Ecosystems

https://doi.org/10.1007/s10021-021-00682-0
 2021 The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature

Predicting Dissolved Organic Matter

Lability and Carbon Accumulation
in Temperate Freshwater Ecosystems
Marcela Bastidas Navarro, Luca Schenone,* Nicolás Martyniuk,
Evelyn Vega, Beatriz Modenutti, and Esteban Balseiro

Laboratorio de Limnologı́a, INIBIOMA, CONICET-Universidad Nacional del Comahue, 1250, 8400 Bariloche, Quintral, Argentina

ABSTRACT
Dissolved organic matter (DOM) dynamics influence
aquatic ecosystem metabolism with ecological and
biogeochemical effects. During microbial degradation,
certain DOM molecules accumulate in the environ-
ments constituting the residual refractory carbon (C)
pool that has a key role in the global carbon cycle in
lakes and oceans. The present study aims to model the
factors driving bacterial C-consumption, thus predict-
ing the potential residual carbon accumulation. We
developed mechanistic models to represent bacterial
C-consumption, considering the contribution of DOM
quality and phosphorus (P) and nitrogen (N) concen-
trations in the total carbon pool. Based on 59 different
environments, we established DOM components and
nutrient concentration for deep lakes, shallow lakes,
high-altitude lakes, and wetlands from North-Andean
Patagonian glacial lake district (around 41S). We ap-
plied Bayesian methods to estimate model parameters
from laboratory C-lability experiments performed in
26 environments. We tested the statistically predictive
accuracy of our models with an external dataset con-
sisting of C-lability experiments with natural lake
water enriched with organic matter from different
sources. We found a model that performed excellently
in both fit to training data and prediction to external
experiments. The selected model showed that an in-
crease in P concentration stimulates C-consumption,
and an increase in the proportion of DOM protein-like
compounds reduces the amount of residual C. Based
on the statistically predictive accuracy, we showed that
our model is very useful to anticipate C-accumulation
due to changes in the inputs to water bodies.
Key words: Microbial respiration; Dissolved or-
ganic matter; Modeling; Forecasting; Browning;
Bayesian; PARAFAC.

HIGHLIGHTS
Received 27 August 2020; accepted 11 July 2021

Supplementary Information: The online version contains supple-  We develop a general model to represent
mentary material available at https://doi.org/10.1007/s10021-021-0068 C-consumption in a wide range of ecosystems
2-0.
 Phosphorus and DOM components resulted in
Marcela Bastidas Navarro and Luca Schenone are co-first authors
good predictors of C-consumption
Authors Contribution: MBN, EB, and BM conceived the study and  Our model was able to statistically predict
designed the experiments; MBN collected the samples; LS developed the C-accumulation and thus to anticipate browning
modeling; MBN, NM, and EV performed the experiments and analyzed
the samples; LS, EB, and BM wrote the paper. All authors discussed the
presentation of results, read, commented, and approved the final version
of the manuscript.
*Corresponding author; e-mail: lucaschenone@comahue-conicet.gob.ar
M. Bastidas Navarro and others
INTRODUCTION
Dissolved organic matter (DOM) is a complex
assemblage of compounds that are consumed and
incorporated in aquatic ecosystems. Thus, DOM
decomposition has been broadly investigated in the
last decades since it influences the pool sizes and
fluxes of organic carbon and nutrient budgets
(Amado and others 2015; Toming and others
2020). Microbial degradation is one of the most
important pathways by which DOM may influence
aquatic metabolism with ecological and biogeo-
chemical effects (Del Giorgio and Davis 2003;
Obernosterer and Benner 2004; Guillemette and
others 2013). Natural DOM is a combination of
autochthonous and allochthonous sources (Findlay
2003) that will affect microbial degradation
(Amaral and others 2016; Guillemette and others
2016; Jiao and others 2018). In lake ecosystems,
the organic carbon flux of terrestrial origin is pro-
cessed releasing carbon dioxide (CO2) and methane
(CH4) to the atmosphere (Raymond and McKenzie
2012) or accumulated in their sediments (Men-
donça and others 2017). The magnitude and con-
tribution of microbial degradation in natural
systems are associated with light availability (Cory
and others 2015; Dempsey and others 2020), water
residence time (Mari and others 2007), dissolved
ions (Soumis and others 2007), nutrient concen-
tration (del Giorgio and Newell 2012), and chemi-
cal characteristics of the DOM (Guillemette and del
Giorgio 2011).
The overall bioavailability of the DOM bulk
typically declines over time when isolated from
fresh inputs (Del Giorgio and Davis 2003). In this
sense, ‘‘DOM lability’’ is an operational term ap-
plied to the proportion of carbon (C) removed by
bacteria over a certain period (Del Giorgio and
Davis 2003). Thus, the C-consumption curve of a
particular DOM bulk shows the contribution of
various pools that would differ in bioavailability
and degradation dynamics (Guillemette and del
Giorgio 2011). Early studies have recognized labile
and recalcitrant DOM components to bacteria
degradation (Tranvik 1992, 1998). Different studies
have indicated that bacteria consume both auto-
chthonous (algal) and allochthonous (terrestrial)
DOM when grown on natural lake water (Kritzberg
and others 2004; Karlsson and others 2007;
McCallister and del Giorgio 2008). In particular,
bacteria consume a fraction of terrestrial C that is
selectively allocated to biosynthesis (Guillemette
and others 2013; Guillemette and others 2016).
The organic matter originated in terrestrial ecosys-
tems and metabolized in lakes exhibits high car-
bon/nutrient ratios (Lennon and Pfaff 2005). Under
this condition of nutrient limitation, microbial
communities need to adapt their foraging to the
available substrates; however, growth rates and
consumption are, in turn, affected (Sinsabaugh and
others 2013). Nutrients such as P (phosphorus) are
important in regulating microbial metabolism
affecting also C-consumption (del Giorgio and
Newell 2012; Mutschlecner and others 2017;
Modenutti and others 2018). Finally, the intrinsic
chemical properties of the DOM would affect their
availability to bacteria (Johansson and others
2010). These differences in carbon consumption by
bacteria would determine the residual carbon,
affecting global carbon dioxide and methane
emissions (Girkin and others 2019).
Studies in freshwater ecosystems have shown
that the residual carbon pool accumulation was
related to differences in the C dynamics consump-
tion (Guillemette and del Giorgio 2011; Guillem-
ette and others 2016). During bacterial
degradation, certain DOM molecules accumulate in
the environments constituting the residual refrac-
tory pool (Jiao and others 2018). This long-lived
dissolved organic carbon (DOC) is thought to per-
form a key role in the global carbon cycle by
accumulating carbon in lakes and oceans (Jiao and
others 2018; Toming and others 2020). In addition,
freshwater ecosystems receive a large amount of
chromophoric DOM (CDOM) mainly from their
surrounding terrestrial catchments (Massicotte and
others 2017). The CDOM accumulation results in
lower bioavailability at least in the short-term
timescale (Jones and Lennon 2015). During the last
decades, many lakes had increased water color and
concentrations of this terrestrially derived DOM, a
phenomenon called browning (Monteith and oth-
ers 2007; Williamson and others 2015). This situ-
ation has been attributed to various environmental
drivers related to land use, climate, hydrology, and
sulfate deposition (Weyhenmeyer and others 2014;
Meyer-Jacob and others 2019). The comprehen-
sion of the global carbon cycle is now an urgent
requirement to understand and predict the impact
derived from climate change and watershed land
use (Kritzberg 2017; Toming and others 2020).
Despite the importance of residual carbon for
ecosystem metabolism, there were few attempts to
model which internal factors (for example, DOM
quality and/or nutrient concentrations) drive bac-
terial degradation to predict C-accumulation in
freshwater ecosystems. This gap in knowledge takes
particular importance in a global warming scenario
in which freshwaters will be affected by modifica-
tions of the surrounding terrestrial ecosystems
 Predicting Dissolved Organic Matter Lability and Carbon Accumulation
(Leavitt and others 2009; Kritzberg 2017) and an
increase in terrestrial DOM inputs (Solomon and
others 2015). The present study aims to model the
factors driving bacterial C-consumption, thus pre-
dicting the potential residual carbon accumulation.
To achieve this, we developed mechanistic models
to represent bacterial C-consumption, hypothesiz-
ing that DOM quality and P and N concentrations
can be used to predict labile and residual carbon
pool. We carried out this study in the North-An-
dean Patagonian glacial lake district (around 41S).
We established DOM components and nutrient
concentration in a database of 59 different lentic
ecosystems including deep lakes, shallow lakes,
high-altitude lakes, and wetlands. We selected 26
environments (7 deep lakes, 6 shallow lakes, 6
high-altitude lakes, and 7 wetlands), and we car-
ried out bacterial C-consumption laboratory
experiments under standardized controlled labora-
tory conditions. Based on these data, we applied
modern Bayesian methods to estimate the param-
eters of the C-consumption models. With the cali-
brated model, we addressed what variables (DOM
quality and/or nutrient concentration) are impor-
tant for predicting the C that can be consumed by
bacteria, and thus, changes in the residual C pool.
The statistically predictive value of the model was
tested with independent experiments with natural
lake water enriched with organic matter from dif-
ferent sources.
MATERIALS AND METHODS
Study Area and Sampling Procedures
We sampled a total of 59 different lentic ecosystems
(21 shallow lakes, 13 wetlands, 19 deep lakes, and
6 high-altitude lakes) located between 40 41¢ S,
71 42¢ W and 41 31¢ S, 71 32¢ W in the North-
Andean Patagonian glacial lake district (Figure 1).
The climate is humid temperate, and precipitation
ranged from 900 to 3500 mm y-1 (Paruelo and
others 1998). Vegetation shifts from the Valdivian
rainforest to the humid temperate evergreen or
deciduous Nothofagus forest (N. dombeyi and N. pu-
milio) (Daniels and Veblen 2004). The studied
environments (Table S1) include: (a) DL: deep
piedmont lakes (Zmax > 100 m) located around
700 – 800 m a.s.l., which are very transparent
environments and with very low nutrient con-
centration (Morris and others 1995; Callieri and
others 2007; Modenutti and others 2013a); (b)
HAL: high-altitude lakes located above 1300 m
a.s.l. with extremely high transparency and low
nutrient concentration (Morris and others 1995;
Bastidas Navarro and others 2014); (c) SHL: shal-
low lakes (Zmax < 12 m) located in an altitudinal
gradient (from 700 to 1300 m a.s.l.), which are less
transparent and have relatively higher nutrient
concentrations (Bastidas Navarro and others 2009;
Bastidas Navarro and others 2014); and (d) WET:
wetlands, temporary environments located in the
same altitudinal gradient as shallow lakes.
Environments were sampled once in summer
(January or February 2016–2017). In the different
environments, we took samples at 0.5 m from the
surface at a central point. In all cases, 500 mL of
water was immediately filtered through GF/F pre-
combusted filters (0.75 lm pore size) and 50 mL
was stored in pre-combusted acid-washed glass
vials in darkness for DOC quantification and optical
properties analyses. A volume of 250 mL of the
filtered water was stored in other acid-washed vials
for total dissolved nitrogen (TDN) and phosphorus
(TDP) determinations. All samples were immedi-
ately stored in cold and dark conditions and
transported to the laboratory. Nutrients and optical
analyses were performed the same day or the fol-
lowing.
Laboratory Determinations
DOC concentration was determined with a high-
temperature combustion analyzer (Shimadzu TOC
V-CSH) using potassium hydrogen phthalate as the
standard (detection limits: 0.5 lg L-1 = 0.04 lmol
L-1). TDN concentration was analyzed using a TN-
M1 unit on the Shimadzu TOC V-CSH (detection
limits: 10 lg L-1 = 0.7 lmol L-1). TDP was deter-
mined by digestion with potassium persulfate at
125 C and 1.5 atm for 1 h followed by the ascor-
bate-reduced molybdenum method (APHA 2005)
in 100-mm cuvettes with a Shimadzu UV2450 dual
beam spectrophotometer (detection limits: 0.5 lg
L-1 = 0.016 lmol L-1).
Single measurements at specific excitation–
emission wavelengths and excitation–emission
matrices (EEMs) were performed with a Perk-
inElmer LS 45 fluorescence spectrometer. The
excitation wavelength intervals were 2 nm, be-
tween 240 and 450 nm, and the emission ranged
between 300 and 550 nm, with 5-nm increments.
The measurements were performed at a constant
room temperature of 20 C in a 1-cm quartz fluo-
rescence cell. To characterize DOM, fluorescence
data were normalized according to Murphy and
others (2013) by dividing the obtained fluorescence
values (relative Units) by the Raman peak of Milli-
Q water at 350 nm excitation on the same day as
the measurement. Fluorescence was then ex-
M. Bastidas Navarro and others

S 40° 21'

Deep lake
Shallow lake
High Altitude lake
Wetland

S 40° 45'

S 41°

S 41° 24'

20 Km

W 71° 48' W 71° 30' W 71° 12'

 Predicting Dissolved Organic Matter Lability and Carbon Accumulation
b Figure 1. Map of the sampled sites. Symbols represent
the different ecosystem types. Note that not all sampled
lakes can be identified at this scale.
pressed as Raman units (RU) (Lawaetz and Sted-
mon 2009).
C-Lability Experiments
In 26 different environments (7 deep piedmont
lakes, 6 shallow lakes, 6 high-altitude lakes, and 7
wetlands), we took a volume of 3 L of water to
carry out C-consumption experiments. We carried
out standardized laboratory experiments in dark-
ness at 20 C for 20 days. The experiments were
started on the same day the samples were collected
and were run in two replicates. We applied a dual
approach to assessing DOM lability (Guillemette
and del Giorgio 2011). In the first two days, water
was incubated in 500-mL ground stoppered
Erlenmeyer flasks (without internal atmosphere)
and we measured the concentration of dissolved
oxygen every 6 h with an optical-oximeter (ODO,
Fibox 4 Presens). The oxygen consumption rates
were converted to CO2 production to provide esti-
mates of short-term C-consumption using a respi-
ratory quotient of 1 (McCallister and others 2006).
The long-term dynamics were evaluated by deter-
mining the DOC decay over the remaining 18 days
of incubation every 2–4 days. After 20 days of
incubation, the remaining DOC was considered as
residual carbon, while labile carbon was considered
as the consumed carbon during the incubations.
These experiments were used to construct and train
the models (see model description).
In addition, we carried out another set of inde-
pendent experiments to test the statistically pre-
dictive value of the model. These data came from
two independent datasets, and details in the pro-
cedures can be seen in Bastidas Navarro and others
(2019) and Vega and others (2020). Briefly, we
conducted the same DOM lability procedures in
enriched natural lake water: 1) Water from Lake
Los Patos added with benthic algal exudates (Spy-
rogira and Mougeotia) coming from the same envi-
ronment, 2) water from Lake Los Patos added with
senescent Nothofagus pumilio leaf leachates collected
in the surrounding forest, 3) water from Lake
Ventisquero Negro enriched with feces leachates of
autochthonous goose (Chloephaga poliocephala), and
4) water from Lake Ventisquero Negro enriched
with feces leachates of the European hare (Lepus
europaeus). Experiments 1 and 2 are referred as
plant enriched experiments (PE) while 3 and 4 as
feces enriched experiments (FE). We choose these
two independent datasets (PE and FE) because 1-
they were carried out with the same laboratory
methodology, 2- DOC and nutrient sources ensure
contrasting results and very different from the
training data set that would serve for testing the
statistically predictive value of our model, and 3-
because of the ecological relevance of the external
dataset that represents very different DOC sources
regarding changes in land use (changes in vegeta-
tion, livestock and animal movement).
Data Analyses
The fluorometric excitation–emission matrices
(EEMs) were analyzed through a Parallel Factor
Analysis (PARAFAC) with the DOMFluor toolbox
in MATLAB (Stedmon and Bro 2008). PARAFAC is
used to decompose trilinear multi-way data arrays
and facilitate the identification and quantification
of independent underlying signals, termed ‘com-
ponents’ (Stedmon and Bro 2008). To validate the
PARAFAC model, the split-half method analysis
was applied (Stedmon and Bro 2008). Fluorescing
components were then cross-referenced with the
OpenFluor database (Murphy and others 2014)
through a comparison of spectra from other studies
to provide further context to the results.
We estimated the proportion of protein-like
carbon component (Cprot), based on the fluores-
cence of the components obtained from the PAR-
AFAC analysis. Cprot was calculated as the quotient
of the fluorescence of protein-like C-component on
the sum of the fluorescence of all the components.
Thus, Cprot takes values from 0 (no protein com-
ponent) to 1 (no other component but protein
one).
Comparison among different environments
(DOC, TDP and TDN and Cprot) was carried out
with a Kruskall–Wallis nonparametric analyses
followed by a multiple comparison Dunn’s test.
Model Description
We modeled the curve of carbon consumption over
incubation time through a first-order exponential
decay based on the classical multi-G model (Wes-
trich and Berner 1984) developed to represent
carbon lability
DOCðtÞ ¼ Clab  ekt þ Cres ð1Þ
where Clab and Cres (mg C L-1) are parameters for
the labile and residual C pools, respectively, k (day-
1
) is the first-order decay constant, and t (day) is the
time of decomposition. The parameter k represents
M. Bastidas Navarro and others
the shape of the overall DOC decline, thereby
indicating the evolution of the initial consumption
over time.
Using Eq. 1 as the null model, a control model
was developed by adding only the initial DOC
conditions (DOC0, mg L-1)
 
DOCðtÞ ¼ pClab  ekt þ pCres  DOC0 ð2Þ
where pClab and pCres are the proportion of DOC
of the labile and residual C pool, respectively. Then,
alternative models were proposed by adding pre-
dictor variables in the exponent of the labile carbon
term and in the residual carbon term
 
kx1 xx1 t pCres
DOCðtÞ ¼ pClab  e þ  DOC0
1 þ x2  xx2
ð3Þ
where x1 and x2 represent our independent
variables while xx1 and xx2 are conversion factors
for transforming x1 and x2 as dimensionless vari-
ables, respectively. The values of xx1 and xx2 are 1,
and their units are the inverse of those of x1 and x2,
respectively.
Based on del Giorgio and Newell (2012) and
Guillemette and del Giorgio (2011), we choose
three independent variables as possible predictors
for Eq. 3: total dissolved phosphorus (TDP, lmol L-
1
), total dissolved nitrogen (TDN, lmol L-1), and
the proportion of protein-like carbon component
(Cprot). In addition, we explored the combined
effect of dissolved nutrients and Cprot through
linear and nonlinear interactions. Therefore, com-
binations between seven candidate predictors for x1
and x2 were evaluated: TDP, TDN, Cprot, Cprot *
TDP, Cprot * TDP, Cprot * TDN, and Cprot * TDN,
giving a total of 49 alternative models for Eq. 3.
Model Calibration
Based on the results of the C-lability experiments of
the 26 environments, we choose a Bayesian
framework to fit the models with our experimental
data. Bayesian inference provides a useful frame-
work for characterizing the uncertainty around
models in ecology (Clark 2005; Zhao and others
2008). Bayesian analysis was performed using
STAN code interfaced with R (R Core Team 2019)
through ‘brms’ package (Bürkner 2017). Model
parameters were estimated using Hamiltonian
Markov chain Monte Carlo (MCMC) and the re-
sults obtained from the lability experiments. The
MCMC technique utilizes consecutive model sim-
ulations with judicious parameter updating to
produce a sample from the prior probability distri-
bution (uncertainties) of the parameters (Haario
and others 2006). Weakly informative priors for
initial dynamic parameter values were applied,
assuming positive half-normal probability distri-
butions. Then, a sample of possible parameter val-
ues was produced by the MCMC algorithm,
forming the posterior distribution of the parameters
for each model. We checked parameter conver-
gence using three Markov chains with 3000 itera-
tions each and a burn-in phase of 1500 iterations.
Model Selection
The selection for the best model was assessed con-
sidering two main aspects: fit accuracy to known
data and statistically prediction accuracy to inde-
pendent experiments. Fit accuracy was quantita-
tively assessed by using the leave-one-out cross-
validation (LooCV), a powerful technique to com-
pare Bayesian-fitted models (Vehtari and others
2017). We ranked the models according to the Loo
Information Criterion (LooIC). A smaller value of
LooIC indicates a lower error between out of
sample real value and the value predicted by the
within-sample fit (McElreath 2020). Finally, sta-
tistically prediction accuracy was performed in the
test datasets using the package ‘forecast’ in R (R
Core Team 2019). We ranked the models according
to the lowest mean absolute error (MAE) between
observed DOC in the laboratory lability experi-
ments and predicted DOC by the fitted models
(Hyndman and Koehler 2006).
RESULTS
The Lentic Ecosystems
In the 59 environments (deep, shallow and high-
altitude lakes, and wetlands, DL, SHL, HAL, and
WET, respectively), we identified 4 different DOM
fluorescent components based on the PARAFAC
analysis (Table 1). Components 1, 2, and 4 (C1, C2,
and C4, Table 1) had high similarity scores
(> 0.97) with components in the OpenFluor da-
tabase (Murphy and others 2014). C1 and C4 had
fluorescence emissions that resembled terrigenous
humic substances, whereas C2 showed fluores-
cence emissions similar to the free tryptophan,
indicating that it is a protein-like compound. Fi-
nally, we were unable to identify C3 based on the
OpenFluor database, but it can be associated with a
humic-like substance based on Coble (1996).
The proportion of the protein-like component
(Cprot) was significantly different in the different
types of ecosystems (K-W, H = 21.81, d.f. = 3,
p < 0.001) (Figure 2). Wetlands showed the low-
 Predicting Dissolved Organic Matter Lability and Carbon Accumulation

Table 1. DOM Components Obtained with PARAFAC Analysis on 82 Environments.

Component Excitation Emission Tucker congruence Reference Component
maxima (nm) maxima (nm) coefficient identity

1 282 (340) 470 0.97 Dainard and others Terrestrial hu-

(2015) mic-like
2 278 330 0.99 Hambly and others Tryptophan-
(2015) like
0.99 Stedmon and others
(2011a)
0.98 Kowalczuk and others
(2009)
3 310 540 Not found in Coble (1996) Terrestrial hu-
OpenFluor mic-like
4 252 (310) 430 0.98 Stedmond and Marka- Terrestrial hu-
gen (2005) mic-like

Emission and excitation maxima of each component (for C1 and C4 the secondary maxima are in brackets), Tucker congruence coefficient obtained from the Open Fluor
database (Murphy and others 2014), reference that best matches in OpenFluor database, and probable identity of the components.

est values of Cprot and differed significantly with all
other ecosystems (a posteriori Dunn’s test, WET vs
all other ecosystems p < 0.005).
DOC and nutrient concentration (TDP, and TDN)
varied significantly in the different environments
(K-W, H = 32.31, for DOC, H = 32.31 for TDP,
H = 21.04 for TDN H = 20.45, p < 0.001 for all
cases) (Figure 3). WET showed the highest values
and the widest range of concentrations in the three
variables, differing significantly from the other
ecosystems (a posteriori Dunn’s test DOC:
p < 0.005; TDP: p < 0.001; TDN: WET and SHL
differ from DL and HAL p < 0.002). These data
were not used to adjust the model but gave us the
framework of our systems and serve us to select the
lakes for the laboratory C-lability experiments.
Labile and Residual C in C-lability
Experiments
The DOM lability experiments performed in the 26
selected ecosystems showed significant differences
in the concentration of the residual C pool (Krus-
kall-Wallis, H = 20.57, p < 0.001) (Figure 4).
Wetlands showed the highest stock of residual C
with significant differences with all other ecosys-
tems (a posteriori Dunn’s test, WET vs remaining
ecosystems but SHL, p < 0.001, SHL vs HAL,
p = 0.015).
The results obtained by applying a multi-G model
to each environmental type showed that labile
carbon (Clab) and residual carbon (Cres) parame-
ters and the decay rate (k) have great variation
among them. DL and HAL showed the highest

0.8
Cprot (C2 / C1+C2+C3+C4)

0.6

0.4

0.2

0.0
DL HAL SHL WET

Figure 2. Box plot of the proportion of the protein-like component (Cprot) in the different ecosystems sampled in this
study. References: DL: deep lakes, HAL: high-altitude lakes, SHL: shallow lakes, WET: wetlands.
M. Bastidas Navarro and others

20

15

DOC (mg L -1)

10

0.8
TDP (µmol L -1)

0.6

0.4

0.2

0.0

90
TDN (µmol L -1)

60

30

0
DL HAL SHL WET

Figure 3. Box plot of nutrient concentration in the different ecosystems sampled in this study. DOC, dissolved organic
carbon; TDP, total dissolved phosphorus; TDN, total dissolved nitrogen. References: DL: deep lakes, HAL: high-altitude
lakes, SHL: shallow lakes, WET: wetlands.

values of decay, indicating a rapid consumption of External C-lability Experiments

the DOM in these ecosystems. On the contrary, the
Two external datasets of C-lability experiments on
decline in consumption rate was more gradual for
enriched lake water (leaf leachates and algal exu-
WET and SHL (lower k) with a higher Cres (Ta-
dates: PE, and hare and goose feces: FE) were used
ble 2) resulting in a higher residual DOM (Fig-
ure 4). The differences in the obtained decay rates, for testing the statistically predicting value of the
selected models (see below). These datasets exhibit
Clab and Cres, indicate that a general model will
also a high heterogeneity in the variables DOC,
have a weak power fitting the whole dataset that
TDP, and TDN concentration, and Cprot (Table 3).
includes different ecosystem types.
 Predicting Dissolved Organic Matter Lability and Carbon Accumulation

Figure 4. Labile and residual carbon pools in the C-lability experiments in the different environments. References: DL:
deep lakes, HAL: high-altitude lakes, SHL: shallow lakes, WET: wetlands. Error bars represent 1 s.e.

Table 2. Multi-G Model (Eq. 1) Fit of DOM Lability in the Different Ecosystems.
Clab (mg L-1) s.e Cres (mg L-1) s.e k (day-1) s.e

DL 0.61 0.44 0.58 0.32 0.798 0.600

HAL 0.59 0.44 0.50 0.29 0.809 0.583
SHL 1.18 0.64 2.37 0.54 0.504 0.501
WET 3.77 0.76 4.12 0.76 0.021 0.019

DL deep lakes, HAL high-altitude lakes, SHL shallow lakes, WET wetlands. Clab labile carbon, Cres residual carbon, s.e. standard error, k first-order decay rate.

Table 3. Summary of the External Dataset Used for Predictive Accuracy Test.
Exp source Rep DOC (mg L-1) TDP (lmol L-1) TDN (lmol L-1) Cprot dimensionless

PE Control 9 1.01 (0.83 – 1.40) 0.22 (0.12 – 0.32) 29.43 (16.33 – 43.32) 0.28 (0.24 – 0.35)
Leaf leachates 9 1.34 (0.91 – 1.99) 0.74 (0.34 – 1.09) 99.20 (45.91 – 145.5) 0.38 (0.34 – 0.42)
Algal exudates 9 1.61 (0.96 – 2.05) 0.20 (0.11 – 0.29) 27.14 (14.20 – 39.06) 0.31 (0.23 – 0.35)
FE Control 3 0.66 (0.62 – 0.74) 0.28 (0.23 – 0.32) 7.36 (6.25 – 9.46) 0.46 (0.40 – 0.50)
Hare feces 3 3.45 (3.37 – 3.51) 6.17 (5.41 – 6.59) 29.21 (25.86 – 30.36) 0.39 (0.37 – 0.43)
Goose feces 3 11.49 (10.83 – 12.38) 13.06 (7.79 – 15.82) 97.69 (95.14 – 99.68) 0.34 (0.32 – 0.37)

DOC, TDP, and TDN concentration and the proportion of the protein -like component (Cprot) in the two external datasets of C-lability on enrichment experiments (PE and FE).
PE: plant enriched experiments. FE: feces enriched experiments. Rep: number of replicates. Values are expressed as mean (min–max).

Model Fit and Statistically Predictive
Accuracy
Based on the 26 C-lability experiments, we con-
structed and trained the null, control and the 49
different alternative models. All the alternative
models evaluated showed better fit accuracy than
the null model (smaller LooIC), whereas 38 alter-
native models were better than the control model
(Table 4). The smallest LooIC evaluated in the
training dataset (26 different C-lability experi-
ments) was obtained with the model #9 (Table 4:
‘C_PC’), which has Cprot in the exponent of the
labile carbon term and the linear product between
Cprot and TDP in the residual carbon term. How-
ever, the second best model according to LooIC was
the best model predicting external data (Table 4).
The statistically predictive value of the models
was tested with two external datasets of C-lability
on enrichment experiments (PE and FE). All the 49
alternative models evaluated showed better pre-
dictive accuracy than the null model (smaller
MAE), of which 32 alternative models were better
than the control model. The best prediction accu-
M. Bastidas Navarro and others

Table 4. Model Fit And Ranks According To A Fit Accuracy To The Training Data (LooIC) and to Prediction
of External Data (MAE).
Model Model Equation Predictor variables units LooIC Rank MAE
number name (LooIC) Rank
x1 x2
pffiffiffiffiffiffiffiffiffi -1 ½
1 sPC_C 3 Cprot  pTDP
ffiffiffiffiffiffiffiffiffi(mg L-1)½ Cprot dimensionless
pffiffiffiffiffiffiffiffiffiffi 2 (3.57) 1
2 sPC_sNC 3 Cprot  pTDP
ffiffiffiffiffiffiffiffiffi(mg L-1)½ Cprot  TDN (mg L-1)½ 5 (6.29) 4
3 sPC_NC 3 Cprot  pTDP
ffiffiffiffiffiffiffiffiffi(mg L-1)½ Cprot  TDN mg L-1 6 (7.42) 5
4 sPC_N 3 Cprot  pffiffiffiffiffiffiffiffiffi
TDP (mg L ) TDN mg L-1 8 (7.65) 6
-1 ½
5 sPC_P 3 Cprot  pTDP
ffiffiffiffiffiffiffiffiffi(mg L-1)½ TDP mg L-1
pffiffiffiffiffiffiffiffiffi 7 (7.47) 7
6 sPC_sPC 3 Cprot  TDP (mg L ) Cprot  TDP (mg L-1)½ 3 (5.31) 10
7 cntr 2 – pffiffiffiffiffiffiffiffiffi – 39 (164) 33
8 sPC_PC 3 Cprot  TDP (mg L-1)½ Cprot  TDP mg L-1 4 (5.83) 34
9 C_PC 3 Cprot dimensionless Cprot  TDP mg L-1 1 (0) 35
10 null 1 - - 51 (1445) 51

Comparison of the best 8 alternative models, the control model, and the null model. x1 and x2 represent our predictor variables from Eq. 3. Rank LooIC (LooIC) is the rank of
the models according to their difference in LooIC (leave one out) to the smaller LooIC, in brackets is the LooIC value. Rank MAE is the rank of the model according to the mean
absolute error in predicting external data.

racy (lowest MAE) for the external dataset was
found with the model #1 (‘sPC_C’) (Table 4), which
has the nonlinear product between TDP and Cprot
in the exponent of the labile C term and Cprot in
the residual C term. This model was the second best
model fitting the training data, thus it was the best
overall model, since the only better fitting model
resulted in rank 35 predicting external data.
The relationships involving N were much weaker
than those with P (Table 4). Nitrogen only ap-
peared in three models in the residual term but
never without P in the equation. In particular, in 7
of the 8 lowest LooIC models the exponent was the
pffiffiffiffiffiffiffiffiffi
same: Cprot  TDP (Table 4).
Visual assessment of the predicted versus ob-
served DOC concentration of the training dataset
showed a similar fit among the two best models
(Figure 5). The null model had a poor fit with the
whole training dataset (Figure 5a). There was a
remarkable improvement in the fit accuracy from
the null model to the control model (Figure 5b)
and a further improvement in the fit from the
control model to the two best alternative models
(model #9 and #1) (Figure 5c and d), especially for
higher DOC concentrations. Finally, no visual dif-
ferences can be assessed between the best model
according to the lowest LooIC (Figure 5c) and the
second best model presented here (Figure 5d),
where almost all points lay over the 1:1 line.
As in the training dataset, visual assessment of
the predicted versus observed DOC concentrations
obtained in PE and FE experiments showed a very
poor predictive capacity of the null model (Fig-
ure 6a). An important improvement was observed
in the control model; however, there is an under-
estimation of almost all tested values (Figure 6b).
The inclusion of the best LooIC model did not im-
prove the statistically predictive capacity compared
to the control model and most of the data were
overestimated (Figure 6c). Remarkably, the model
#1 with almost all points over the 1:1 line showed
high statistically predictive accuracy for external
data (Figure 6d). However, few points (8 out of 469
points) around 5 mg L-1 resulted overestimated
(Figure 6d). Because this model showed the second
lowest LooIC and lowest MAE with high statisti-
cally predictive value, we consider that model #1
has the best overall fitness and statistically predic-
tive capacity. Thus, we choose this model (Eq. 4) as
the best model to predict C-consumption.
DOCðt;Cprot ;TDPÞ ¼
 
pffiffiffiffiffiffiffi Cres
Clab  ekCprot  TDPxx1 t þ  DOC0
1 þ Cprot  xx2
ð4Þ
Posterior mean and 95% credible intervals for
each parameter are shown in Table 5. Estimate
errors of all parameters are smaller than their
means, and parameter posterior 95% credible
intervals do not include zero (Table 5).
 Predicting Dissolved Organic Matter Lability and Carbon Accumulation

a b
15

10

5
Predicted DOC

c d
15

10

0
0 5 10 15 0 5 10 15

Observed DOC
Figure 5. Model fit to the 26 C-lability experiments (training dataset): predicted vs observed DOC concentration (mg L-1).
The models compared here are: a. Model #10 (null), b. Model #7 (control), c. Model #9, d. Model #1.

DISCUSSION this heterogeneity gives robustness to the selected

In this study, we have analyzed DOM lability in
aquatic ecosystems through a mechanistic model
designed and optimized to recreate the C-con-
sumption dynamics. We tested 49 alternative
models with different independent variables for
explaining C decay. Bacterial C-consumption
experiments in the training dataset covered differ-
ent environment types and in all individual cases,
the C decay fitted a multi-G model. However,
parameters varied greatly among experiments and
when all experiments were considered together in
a unique multi-G model (our null model) it failed
to fit the whole data set (Table 3, Figure 5a). The
high heterogeneity, in nutrient and DOC concen-
trations and DOM quality properties, among the
environments included in our dataset would ac-
count for the failure of the null model. However,
alternative models, as they fit and can statistically
predict despite of it. The sampled environments
presented a wide range in DOC from 0.5 to 12 mg C
L-1. Deep and high-altitude lakes are in the lower
extreme (less than 1 mg C L-1) and these values
are seldom included in C-consumption models (Del
Giorgio and Cole 1998; Del Giorgio and Davis 2003;
Guillemette and del Giorgio 2011). The hetero-
geneity was also observed in the variation of the
proportion in the protein-like component, ex-
pressed as Cprot, varying from 0.06 in wetlands and
shallow lakes to 0.7 in deep and high-altitude lakes.
The differences in this ratio would reflect the
importance of autochthonous production in deep
and high-altitude lakes (Stedmon and others
2011b).
The best fit for the pooled 26 C-lability experi-
ments was obtained with the model # 9 C_PC,
M. Bastidas Navarro and others

Control Goose Hare Leaf Exudates Leaf Leachates

a b
15

10

5
Predicted DOC

c d
15

10

0
0 5 10 15 0 5 10 15

Observed DOC
Figure 6. Model prediction to the external dataset of C-lability experiments (test dataset): predicted versus observed DOC
concentration (mg L-1). The models compared here are: a. Model #10 (null), b. Model #7 (control), c. Model #9, d. Model
#1. The different experiments are shown in different colors.

Table 5. Summary of Posterior and Convergence Statistics for the Best Model.
Parameter Post. Mean Post. s.e 95% CI R ESS

pClab 0.887 0.036 0.816–0.960 1.004 1337

k 0.119 0.005 0.110–0.129 1.001 1553
pCres 0.106 0.039 0.027–0.184 1.004 1321
SD 0.220 0.010 0.201–0.242 1.001 2046

Post. Mean = posterior mean; Post. s.e. = posterior standard error. 95% CI = 95% Bayesian credible interval; ESS = effective sample size; R=Gelman–Rubin Statistic.

which has Cprot in the exponent of the labile car-
bon term and the linear product between Cprot and
TDP in the residual carbon term. However, this
model did not result in the best for statistically
predicting external data. Previous studies showed
that P has a direct effect on bacteria respiration (del
Giorgio and Newell 2012). In particular, P en-
hances labile carbon respiration with an increase in
the exponent of the C decay model (Modenutti and
others 2016). Noticeably, in model #9, P is not in-
cluded in the exponent of the decay model but only
in the residual term of it. Probably, the lack of the
variable P in the exponent of decay weakened this
model when predicting external data of so different
sources (plant and feces leachate enrichments).
 Predicting Dissolved Organic Matter Lability and Carbon Accumulation
The best statistically prediction for external data
was obtained with the model #1 sPC_C. In our se-
lected model, the decay factor (exponent of the
model) is affected by P concentration and DOM
structure (Cprot). In our model #1, both variables
are included in this first term, as the final exponent
is the product of the square root of P and Cprot. This
implies that as P or the protein fraction of DOM or
both increases, the DOM will be more rapidly
consumed in a short period. Moreover, the non-
linear interaction between P and Cprot (given by
the square root) indicates that carbon consumption
by bacteria is dampened toward higher P concen-
trations. Nonlinear effects outperform linear mod-
els in several physiological and trophic traits
(Amarasekare 2015). Accordingly, a nonlinear ef-
fect of nutrients persisted in the 7 best statistically
predicting models and in 7 of the 8 best fitting
models (Table 4). On the other hand, the residual
term of the equation (the second term) that rep-
resents the residual pool, is only affected by the
DOM structure, which is the proportion of protein-
like components. In this case is clear that as the
protein-like components increases in the DOM, the
residual pool will be smaller. However, as this
residual pool is determined by the fraction of non-
consumable or recalcitrant organic matter, the
contribution of P should be negligible, and our
model shows that its inclusion did not increase its
statistically predictive capacity (Table 4, Figure 6 c
and d).
In our analysis, we found two alternative models
(#1 and #9). However, our best statistically pre-
dicting model (#1) was the second best fitting
model and did not show enough differences (LooIC
difference < 4, in Table 4) for selecting one over
the other. On the other hand, when we analyzed
the statistically predictive capacity to external data,
the model #9 dropped to rank 35 showing a very
weak predicting capacity and not better than the
control model (Table 4, Figure 6 b and c). This
weak prediction of model #9 implies that the model
is not generalizable enough to data outside the
training dataset. On the contrary, model #1 has a
very good fitting (rank 2) and the best predicting
(rank 1) and showed that independently of the data
source was able to account for changes in P con-
tent, C:P ratios, and DOM components. In this
sense, models that are more appropriate for pre-
diction should be prioritized, as prediction is a
commitment in modern ecology (Houlahan and
others 2017; Dietze and others 2018). Thus, the
generalizability of our model #1 would imply an
improvement in the model equation for the
appropriate prediction of C-consumption and the
importance of resource imbalances as P and DOM
components.
Resource imbalance is an important factor for
bacteria respiration and P limitation-induced C-
accumulation (Godwin and others 2017). In all the
environments of our dataset, the residual DOC pool
resulted higher than 50%, with the highest values
in the wetlands. Interestingly, deep lakes and high-
altitude lakes with DOC concentration less than
1 mg L-1 showed a high relative residual C
meaning that in these ultraoligotrophic P-limited
environments (Bertoni and others 2008; Modenutti
and others 2016; Modenutti and others 2018) there
is a proportional high C-accumulation. This resid-
ual fraction seems high according to the Cprot ob-
served in them. However, the absolute amount of
residual C is very low ( 0.5 mg C L-1). Microbial
communities can adapt to differences in resources
(Sinsabaugh and others 2013). However, if this
residual C is in very low concentration and is
composed of different labile molecules, each one
individually below the uptake threshold of bacte-
ria, bacteria physiology would be unable to access
them (Jiao and others 2018). Despite this, our
model was able to statistically predict C-consump-
tion when DOC concentration was below 1 mg C
L-1. On the contrary, the high concentration of
residual DOC observed in wetlands and shallow
lakes seems to be associated with an increase in
more terrigenous DOM (low Cprot). This increase
was associated with the process of ‘‘browning’’ that
is caused by many factors, including increases in
precipitation and changes in land use (Kritzberg
2017). An increase in precipitations was related to
an increase in DOC concentration and water color
in small and shallow Patagonian lakes (Bastidas
Navarro and Modenutti 2012; Soto Cárdenas and
others 2017). Our model was also able to statisti-
cally predict C-consumption at high DOC concen-
trations, high P, or low Cprot that could be induced
by these environmental changes that cause
browning and thus C-accumulation.
Elemental ratios (/ ratios) directly affect a large
variety of organisms, including bacteria (Elser and
others 2003), and high C:P ratios decrease bacterial
production (Lennon and Pfaff 2005) and C-con-
sumption rates (Modenutti and others 2018),
increasing the accumulation of C in the system
(Godwin and others 2017). In our model, though
the C:P ratio is not directly included, it is implicitly
considered. The labile C term of the equation has P
in the negative exponent; thus, C is divided by P. It
has been shown that the labile DOM/TDP ratio has
a negative relationship with bacterial production
and bacterial growth efficiency (del Giorgio and
M. Bastidas Navarro and others
Newell 2012). In our selected model, low concen-
trations of P relative to C decrease the rate at which
C is consumed, reducing the exponent of the C
decay. Both variables, individually and combined,
were observed in our C-consumption experiments
and successfully represented by our model.
DOM processes are a concern for aquatic re-
searchers and resource managers because affects
different ecosystem mechanisms that will have
multiple consequences for the environment
including negative effects on important ecosystem
services (Solomon and others 2015; Williamson
and others 2015). As our model considers simple
and easy to determine variables (nutrient concen-
tration, total DOC and DOC components), it can be
very useful to predict C-accumulation due to
changes in the inputs to water bodies. On the one
hand, certain DOM molecules are accumulated in
the environments constituting the C sequestration
in the residual refractory pool that would represent
a significant fraction of the uptake of atmospheric
CO2 by aquatic ecosystems (Jiao and others 2018).
On the other hand, browning for a majority of
lakes is related to changes in land use: agriculture
and afforestation (Kritzberg 2017). In addition,
warming and agricultural expansion will also con-
tribute to changes in nutrients (Feuchtmayr and
others 2009) and DOM inputs (Hunting and others
2016) affecting C-accumulation in freshwater sys-
tems. Our predicting dataset included experiments
enriched with terrestrial leaf litter leachates
(Nothofagus), algal exudates, and avian and mam-
mal feces. These enrichments represent increases
up to two folds in N and ten folds in P concentra-
tion and substantial changes in DOM components.
In addition, these enrichments can be associated
with human practices and natural disturbances that
occurred in the North-Andean Patagonian. The
Nothofagus native forest is being progressively sub-
stituted by rapid growth exotic tree species, mainly
Pinaceae, and these actions will cause important
changes in organic matter input to aquatic envi-
ronments (Albariño and Balseiro 2002). Further-
more, natural and anthropogenic disturbances will
change nutrient inputs affecting algal populations
(Reissig and others 2006; Modenutti and others
2013b) and thus DOM inputs (Bastidas Navarro
and others 2019). Finally, animals can play an
important ecological role by supplying allochtho-
nous DOM and nutrients to newly formed lakes
during glacial recession due to global warming
(Vega and others 2020). These different sources
would represent alternative changes in DOM in-
puts of autochthonous and allochthonous origins,
and DOM switching from different sources are
important for ecosystem structure and function
(Hosen and others 2020). In this sense, this exter-
nal dataset shows the power of the model in sta-
tistically predict changes in C fractions due to land
use (forest management) and lake trophic levels
(increase in nutrients). Thus, with our model, we
would be able to statistically predict C-accumula-
tion and anticipate browning. According to our
model, a decrease in Cprot will promote carbon
accumulation and an increase in P concentration
will increase the consumption rate of the labile
fractions but not necessarily a reduction in the
residual fractions. Thus, based on simple variables
(nutrient and DOC concentrations, and DOM
components) and without the need to carry out
more complex laboratory experiments our model
could be a tool to statistically predict changes in
labile and residual C fractions.
ACKNOWLEDGEMENTS
We thank the SME Wolf Mooij and two anony-
mous reviewers whose comments greatly improved
this manuscript. This work was supported by the
Fondo Para la Investigación Cientı́fica y Tec-
nológica Argentina (FONCyT), PICT 2017-1940,
PICT 2018-1563. Sampling and experiments were
conducted with permission N734 by Adminis-
tración Parques Nacionales, Argentina.
DATA AVAILABILITY
All the data generated during and/or analyzed
during the current study and the model script for R
are available at http://rdi.uncoma.edu.ar/handle/1
23456789/15901.
Declaration
Conflict of interests The authors declare
that they have no competing interests.
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