.


Lakes Within Changing Climate and Changing Land-

scapes

Q8: How is OC Cycling Coupled with Nutrients,Such As Phosphorus (P) and Nitrogen (N), and Dothe Interactions Change Across Trophic States?Although P and N control autochthonous produc-

tion in lakes, the nutrient loading threshold where

OC storage exceeds mineralization is typically un-

known for a lake. However, in an exploratory

modeling study (Hanson and others 2004),

thresholds for total phosphorus (TP) concentrations

were about 20 and 80 mg m-3 for oligotrophic and

eutrophic lakes, respectively. These results suggest

lake conditions where OC fluxes (for example,

mineralization, burial) may alter as a function of

nutrient cycling and provide a starting point for

further research. In addition, long-term effects of

nutrient loading on lake OC cycling remain unex-

plored. Although it is clear that persistent eutro-

phication leads to increasing anoxia in thermally

stratified lakes (Carpenter and others 1999), the

impact of nutrients on overall carbon cycling in

lakes remains poorly resolved. For example, it is

difficult to answer questions like: is there greater

relative mineralization of DOC in eutrophic lakes

and is the degradation of allochthonous inputs

stimulated in more eutrophic systems? These

questions point to the need for more studies on OC

cycling in eutrophic lakes particularly those that

consider both allochthonous and autochthonous

pools. To underscore the significance of additional

studies of eutrophic lakes, a recent evaluation

indicates a large proportion of U.S. lakes are in

agricultural landscapes (Winslow and others 2014),

and as a consequence have excess nutrient loads

(ILEC 1994).

Q9: What are the Key Gradients over Which toStudy Lake OC Cycling? Several features of lakesincluding hydrology, morphometry, nutrient load,

latitude, altitude, and surrounding land cover are

related to controls of OC cycling and budgets. These

features represent potentially interesting gradients

for comparative lake studies. Lake size clearly

matters with variability and concentration of OC

generally inversely related with lake surface area.

Certainly at the extremes of lake size, OC cycling is

tied to hydrology (smaller lakes have higher areal

water and OC loads), as well as morphometry

(large lakes have smaller perimeter:area ratios).

Although the relative input of OC sources in rela-

tion to lake size has not been well documented, the

proportion of OC of allochthonous origin should

scale with lake area, and this hypothesis is sup-

ported by isotopic studies (Wilkinson and others

2013b). A second priority for comparative study is

latitudinal and altitudinal where lake temperature,

ice cover and mixing regime will differ and these

climatically driven processes, in turn, should

strongly influence OC cycling.

Q10: How will Changing Land Use and Climate AlterLake OC Cycling? Three related issues need con-sideration to address this question. First to make

credible predictions about the effects changing land

use and climate, answers are needed to the nine key

questions raised above about lake OC cycling. Sec-

ond, the study of lakes in a landscape context must

continue to broaden so that lakes are included in

regional and global models of C-cycling (Raymond

and others 2013). A third issue is the need for a new

generation of lake ecosystem models especially

those that can encompass longer time scales (be-

yond seasonal and annual) and greater numbers of

lakes (lake districts, regions). These models would

be the most useful for contributing to current large-

scale climate and carbon modeling efforts (for

example, land surfaceatmosphere models). The

data and knowledge necessary to develop such

models capable of predicting long-term dynamics

and broad spatial patterns are scattered among

many scientists and many lake observatories. A new

scale of knowledge-data-model harmonization is

required to produce robust models, improve lake

and landscape C-flux estimates, and inform large-

scale models.

Contributions to Ecosystem Science

The research that we recommend will resolve

critical questions about OC cycling at the scales of

individual lakes, lake-rich regions, and the globe.

In addition, the research will resolve questions that

currently impede synthesis and prediction of long-

term changes in lake OC processes.

At the scale of individual lakes, the research will

improve estimates of OC burial and lake-atmo-

sphere C exchanges. These fluxes are essential for

understanding the roles of lakes as landscape

repositories of stored OC and as net sources of CO2and CH4 to the atmosphere. In addition, the re-

search will provide better data on the relative flows

of terrigenous versus aquatically-generated OC to

lake food webs.

With respect to sources of OC, aquatic consumers

exhibit a wide range of composition from mostly


aquatic to mostly terrestrial in origin (Cole and

others 2011; Wilkinson and others 2013a). The

magnitude of terrestrial contributions to lake food

webs may affect food web stability (Polis and others

1997) and the strength of trophic cascades in lakes

(Leroux and Loreau 2008). It is not clear whether

variation in lake OC budgets can explain the ob-

served variation in OC sources to food webs (Cole

2013). Such relationships could be investigated gi-

ven results of the research proposed here.

At broader spatial extents, the research will

provide a firm basis for estimating the contributions

of lakes to regional and global C cycles. A more

comprehensive suite of rigorous, whole-lake OC

budgets will facilitate comparative studies across

gradients of trophic state, latitude, climate, and

watershed characteristics. Such comparisons will

allow limnologists to interpolate lake OC storage

and processing over broad regions relevant to re-

gional, continental, or global C cycle studies. In

addition, these comparisons and analyses will im-

prove the integration of lakes with terrestrial and

lotic ecosystem OC dynamics.

Conceptually, the research will expand ecolo-

gists opportunities for synthesis and prediction of

OC processes in lakes. The results will underpin the

development, validation, and application of a new

generation of lake OC models. These will enable us

to interpret ongoing changes in lake OC budgets

and project future changes, thereby establishing

hypotheses for future empirical testing. Such

models have important applications in analyses and

projections of lake OC dynamics in watersheds with

changing land use under a changing climate.

Historically, the study of inland water ecosystems

has benefitted from budgetary approaches. Illumi-

nation of phosphorus and nitrogen budgets led to

effective strategies for managing eutrophication

(Vollenweider 1976; Smith 1998). Similarly, eval-

uation of charge balance budgets for acid anions

and base cations (Galloway and others 1983) pro-

vided key insights into acidification of inland wa-

ters (for example, Driscoll and Newton 1985;

Schindler 1986; Likens and others 1996) and con-

tributed importantly to the development of policies

to ameliorate acid deposition (Weathers and Lovett

1998). Current research suggests that lakes may be

hot spots of OC storage and processing on land-

scapes, yet the fundamental budgetary data needed

to estimate, analyze, and predict the roles of lakes

in landscape OC cycles remain poorly developed.

The research priorities suggested here would create

the foundation for new understanding of the role

of lakes in landscape OC processes.

ACKNOWLEDGEMENTS

This work was supported by the following Grants

from the National Science Foundation: DEB-

0917696, IIS-1344272, DEB-1256119, and the

NTL-LTER.

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Integrating Landscape Carbon Cycling: Research Needs for Resolving Organic Carbon Budgets of LakesAbstractIntroductionExample Carbon BudgetsTen Unanswered Questions About Lake OC BudgetsLakes at the Interface (Inputs, Outputs)Q1: What are the Allochthonous Loads to Lakes, How are They Partitioned Among Sources, and How are Loads Driven by Events?Q2: How does Control over Gas Exchange Vary by Lake and What are the Underlying Physical Factors Governing the Differences?Q3: How Does the Source of Allochthonous OC That is Loaded (That is, Fluvial OC, Leaf Fall, Peat Pore Water, and So on) Determine Its Fate in Lakes?

Internal Cycling and Lakes as Sinks (Within-Lake Processes)Q4: Do the Estimated Fates for Allochthonous OC Match Estimates of External Loads?Q5: What are OC Respiration Rates for Lake Ecosystems?Q6: What Controls Burial Rates of OC, and What are the Origins of Buried OC?Q7: What are the Relative Concentrations of OC Derived from Internal Net Primary Production (NPP) Versus Allochthonous OC Loading to Budgets and to Aquatic Consumers?

Lakes Within Changing Climate and Changing LandscapesQ8: How is OC Cycling Coupled with Nutrients, Such As Phosphorus (P) and Nitrogen (N), and Do the Interactions Change Across Trophic States?Q9: What are the Key Gradients over Which to Study Lake OC Cycling?Q10: How will Changing Land Use and Climate Alter Lake OC Cycling?

Contributions to Ecosystem Science

AcknowledgementsReferences

integrating landscape carbon cycling: research needs for resolving organic carbon budgets of lakes

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