Determining the high variability of pCO2 and pO2 in the littoral zone of a subtropical coastal lake

Determinando a alta variabilidade da pCO2 e pO2 na zona litorânea de uma lagoa costeira subtropical

Determining the high variability of pCO₂ and pO₂ in the littoral zone of a subtropical coastal lake

Determinando a alta variabilidade da pCO₂ e pO₂ na zona litorânea de uma lagoa costeira subtropical

Denise Tonetta^I; Maria Luiza Schmitz Fontes^II; Mauricio Mello Petrucio^I

^ILaboratório de Ecologia de Águas Continentais, Departamento de Ecologia e Zoologia, Centro de Ciências Biológicas, Universidade Federal de Santa Catarina – UFSC,

Campus Universitário, s/n, Trindade, CEP 88040-900, Florianópolis, SC, Brazil, e-mail: [e-mail]; [e-mail]

^IISchool of the Environment, University of Technology Sydney, NSW, Australia, e-mail: [e-mail]

ABSTRACT

The aquatic metabolism comprises production and mineralization of organic matter through biological processes, such as primary production and respiration that can be estimated by gases concentration in the water column.

AIM: The study aimed to assess the temporal variability of pCO₂ and pO₂ in the littoral zone of a subtropical coastal lake. Our hypotheses are i) high variability in meteorological conditions, such as temperature and light, drive the high variability in pCO₂ and pO₂, and ii) the lake is permanently heterotrophic due to the low phosphorus concentration.

METHODS: We estimated pCO₂ from pH-alkalinity method, and pO₂ from dissolved oxygen concentration and water temperature measured in free-water during 24 hours in the autumn, winter, spring and summer.

RESULTS: Our findings showed that limnological variables had low temporal variability, while the meteorological variables and pCO₂ presented a high coefficient of variation, which is representative of each climatic season. In autumn and winter, it was recorded that the lake was supersaturated in CO₂ relative to the atmosphere, while in spring and summer CO₂ concentration was below the concentration found in the atmosphere. Over 24 hours, pCO₂ also showed high variability, with autumn presenting higher concentration during the night when compared to daytime. Water temperature and chlorophyll a were negatively correlated with pCO₂, while pO₂ was positively correlated with wind and light.

CONCLUSION: Agreeing with our first hypothesis, pCO₂ showed an expressive temporal variation in a subtropical lake associated to the high variability in meteorological conditions. On the other hand, our second hypothesis was not confirmed, since Peri Lake exported CO₂ to the atmosphere in some periods and in others, CO₂ was removed from the atmosphere.

Keywords: subtropical, temporal variation, aquatic metabolism, meteorological conditions, seasonality.

RESUMO

O metabolismo aquático envolve os processos de produção e mineralização da matéria orgânica através de processos biológicos, tais como produção primária e respiração, que podem ser estimados através da concentração de gases na coluna d’água.

OBJETIVO: O objetivo do presente estudo foi determinar a variabilidade temporal da pCO₂ e da pO₂ na zona litorânea de uma lagoa costeira subtropical, tendo como hipótese que i) a alta variabilidade nas condições meteorológicas, tais como temperatura e luz, direcionam a elevada variabilidade na pCO₂ e pO₂ e que ii) o ambiente é permanentemente heterotrófico devido à baixa concentração de fósforo.

MÉTODOS: Nós estimamos a pCO₂ através do método pH-alcalinidade, e a pO₂ a partir da concentração de oxigênio dissolvido e temperatura da água, medidos em água livre, durante 24 horas, no outono, inverno, primavera e verão.

RESULTADOS: Nossos resultados mostraram que as variáveis limnológicas amostradas apresentaram baixa variabilidade temporal, porém as variáveis meteorológicas e a pCO₂ apresentaram elevado coeficiente de variação, refletindo a variação em cada estação amostrada. No outono e no inverno foi registrado que o ambiente foi supersaturado em CO₂ em relação à atmosfera, enquanto na primavera e no verão a concentração de CO₂ foi abaixo da concentração encontrada na atmosfera. Ao longo de 24 horas, a pCO₂ também se apresentou variável, sendo que no outono ocorreu maior pCO₂ durante a noite que durante o dia. A pCO₂ foi correlacionada negativamentecom a temperature da água e a concentração de clorofila a, enquanto que a pO₂ foi positivamente correlacionada com o vento e a luz.

CONCLUSÃO: De acordo com a nossa primeira hipótese, a pCO₂ apresentou expressiva variação temporal na zona litorânea de um lago costeiro subtropical, juntamente com a alta variabilidade das condições meteorológicas. Entretanto, nossa segunda hipótese não foi confirmada uma vez que em alguns períodos ocorreu um balanço líquido de liberação de CO₂ para a atmosfera, enquanto em outros períodos ocorreu absorção de CO₂ da atmosfera.

Palavras-chave: subtropical, variação temporal, metabolismo aquático, condições meteorológicas, sazonalidade.

1. Introduction

Lakes are recognized for their substantial role in global carbon cycle. They are extremely active sites for transport, transformation and storage of considerable amounts of carbon received from the terrestrial environment (Tranvik et al., 2009). In this way, primary production and respiration are the most important biological processes responsible for production and mineralization of organic matter and involve CO₂ uptake by primary producers, releasing O₂, which is, in turn, used by heterotrophic organisms that release CO₂ (Cole et al., 2000). The net balance between production and mineralization result in an environment considered as a carbon source or sink.

The trophic status is one of the most important variables related to metabolic processes. The majority of the oligotrophic aquatic environments are typically heterotrophic, which means respiration is higher than primary production, making lakes important sources of CO₂ to the atmosphere. On the other hand, when the primary production is higher than respiration, the environment is considered autotrophic, thus CO₂ is removed from atmosphere and carbon can be stored as organic carbon (Cole et al., 1994, 2007). Therefore, changes in nutrient concentrations can influence biological processes and consequently, the ecosystem net balance.

Other variables have been related to extent and magnitude of temporal variability in metabolic processes. Variations in irradiance, temperature, and organic matter affect aquatic organisms and their metabolisms, driving the net ecosystem production and shifting between autotrophic and heterotrophic phases during the course of a day or year (Staehr et al., 2010; Marotta et al., 2010). However, the intensity of these metabolic processes can vary between temperate and tropical/subtropical lakes (Amado et al., 2013), both daily and seasonally, since temperature and light are highly variable in boreal and temperate regions compared to tropical areas (Barbosa, 1997).

The diel variation, especially in temperature and radiation, affect the photosynthetic rates of the community and act indirectly on the regulation of other metabolic processes. Petrucio and Barbosa (2004) demonstrated that bacterioplankton production may vary widely over the course of the day even in tropical lakes. On the other hand, Sadro et al. (2011) reported higher respiration rates occurring at dusk and in the first part of the night, coupled directly to the diel production of organic carbon. Although changes in temporal patterns have been studied for several decades, much less is known about the diel changes in aquatic metabolism (Staehr and Sand-Jensen 2007; Marotta et al., 2012).

Aiming to determine the temporal variability (diel and seasonal) of pCO₂ and pO₂ in the littoral zone of a subtropical coastal lake, and to infer about the aquatic metabolism, we estimated pCO₂, and pO₂ in free-water, during 24 hours in four periods (autumn, winter, spring and summer). Our hypotheses are i) subtropical lakes will show high diel and seasonal variability in pCO₂ and pO₂, and ii) the low phosphorus concentration of the lake drive to a permanently net heterotrophic condition.

2. Material and Methods

2.1. Study site

Peri Lake is a freshwater coastal lake, with a surface area of 5.07 km², average and maximum depths of 4.2 m and 11.0 m, respectively, located in the southeast of Santa Catarina Island (27°44’S and 48°31’W), Brazil, into a environmental protected area. Spatial homogeneity of nutrients and chlorophyll a, elevated densities of the cyanobacteria Cylindrospermopsis raciborskii (Woloszinska) Seenayya and Subba-Raju, and low phosphorus concentration have been observed in the lake (Hennemann and Petrucio 2011; Tonetta et al., 2013). The system has two main tributaries (Cachoeira Grande and Ribeirão Grande Streams) and it is the largest source of drinking water in Santa Catarina Island (Figure 1).

2.2. Environmental variables

All variables were sampled at the following hours of one day cycle: 9:00, 12:00, 15:00, 18:00, 24:00, 6:00 and 9:00 h in four different periods of the year: autumn (May 23, 2010), winter (August 1, 2010), spring (September 30, 2010) and summer (January 13, 2011). Since the lake has spatial homogeneity concerning nutrients and chlorophyll a, water samples were taken in the subsurface of the littoral zone in the northeast portion of Peri Lake for determination of water temperature and dissolved oxygen with a multiparameter probe (YSI-85). pH was determined using a Digimed pH meter (DM-22) and alkalinity determined by Gran’s titration, immediately after sampling. For chlorophyll a analysis, 500 mL of water was filtered (0.7 µm, Millipore AP40 glass fibre) and kept frozen at –20°C, followed by extraction using 90% acetone (Lorenzen, 1967). The light – photosynthetically active radiation (PAR) was measured at the subsurface in the water column using a radiometer (Li-cor 250A) with a spherical sensor, and wind speed was estimated using an anemometer (Instrutherm TAD 500). Precipitation records were obtained from the Santa Catarina Environmental Resources and Hydrometeorology Information Centre (EPAGRI/CIRAM). The complete values of nutrient concentration can be accessed in Tonetta et al. (2013).

2.3. pCO₂ and pO₂

CO₂ concentrations were estimated in subsurface waters, determined from pH and alkalinity measurements (Stumm and Morgan, 1996) with correction for temperature, altitude, and ionic strength (Cole et al., 1994). pCO₂ and pO₂ were determined from the Henry’s law with appropriated adjustments for temperature and salinity for CO₂ (Weiss, 1974) and O₂ solubility (Garcia and Gordon, 1992). CO₂ saturation was calculated considering the equilibrium with atmosphere of 393 µatm in May/2010, 388 µatm in August/2010, 387 µatm in September/2010 and 391 µatm in January/2011 (Data from Mauna Loa Observatory at http://www.esrl.noaa.gov/gmd/ccgg/trends/; Tans (2013)). O₂ saturation was considered in equilibrium with the atmosphere at 22,000 µatm.

2.4. Statistical analysis

The coefficient of variation was calculated for all variables to estimate the variability along the day and among periods. This coefficient gives a relative measure of variability and is not sensitive to extreme values (Melack, 1979). Pearson correlation coefficients were used to identify significant correlations between pCO₂ and pO₂ and environmental variables. Variables were log (x+1) transformed and analysis was conducted in the software Statistica 7 (StatSoft®).

3. Results

3.1. Environmental variables

Water temperature was higher in summer and lower in winter, whereas dissolved oxygen showed an opposite pattern (Figure 2c, e). Summer also recorded the highest values of PAR at the water subsurface, whereas in autumn and winter they were similar (Figure 2a). Chlorophyll a was higher in spring and summer (Figure 2f) and the pH was also higher in spring and summer (Figure 2d). Mean wind speed in the 24h period was higher in winter, reaching 11 m s^–1 (Figure 2b), while mean precipitation, for seven days previously each period sampled, ranged from 0.1 mm day^–1 in the winter to 16.8 mm day^–1 in the autumn, with 9.5 mm day^–1 and 3.0 mm day^–1 in spring and summer, respectively. Meteorological variables, e.g. wind and PAR showed high variability, 39 and 52%, respectively; while limnological variables in Figure 2 showed variability lower than 10%.

3.2. pCO₂ and pO₂

Figure 3 shows the diel and seasonal variability of pCO₂ and pO₂. Along the 24 hours, pO₂ showed a similar pattern in all periods sampled, with a maximum pO₂ at 15:00 h (in summer the pO₂ increased until 18:00 h, Figure 3b). For pCO₂ no clear pattern was observed, and high variability was recorded (29%), with some periods of pCO₂ decrease during the day and increase during the night (Figure 3a). The variation in both gases showed that, in general, pCO₂ is undersaturated in spring and summer, suggesting a CO₂ uptake from the atmosphere, while in autumn and winter, pCO₂ values suggest a release from the lake to the atmosphere. On the other hand, pO₂ was always below saturation level and showed low variability (3%).

In autumn and some periods of summer, we observed an inverse relationship between pCO₂ and pO₂, as expected, since the biological production of a gas requires the consumption of another. In other periods, this relationship was not clear. In general, pCO₂ and pO₂ maintained a negative relationship, although it was not statistically significant (r=–0.36, p>0.05; Table 1). The strong correlation between pO₂ and DO is because this variable was used to calculate the O₂ partial pressure; the same is valid to pH relative to pCO₂. Water temperature and chlorophyll a were also negatively correlated with pCO₂, while pO₂ was positively correlated with wind and PAR (Table 1).

4. Discussion

Our data was recorded in only four days along 2010-2011, but it was possible to observe important environmental variations, especially meteorological ones (e.g. wind, PAR and precipitation), and their influence in the metabolism of a subtropical environment. Even though the limnological variables seem not to be directly influenced by wind and PAR, due to the low variability recorded, pCO₂ showed a high variability, in accordance with the variability of biological process. Thus, we confirmed our first hypothesis, since high variability of pCO₂ over the course of both the day and the year was recorded.

The variation observed in pO₂ along 24 hours was similar in all periods sampled, increasing along the morning showing maximum values in mid-afternoon, and decreasing at night. This diel variation follows the variation in water temperature, pH and PAR availability, and these variables are associated with photosynthesis (Boehrer and Schultze, 2008; Kosten et al., 2010). Even tough photosynthesis varies along the day, the heterotrophic bacterioplankton also changes in a diel cycle (Fontes et al., 2013), related to environmental condition, thus influencing the variability of the pCO₂, as observed and recorded in tropical lakes (Marotta et al., 2012).

Opposite to pO₂, the pCO₂ had no clear diel pattern, even though we found a negative correlation between water temperature, chlorophyll a and pCO₂. Although biological activity is important on regulating CO₂ and O₂ gases, physical forces, such as solar radiation, heat loss and wind, will also influence the turbulence of the water column and depth of the surface mixed layer, which will act over the gas exchanges in the lake-air interface (Read et al., 2012). Since the correlation between pCO₂ and pO₂ was weak, other processes may be contributing to CO₂ and O₂ saturation in the water column, such as organic matter photooxidation, intrusion of supersaturated groundwater, and wind action (Kling et al., 2001).

We are aware that lakes generally present differences between pelagic and littoral zones, and that shallow areas are more influenced by benthic processes than pelagic zones (Staehr et al., 2012; They et al., 2013). However, our aim here was the temporal variability specifically in the littoral zone, since no spatial variation of pCO₂ and pO₂ in nutrients and chlorophyll a was recorded in Peri Lake (Hennemann and Petrucio, 2011).

The known characteristics of the Peri Lake, such as low phosphorus concentration, Cyanobacteria dominance, nutrient and light limitation (Tonetta et al., 2013) suggest a persistent heterotrophic condition (Cole et al., 1994). However, the high water temperature and PAR in summer favored autotrophic instead of heterotrophic activities, increasing pH and resulting in lower pCO₂ in the water compared to the atmosphere. The autumn and winter may be considered as having high heterotrophic biological activity, since pH was low and higher pCO₂ in the water than in the atmosphere was recorded. Thus, our second hypothesis was not confirmed, since there were shifts between autotrophic and heterotrophic periods. This high variability in pCO₂ is similarto the one observed in tropical lakes (Marotta et al., 2009).

Besides PAR and wind were positively correlated with pO₂, precipitation also influenced the biological processes, increasing pCO₂. The highest precipitation was recorded in autumn, what promoted organic matter inputs and decreased water transparency, consequently lowering photosynthesis and resulting in high heterotrophic activity and the highest pCO₂ in this period. Precipitation is a common variable leading the aquatic metabolism to net heterotrophy (Lennon, 2004), even in tropical lakes (Marotta et al., 2010).

Transitions between autotrophy and heterotrophy are mostly known to be controlled by changes in limnological variables, especially phosphorus, dissolved organic carbon, light attenuation, and by living organisms inhabiting the system (Loebl et al., 2007; Hagerthey et al., 2010; Montero et al., 2011). Even though tropical lakes have been pointed out to act as important CO₂ sources to the atmosphere (Marotta et al., 2009), our findings demonstrate the importance of meteorological variables driving limnological conditions. Consequently, shifts in aquatic metabolism along the year are found, as has been recorded in other subtropical (Carmouze et al., 1991; Thomaz et al., 2001) and temperate lakes (Staehr et al., 2010).

Whether the entire lake ecosystem is net autotrophic or heterotrophic on a yearly basis remains unclear, and sampling in short-term can improve our understanding about carbon cycling in this environment. However, this high variability illustrates that subtropical lakes can be very dynamic concerning the carbon cycle, where in some periods, Peri Lake is a source of CO₂ to the atmosphere, while in others; it stores the CO₂ as organic carbon. Thus, in Peri Lake the meteorological conditions were strongly responsible for changes in pCO₂ and pO₂, through their influence on terrestrial inputs of nutrients and carbon into aquatic ecosystems and light availability.

Acknowledgements

We are grateful to Danilo Funke (FLORAM/Parque Municipal da Lagoa do Peri), Alex Pires De Oliveira Nuñer (LAPAD – UFSC) and the PPGECO (Programa de Pós-graduação em Ecologia) for providing assistance in the field and lab equipments. This study was funded by CNPq – Brazil (Conselho Nacional de Desenvolvimento Científico e Tecnológico, Universal Process: 473572/2008-7) and the first author was supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).

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Received: 12 February 2014

Accepted: 18 August 2014

• BARBOSA, FAR. 1997. The importance of diurnal cycles for the conservation and management of tropical waters: examples from the Rio Doce Valley lakes system. In TUNDISI, JG. and SAIJO, Y., ed. Limnological Studies on the Rio Doce Valley Lakes, Brazil São Carlos: Brazilian Academy of Sciences. p. 449-456.
• BOEHRER, B. and SCHULTZE, M. 2008. Stratification of lakes. Reviews of Geophysics, vol. 46, no. 2, p. 1-27. http://dx.doi.org/10.1029/2006RG000210
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Publication Dates

• Publication in this collection
  18 Nov 2014
• Date of issue
  Sept 2014

History

• Received
  12 Feb 2014
• Accepted
  18 Aug 2014