Despite the increasing understanding about differences in carbon cycling
between temperate and tropical freshwater systems, our knowledge on the
importance of organic matter (OM) pools on light absorption properties in
tropical lakes is very scarce. We performed a factorial mesocosm experiment
in a tropical lake (Minas Gerais, Brazil) to evaluate the effects of
increased concentrations of allochthonous and autochthonous OM, and
differences in light availability on the light absorption characteristics of
chromophoric dissolved organic matter (CDOM). Autochthonous OM deriving from
phytoplankton (
Organic matter (OM) consists of particulate organic matter (POM; organic
compounds represented by aquatic communities and detritus) and dissolved
organic matter (DOM – in most DOM studies it is the compounds smaller
than 0.2 or 0.7
The main sources of DOM in aquatic ecosystems can be divided into two main categories: the allochthonous pool, which comes from terrestrial vegetation and soil sources (Kieber et al., 2006; Miller et al., 2009), and the autochthonous pool which is produced by aquatic primary producers (Kritzberg et al., 2004; Guillemette and Del Giorgio, 2012). These two DOM pools have fundamental differences in their optical and chemical characteristics which in turn influence the mechanisms by which DOM is degraded (Wetzel et al., 1995; Bertilsson and Tranvik, 2000). The allochthonous DOM is considered to be more susceptible to photodegradation because it contains relatively large molecules with high numbers of aromatic compounds which strongly absorb UV light (Amon and Benner, 1994; McKnight et al., 1994; Benner, 2002; Helms et al., 2008). The autochthonous DOM originating from phytoplankton mainly consists of simple molecules (carbohydrates, proteins, amino acids) of low molecular weight and is typically more labile for microbial community (Farjalla et al., 2009; Fonte et al., 2013).
The rate of photodegradation depends on a combination of available sunlight and the chemical characteristics of DOM (Benner, 2002), whereas the microbial degradation rate depends on the inherent DOM bioavailability and the utilization efficiency of the bacterial community (Catalán et al., 2013; Asmala et al., 2014), and both are important processes that transform and remove DOM in aquatic ecosystems (Roland et al., 2010; Mopper et al., 2015). Photodegradation is also known to transform DOM to ammonia and other highly bioavailable compounds (Aarnos et al., 2012), which can be an important nutrient supply for both phytoplankton (Hessen and Tranvik, 1998) and heterotrophic bacterial communities (Kieber et al., 1989; Miller et al., 2002; Lønborg et al., 2010). The microbial uptake of DOM by heterotrophic organisms converts it to POM, which in turn can be assimilated by protozooplankton through the microbial loop (Azam et al., 1983). Additionally, biodegradation of DOM can be stimulated by inorganic nutrients, mainly nitrogen and phosphorus, which increase the bacterial growth efficiency (Zweifel et al., 1995; Asmala et al., 2013) by reducing the energetic cost of substrate acquisition (Hopkinson et al., 1998). In tropical lakes, aquatic processes including mineralization of organic compounds occur more rapidly than in temperate lakes due to high temperatures and water light availability throughout the year (Marotta et al., 2010). However, there are only few studies on the photochemical (Teixeira et al., 2013; Bittar et al., 2015) and bacterial (Farjalla et al., 2002; 2009; Roland et al., 2010) degradation of DOM in tropical environments compared to temperate freshwater systems and estuaries (Bertilsson and Tranvik, 2000; Anesio and Granéli, 2003; Boreen et al., 2008; Asmala et al., 2014; Attermeyer et al., 2015).
The drivers of DOM dynamics in tropical environments are different from those in temperate environments, because in the tropics the seasonality of rainfall is the main driver for allochthonous contribution to the aquatic system (Suhett et al., 2006) and in temperate systems it is related to changes in temperature (such as by the flow of the melting water in the surroundings or by the destratification of lakes; Lindell et al., 2000). Brazil has a variety of complex freshwater systems that behave in different ways regarding the temporal dynamics of DOM. For example, in most tropical rivers and lakes, the seasonal allochthonous contribution occurs via runoff in the rainy season (between September and April), raising humic carbon concentrations and water color (Farjalla et al., 2002). In some regions, such as the complexes of Brazilian rivers and Amazonian lakes, the contribution of allochthonous material is related to the hydrological pulse, which raises the level of the water invading the surrounding forests (Amado et al., 2006).
The lake system of the Middle Rio Doce is composed of about 300 natural lakes and is among the three most important in Brazil, behind the Amazonian and Pantanal basins (Maillard et al., 2012). Many of these lakes are used by the local population both for water supply for human consumption and for water use in economic activities such as agriculture, livestock and large mining companies present in the region. Fishing is also an important activity in this region. Recent studies in this region have shown that the marked seasonality in the inputs of allochthonous material (nutrients and organic matter) during periods of rain (thermal stratification period, summer) plays a key role in the pattern observed for the optical characteristics of lakes, for example the transparency to photosynthetically active radiation (PAR) and ultraviolet (UV) (Gagliardi, 2015; Brandão et al., 2016). Contrary to expectations, greater transparency of these lakes is observed during the rainy season, since the allochthonous material remains trapped in the hypolimnium by temperature difference, until the water mixture (dry season, winter) redistributes it throughout the water column (Reynolds, 2009; Brandão et al., 2016). In this context, higher net phytoplankton production rates occur in the mixing periods, with lower solar radiation incidence and lower transparency (Brighenti et al., 2015). Bezerra-Neto et al. (2006) showed a strong negative influence on the concentration of CDOM (chromophoric dissolved organic matter) and transparency to the PAR radiation in a set of lakes of this lacustrine system, which emphasizes the importance of the chromophoric carbon from allochthonous origin for the physical and chemical conditions of the lakes, and consequently seasonal dynamics of phytoplankton and aquatic metabolism. In this way, the physical, chemical and ecological balance of these lakes is strongly affected by inputs of nutrients and organic matter from the catchment during the rainy season. However, the frequency and intensity of precipitation events in this region has changed over the last decade (Roland et al., 2012). In addition, the Atlantic Forest is a threatened and extremely devastated biome (Myers et al., 2000) and most of the lakes have already had the surrounding forest replaced by eucalyptus and pasture plantations. Land use transformation and the disruption of biogeochemical cycles may change the amount and quality of the inputs of dissolved nutrients (such as phosphate and nitrogen compounds) and organic matter into the lake (Vitousek et al., 1997; Pinheiro et al., 2015), changing the balance between allochthonous and autochthonous DOM sources in the systems and consequently DOM degradation pathways. In addition, tropical lakes are considered hot spots for biodiversity and greenhouse gas cycles, and furthermore they are believed to be highly sensitive to climate changes causing profound changes of lake physical (i.e., volume, area, stratification) and chemical (i.e., dissolved oxygen, nutrients, organic matter) conditions with ultimate effects on regional carbon cycling.
Some recent studies have demonstrated that DOM transformations (such as the effect of photodegradation and biodegradation on the absorption properties of CDOM) was not constant over the spectral range, thus influencing the shape of the absorption curve (Helms et al., 2013; Reader et al., 2015). As modifications in the spectral shape reflect underlying changes in the carbon compounds at the molecular level, studies on biological and chemical effects on CDOM spectra allow a better understanding of the DOM transformations and how this links to overall carbon cycling in aquatic ecosystems (Stubbins et al., 2014).
To investigate how the optical properties of the lakes change due to more common anthropogenic impacts (such as eutrophication, land use change) and recent regional changes in rainfall, we performed a mesocosm experiment in a local tropical lake, manipulating nutrients, OM and light conditions. We expected that addition of nutrients would stimulate algal growth and increase the production of autochthonous DOM (Schindler, 1977; Lean and Pick, 1981) until nutrients became exhausted. For comparison, addition of extracted OM from leaves of the native forest mimicked effects of increasing allochthonous DOM concentrations. We hypothesized that OM from different sources would change the CDOM absorption spectra and associated indices differently over time. We also investigated the effect of the two interacting OM sources on the optical characteristics of DOM. Finally, we applied a shading filter to investigate expectations of a high importance of light availability on both autochthonous OM production and variable levels of photodegradation for different pools of OM.
This study was conducted in Lake Carioca (19
To test the effect of organic matter inputs, sunlight, and nutrients on DOM
degradation, we conducted an in situ experiment using a total of 16
cylindrical mesocosms (diameter 1.3 m, height 1.5 m and volume 2 m
Schematic figure of the factorial design of mesocosms experiments.
The organic matter added to the mesocosms was a mixture of leaves, plant
detritus and soil particles adhered to this material from the ground around
the lake (four cylinders, ca. 20 L each). The material was placed in buckets
with distilled water (60 L) for decomposition and stored in the laboratory
under room temperature (ca. 25
Mesocosms were submerged on the surface of the lake and filled with lake
water. Mesocosms with reduced light availability (SH) were shaded with
spectrally neutral shading screens (50 %) and only opened for quick
samplings and measurements. Every day, the mesocosms were gently stirred and
measured for water temperature using a Hydrolab DS5 probe (Hach Inc.). During
the experiment, the water temperature of the mesocosms ranged between 28.4
and 31.3
Water samples were filtered immediately after sampling for Chl
Absorption spectra of CDOM were obtained between 250 and 700 nm at 1 nm
intervals with a spectrophotometer (UV-VIS Shimadzu) using a 5 cm quartz
cuvette and a Milli-Q water sample as blank reference. The absorption spectra
of each sample were measured in replicate (standard
deviation < 0.01). The absorption coefficients
(
We used a simple exponential curve to model the decrease in absorption with
increasing wavelength using the equation (Jerlov, 1968; Bricaud et al., 1981;
Stedmon and Markager, 2001):
The mesocosms were grouped in the figures as follows in order to show the differences between the two different sources of OM (allochthonous versus autochthonous source): the group “OM addition” includes the OM, OMNUT, OMSH and OMNUTSH treatments combined. The group “nutrients addition” includes the NUT, OMNUT, NUTSH, OMNUTSH treatments and the group “with shade” include the SH, OMSH, NUTSH and OMNUTSH. The last three groups “without OM addition”, “without NUT addition” and “full light” include the remaining four treatments, totaling six different groups (see Table S1 in the Supplement). In this context, the group “OM addition” represents the allochthonous source, while the group “nutrients addition” represents the autochthonous OM source.
The relative changes (%) of the parameters over time were calculated by
dividing the value measured at the end of the experiment by the value at the
beginning (day 0) of the experiment, after subtracting this result from 1 and
multiplying by 100 [(1
We performed a three-way ANOVA plus the second-order interactions, in order
to verify the effect of each factor (nutrients and OM additions and shade) on
the response variables (quantity (
A principal component analysis (PCA) was carried out using CDOM absorption
spectra (with 1 nm interval between 250 and 450 nm) on a
The results obtained by three-way analysis of variance (Table 1) showed that
Chl
Temporal variation in the mesocosms units with and without nutrients
(left column) and organic matter additions (right column) for
Chl
Results of the three-way analysis of variance. The coefficient of determination of the analysis of variance partition is represented in the last column by %R2.
OM: organic matter; NUT: nutrients; SH: shade
The partitioned coefficient of determination for
Average phytoplankton biomass (Chl
The relative changes in CDOM absorption along the spectral range were
different for each sampling day (Fig. 3a–e). On the initial day, only
treatments with and without addition of OM had distinct absorption curves,
especially in the UV range below 400 nm, and the absorption spectra for each
treatment group on day 0 are shown in Fig. 3a. To evaluate treatment effects
we determined the change in light absorption spectra for the other sampling
days relative to the initial day (Fig. 3b–e). On day 3, treatments with and
without nutrients added were quite similar, while those with and without OM
and with and without shading showed opposing changes. Loss of absorption
occurred only in treatments with full light (less than 5 % between
300 and 420 nm) and in those without OM addition (the loss of absorption
increased with the increase in wavelength) (Fig. 3b). On day 6 all treatments
showed an increased absorption especially after 350 nm (higher increase with
shade:
Spectral absorption curves of CDOM in the different mesocosms units
for the initial day
The concentrations of DIP and DIN (
The first principal component of the redundancy analysis (Fig. 5a) was mostly
associated with availability of OM. Samples presenting high scores on the
first principal component furthermore tended to have high values of DOC and
SUVA
Temporal variation in the mesocosms units with and without nutrients
additions for dissolved inorganic phosphorus-DIP
Results of redundancy analysis (RDA)
Exploration of spectral PCA loadings (Fig. 5b–c) revealed that principal
component 1 (PC1) had the strongest effect on the shape of CDOM absorbance
between 300 and 400 nm. Principal component 2 (PC2) loadings showed a
quasi-linear decrease with increasing wavelength suggesting that
phytoplankton enrichment had a stronger effect at lower wavelengths.
Furthermore, loading values were negative after
Our results showed a pronounced sensitivity of the composition of DOM in a
tropical lake on artificial alterations in environmental parameters such as
light and nutrient availability and allochthonous matter inputs. As expected,
the addition of allochthonous matter results in a DOM pool which is dominated
by more aromatic carbon with higher molecular weight (Bertilsson and Tranvik,
2000; Benner, 2002) and lower spectral slopes (Helms et al., 2008; Fig. 2f,
h). Addition of nutrients also affected DOM quantity and quality related to
autochthonous production by phytoplankton growth, which can be an important
source of DOM (Zhang et al., 2009, 2013; Brandão et al., 2016). In the
treatments without addition of nutrients, the phytoplankton community was
limited by nitrogen since the beginning of the experiment (DIN
< 100
Although additions of allochthonous OM and nutrients both contributed to
higher DOC concentrations, divergent effects of these additions were evident
in the quality of carbon assessed by optical indices (
Addition of nutrients, however, had little effect on these metrics, which we
interpreted as a consequence of autochthonous production of DOM. This is
likely because these indices are derived from slope intervals in the
ultraviolet range (250–400 nm) known to be influenced by carbon with higher
molecular weight and aromatic compounds capable of absorbing energy at
shorter wavelengths (Bertilsson and Tranvik, 2000; Benner, 2002; Helms et
al., 2008). Moreover, nutrient additions only increased
Manipulations of nutrients, allochthonous OM and light availability caused
distinctive changes in the spectral curves of CDOM over the sampling days
(Fig. 3). Several studies have shown that aromatic organic carbon, typically
of terrestrial origin, has relatively higher absorption in the ultraviolet
range (Bertilsson and Tranvik, 2000; Benner, 2002; Helms et al., 2008). This
can explain the initial (day 0) effects of allochthonous OM addition on
elevated CDOM absorption primarily below 350 nm (Fig. 3a). We interpret the
following increase in the CDOM absorption (days 3 and 6, especially above 350 nm)
for most treatments to result from autochthonous DOM related to
phytoplankton growth, as increases in absorption in the PAR range (Fig. 3b–c)
are known to be related to increases in carbon of simple structures from algal
origin (Amon and Benner, 1994; McKnight et al., 1994; Benner, 2002; Helms et
al., 2008). After day 9 (Fig. 3d–e) the absorption loss was larger than the
gain by the autochthonous production in all treatments, and such spectral
changes with larger absorption decreases in higher wavelengths are likely due
to biological degradation of CDOM (Asmala et al., 2014). However, it is
important to note that the relative changes in the spectral curves shown in
Fig. 3 reflect the net change from two counteracting processes: autochthonous
production and loss of absorption by photodegradation and/or biodegradation.
Treatments that were exposed to full light (orange solid lines) and the
shaded treatments (orange dashed lines) presented notable differences between
each other in the relative changes in the CDOM absorption spectrum. This
corroborates our results of the more aromatic carbon with larger molecular
size (higher SUVA
The PCA and redundancy analysis showed that the increase in allochthonous OM increased absorption between the wavelengths 300 and 400 nm (PC1, Fig. 5b). Several studies have shown that photodegradation is more pronounced at shorter wavelengths (300–400 nm) due to absorption of aromatic carbon compounds (Helms et al., 2008, 2013) typically related to degradation of either terrestrial vegetation (Bertilsson and Tranvik, 2000; Benner, 2002; Helms et al., 2008) or aquatic macrophytes (Catalán et al., 2013). We noticed a decrease in the CDOM absorption below 300 nm, suggesting a greater degradation by photodegradation in these compounds from allochthonous origin affecting the absorption at shorter wavelengths and increasing the absorption between 300 and 400 nm. In contrast, the increase in autochthonous OM from the phytoplankton growth is likely to have resulted in an increase in absorption in the UV range and a loss of absorption at wavelengths beyond 350 nm (PC2; Fig. 5c). The loss of absorption above 350 nm indicates degradation by microorganisms which have a greater impact on the PAR absorption. Substances that absorb in this range are typically non-aromatic compounds originating from algal sources with high lability for bacterial degradation (Baines and Pace, 1990; Berggren et al., 2009).
Additions of terrestrial OM and inorganic nutrients to a tropical lake
mesocosm caused fast changes in the production and transformation of OM pools
as well as distinct changes in the absorption spectra of CDOM. Increased
production of autochthonous OM caused an increase in CDOM absorption in the
UV range. However, we found that CDOM absorption was reduced in the PAR
range, indicating bacterial degradation of highly labile algal material
(Baines and Pace, 1990; Berggren et al., 2009). In contrast, the additions of
allochthonous OM caused increased absorption of CDOM, especially between 300
and 400 nm.
Our experiment adds knowledge on how input of terrestrial OM and nutrients, related to water column mixing and rains, influence carbon cycling in tropical lakes (Brighenti et al., 2015; Brandão et al., 2016). Even small inputs of allochthonous OM can have much larger effects on the spectral characteristics on the lake CDOM, compared to large production of autochthonous OM. Local changes in land use, through replacement of Atlantic Forest, will likely alter the spectral light quality. Such changes can affect a range of chemical (concentration and quality of DOM), physical (e.g upper layer mixing due to changes in the absorption of PAR and UV radiation; Read and Rose, 2013) and biological conditions (vertical distribution and productivity of aquatic organisms; Gagliardi et al., 2018). Recent reductions in regional precipitation (Roland et al., 2012) and observed lake volumes provide further evidence of a strong control by allochthonous OM on the physical, chemical and biological conditions in the Rio Doce region. As drafts are expected to become more common (IPCC, 2013), allochthonous OM will likely have an increasing control on aquatic metabolism, DOM dynamics and water transparency in these tropical lakes (Gagliardi, 2015; Brighenti et al., 2015; Brandão, 2016). These impacts will certainly alter the water quality for consumption and for water use in the economic activities in the region, with ultimate effects on regional carbon cycling.
The data used in this research are being prepared to be
published in the Global Biodiversity Information Facility
(
LPMB designed the experiment and participated in the field work, laboratory analysis and writing the manuscript.
LSB designed the experiment, participated in the field work and laboratory analysis, and reviewed the manuscript.
PAS designed the experiment and participated in the field work, writing and revision of the manuscript.
EA participated in the writing and revision of the manuscript.
PM participated in the writing and revision of the manuscript and the statistical analyses.
DT participated in the field work and revision of the manuscript.
FARB designed the experiment and participated in the field work, and revision of the manuscript.
DP participated in the statistical analyses, creating figures and revision of the manuscript.
JFBN designed the experiment and participated in the field work, writing and revision of the manuscript.
The authors declare that they have no conflict of interest.
This study was supported by the project Carbon Cycling in Lakes (COCLAKE – CAPES Proc. no. 88881.030499/2013-01) and the BONUS COCOA project (grant agreement 2112932-1), funded jointly by the EU and Danish Research Council. We also thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for financial support, scholarship and opportunity for the Science without Borders program and the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG). We would like to thank Gustavo Turci, Ralph Thomé, Patrícia Ferreira and Marcelo Ávila for field support and Marcelo Costa for nutrient analysis. Edited by: Florian Wittmann Reviewed by: three anonymous referees