Continuous and High-Frequency Measurements in Limnology: History

52 REVIEW

Continuous and high-frequency measurements in limnology: history, applications, and future challenges Pille Meinson, Agron Idrizaj, Peeter Nõges, Tiina Nõges, and Alo Laas

Abstract: Over the past 15 years, an increasing number of studies in limnology have been using data from high-frequency measurements (HFM). This new technology offers scientists a chance to investigate lakes at time scales that were not possible earlier and in places where regular sampling would be complicated or even dangerous. This has allowed capturing the effects of episodic or extreme events, such as typhoons on lakes. In the present paper we review the various fields of limnology, such as monitoring, studying highly dynamic processes, lake metabolism studies, and budget calculations, where HFM has been applied, and which have benefitted most from the application. Our meta-analysis showed that more than half of the high-frequency studies from lakes were made in North America and Europe. The main field of application has been lake ecology (monitoring, lake metabolism) followed by physical limnology. Water temperature and dissolved oxygen have been the most universal and commonly measured parameters and we review the various study purposes for which these measurements have been used. Although a considerable challenge for the future, our review highlights that broadening the spatial scale of HFM would substantially broaden the applicability of these data across a spectrum of different fields.

Key words: lake metabolism, temporal variability, spatial variability, extreme events, hydrodynamics. Résumé : Au cours des 15 dernières années, on observe un nombre croissant d’études en limnologie ayant utilisé des données provenant de mesures a` hautes fréquences (HFM). Cette nouvelle technologie offre aux scientiﬁques la possibilité d’étudier les lacs a` des échelles de temps qui étaient impossibles auparavant et dans des endroits où l’échantillonnage serait compliqué ou même dangereux. Ceci a permis de saisir les effets d’événement épisodiques ou extrêmes, tels que des typhons sur des lacs. Les auteurs passent ici en revue différents champs de la limnologie tels que le suivi, l’étude de processus hautement dynamiques, l’étude du métabolisme des lacs ainsi que le calcul des budgets, où on a appliqué la HFM et qui ont le plus bénéﬁcié de cette application. La méta-analyse des auteurs montre que plus de la moitié des études conduites en hautes fréquences dans des lacs l’ont été en Amérique du Nord. Le principal champ d’application a concerné l’écologie des lacs (suivi, métabolisme des lacs), suivi de la limnologie physique. La température et l’oxygène dissout constituent les paramètres les plus universels et communément mesurés et les auteurs passent en revue les objectifs des diverses études pour lesquels ces mesures ont été utilisées. Bien que ceci

For personal use only. constitue un déﬁ considérable pour le futur, cette revue souligne que l’élargissement de l’échelle spatiale des HFM élargirait substantiellement l’applicabilité des données pour un ensemble de champs différents. [Traduit par la Rédaction]

Mots-clés : métabolisme des lacs, variabilité temporelle, variabilité spatiale, évènements extrêmes, hydrodynamiques.

1. Introduction automatic high-frequency measurements (HFM). Even though automatic recording is vulnerable to vandalism, biofouling, Today, global environmental change and the increasing exploi- and occasional failures in the systems, and maintenance issues tation of ecosystem services by man has created complex multiple may causes gaps in time series data (Dur et al. 2007), a fast transi- stressor situations for most inland water bodies (Ormerod et al. tion to automatic HFM in environmental monitoring systems is 2010). This has obviated the need for more and better monitoring inevitable. data and is a prerequisite for understanding the often synergistic, The need for continuous observations has led to automating cumulative, and non-linear impacts of combined stressors (Brown measurements since the early times of limnology. In the first et al. 2013) and for making adequate management decisions report of the Indiana University Turkey Lake Biological Station (Hering et al. 2015). Until recently, the majority of standard lake (the first inland biological station in America), its director, monitoring programs were based on manual in situ measure- C.H. Eigenmann, mentioned, among other equipment, an “auto- ments that can be time-consuming and costly to procure and matic recording apparatus to observe seiches” (Eigenmann 1895, often lack both the necessary spatial coverage as well as an appro- p. 207). In the same year, Warren and Whipple (1895, p. 639) in- priate sampling frequency (Vos et al. 2003). The latter is especially troduced the thermophone, “a new instrument for obtaining the important for detecting the effects of hydrology or weather- temperature of a distant or inaccessible place,” and provided related episodic events, from which biological consequences can some temperature profiles measured in Lake Cochituate, Mass. range from short-term, reversible changes to those that are more Simple physical parameters, such as lake water levels and water Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 persistent (Jennings et al. 2012). Time and reliability issues can be temperature, were among the first limnological variables for efficiently addressed by replacing manual measurements with which measurement could be automated. Parameters recorded in

Received 26 May 2015. Accepted 5 October 2015. P. Meinson,* A. Idrizaj, P. Nõges, T. Nõges, and A. Laas. Centre for Limnology, Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, 61117 Rannu, Tartu County, Estonia. Corresponding author: Pille Meinson (e-mail: [email protected]). *Present address: Kreutzwaldi 5, Tartu 51014, Estonia.

Environ. Rev. 24: 52–62 (2016) dx.doi.org/10.1139/er-2015-0030 Published at www.nrcresearchpress.com/er on 6 October 2015. Meinson et al. 53

physical meteorology, such as air temperature, humidity, wind confront the information management and analytical challenges speed and direction, and the amount of precipitation served as posed by massive volumes of data, while Porter and Lin (2013) important background data supporting lake research (Porter et al. specifically focused on available hybrid wireless sensor network 2005). However, soon the development of electrochemistry — the technologies. Johnson et al. (2007) reviewed the chemical sensing invention of the glass electrode by Cremer (1906) and the intro- capabilities with a special focus on such chemical sensor net- duction of the concept of pH by Sørensen (1909) — gave an impe- works that can be deployed on autonomous platforms in aquatic tus to the development of various chemical sensors initially environments and then operated without significant human in- enabling automatic recording of a number of single charged ions, tervention for extended periods. Crawford et al. (2015) analyzed + + + such as H ,Na ,NH4 , proved soon as limnological key variables. the potential of using advanced sensors to investigate spatial vari- The oxygen electrode widely used in aquatic studies measuring ability in biogeochemistry and hydrology. Besides Porter et al. oxygen on a catalytic platinum surface was invented by Leland (2005), which gives a broad picture of HFM applications in envi- Clark in 1954, initially for blood gas analysis (Severinghaus and ronmental studies, some reviews give more specific insights into Astrup 1986). While chemical sensors still cannot fully compete to the use of high-frequency (HF) data in lakes. For example, with physical sensors regarding their cost or reliability, a variety Jennings et al. (2012) analyzed the potential of HFM for identifying of chemical sensing systems (e.g., for carbon dioxide, pH, and the effects of weather-related episodic events in lakes, whereas oxygen and a number of ions) are now continuously deployed in Staehr et al. (2010) reviewed the use of the diel oxygen technique aquatic environments (reviewed by Johnson et al. 2007). for studying lake metabolism. A big leap in environmental measurement and monitoring In the present paper we review various fields of limnology and technologies came with the transition from analogue to digital lake management that have benefitted or potentially may benefit technologies from the late 1990s to the early 2000s (Hilbert and from using HF measurements, in the hope of stimulating addi- López 2011). Thanks to fast technological development, the auton- tional use of this promising technology. We highlight the advan- omy of different measurement systems has increased. Using wire- tages of using HFM for various purposes compared to discrete or less systems allows retrieving data from the weather and water manual sampling, but also discuss the challenges. We put the monitoring stations in near-real time and without manually vis- main focus on HF data applications related to buoy and mooring iting the study site (Porter et al. 2005). The development of sensors systems and do not discuss other fields of HF technologies, such as has made progress by taking under consideration the protection SONAR, eco-sounding, ADCP or remote-sensing systems. We have from biofouling (Manov et al. 2004) using self-cleaning systems reviewed 154 papers using HFM in lakes and grouped the studies (e.g., wipers or pressure). After reviewing the recent develop- according to their limnological or lake management issues (i.e., ments in HFM systems, sensor technologies and networking in measurement objectives rather than technical parameters of the limnology, Crawford et al. (2015) emphasized the new and unex- study design). Although the list of papers is not exhaustive, it is pected insights into ecosystem processes that would have been representative and sufficiently large to give a broad overview of impossible with previous techniques. Nevertheless, the authors the various applications using HFM in limnology. show that despite the fact that sensor technology is becoming common in limnological research, current applications focus al- 2. Literature search most entirely on temporal patterns and variation while spatial For the literature search, we used the Google Scholar citation variability is rarely documented because of the high investment database. Queries were made using search terms “lake*” and costs for the spatial replication of such infrastructure. “high frequency data”. To focus on recent research only, we re-

For personal use only. The amount of data that can be generated from HFM is huge stricted the time window to the past 15 years (i.e., only articles even if only one set of sensors is deployed in a lake for time published between 2000 and 2015 were considered). Screening of periods of several days or months. Globally, the HFM data from the 1480 papers retrieved revealed the main fields of HFM appli- lakes add volume, velocity, variety, resolution, and relational na- cation for which we repeated more specific queries using as ture, the so-called three Vs and two Rs of big data (Kitchin 2013), search terms “lake*” and “high frequency” in combination with and so dealing with these data are challenging. At the same time, one of the following terms: “monitoring”, “early warning”, “me- more data may lead to more accurate analyses and the high reso- tabolism”, “budget”, “flux”, “migration*”, “sampling design”, “ex- lution allows insights into highly dynamic processes (Coloso et al. treme event*”, and “patchiness”. The first 100 results of each 2008; Schwientek et al. 2013). retrieval were screened for their relevance resulting in a total of Besides challenges related to costs of assessing spatial variabil- 1730 records. Further, we selected studies in which measurement ity and organizing, cleaning, and processing large datasets, other intervals of ≤60 min were used and the deployment time was at challenges exist for HFM including resolution and response time least 6 h. As we could not find any commonly agreed-upon defini- of certain electrochemical sensors (e.g., for pH and dissolved tion for HFM, we set the arbitrary 60 min upper limit for the oxygen (DO)) creating problems for using them in profiling instru- measurement interval considering this the coarsest resolution ments (Taillefert et al. 2000; Tengberg et al. 2006), and the photo- still allowing to follow the diurnal dynamics of processes. Papers bleaching issues with fluorescence sensors (Johnson et al. 2007). using measurement intervals longer than1hordeployment times As Cushing (2013) noticed, the exponential growth in data ac- less than 6 h were excluded from our results. This screening quisition and progress in data documenting, archiving, valida- yielded a final list of 154 papers that met our criteria and were tion, and retrieval have made more (in quantity and diversity) and used as the basis of the present review. better (less “dirty”) data available to scientists. The Global Lake Ecological Observatory Network (GLEON) is a prime example of a 3. Review table lake and data network, sharing and interpreting high-resolution

Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 Relevant information from the papers was extracted to an Excel sensor data from a broad spectrum of lakes across the globe to table to enable future search by meta-analysis. Each article was understand, predict, and communicate the role and response of described in a separate row of the table (154 papers) starting with lakes in a changing global environment (Weathers et al. 2013). a full reference in the first column. A set of 11 parameters, some of Various aspects of using HFM in environmental sciences, in- them with predefined categories, was used to extract important cluding limnology, have been analyzed in a number of earlier information from the papers: review papers. Porter et al. (2005) reviewed some existing uses of wireless sensor networks in environmental sciences, possible ar- 1. Number of lakes and lake type including stratification (strat- eas of application, and the underlying technologies. Porter et al. ified, non-stratified) and trophic state (5 cat.) (2012) provided a synopsis of innovative approaches being used to 2. Geographic location (continent, 7 cat.)

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Fig. 1. Split-off of HF studies by object, subject, and space–time scale. Geographical distribution (a) and ﬁeld of study (b), types of measured parameters (c), space–time scale (d), lake categories by stratiﬁcation (e), and trophic state (f). For personal use only.

3. Field of study (physical limnology, geochemical limnology or 2D horizontal, time series measured at one depth along a tran- lake ecology) sect (e.g., the FerryBox systems) 4. Main purpose of applying HFM (12 cat.) 3D, time series measured at one depth over an area (e.g., poly- 5. Type of parameters measured (meteorological, hydrophysical/ gon measurements) or at several depths along a transect (e.g., optical, hydrochemical, biological) robot fish measurements) 6. Parameters measured (23 cat.) 7. Last year of data collection The table included three types of entries: 8. Year of publication 1. (Free) text columns were used for the full reference and the 9. Temporal scale of study (5 cat. from <1 day to multiannual) lake names, comments. Several initially free text variables, Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 10. Temporal resolution (measurement and aggregation interval, such as temporal resolution, measured parameters, geograph- minutes) ical distribution, and trophic state, were categorized after- 11. Space–time scale wards and included as multiple-choice variables. To describe the space–time scale of the measurement design, we 2. Numerical entries were used for publication year, length of used the following categories: publishing cycle, and temporal resolution of study. 3. Number 1 was used as a tick-mark denoting “Yes” for selecting 1D, time series measured at one station at a single depth one (or more) of the multi-choice columns under different 2D vertical, time series measured at one station in a vertical categories (year of study, temporal and spatial scale of study, profile (e.g., profiling buoys and sensor chains) geographical distribution, field and main purpose, trophic

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Fig. 2. Distribution of the reviewed literature by year of publication and period of data collection.

state and stratification, measured parameters, and temporal Fig. 3. Length of the period from the end of data collection to resolution of study). publication. Cells were left empty if the choice was “No”. For trophic state and stratification we added field “NA” (not applicable). 4. Meta-analysis The meta-analysis was based on numerical variables, such as the year of publication, and counting the numbers of entries in

For personal use only. categorical multiple-choice variables. To assess the significance of differences between proportions of various categories within a population, a Z-test was used, available online at http://www. socscistatistics.com/. 5. Patterns in applying HFM in limnology From a geographical point of view, almost 40% of HF studies were undertaken in North America, which was 1.4 times more than in Europe (Fig. 1a) followed by Asia with 18%. Review papers including data from several continents made up 5% of the studies, whereas the smallest number of studies originated from Africa. The number of publications per year analyzed applying HFM had an increasing trend and the maximum was reached in 2012 (Fig. 2). In 2008, the number of HF studies was significantly higher compared to both neighboring years (z-score > 2.3; p < 0.05). The The majority of studies using HFM were made in lake ecology citation report generated for our search terms by the ISI Web of (56%) covering fields, such as low-maintenance monitoring and Knowledge showed similar patterns, although the number of HF lake metabolism measurements, followed by physical limnology studies in 2008 was significantly higher only compared to 2007 (28%) dealing with hydrological processes and different water (z-score > 2.2; p < 0.05) while the difference with 2009 remained movements (e.g., internal waves, currents, and seiches), and stud-

non-signiﬁcant. ies in geochemical limnology (sensor measurements of CO2, ni- Since the 1990s until 2009, there has been an increasing trend in trates, etc.; 16%) (Fig. 1b). the amount of collected HFM data represented in the publications A substantial part of measured parameters were meteorological Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 analyzed. HFM data collected in 2005 and in the period from 2008 variables (44%; e.g., air temp, wind speed, etc.) (Fig. 1c). A notice-

to 2010 have been most represented in publications so far, able 30% of measured parameters were hydrochemical (e.g., CO2, whereas data collected during recent years are still in the prepa- etc.). Hydrophysical and optical parameters formed 19% of ration phase (Fig. 2). the parameters measured while biological parameters, such as Most often it took between 2 and 3 years after the study period chlorophyll a, phycocyanin, and phycoerythrin, were least until HFM data ﬁrst appeared in publications, although 1 year and studied (7%). 4–5 year publishing cycles were rather common too (Fig. 3). Al- We distinguished 12 main purposes for which HFM have been though older data were often used as part of the database, only a used at different frequencies (Fig. 4). Most often HFM have been few papers were entirely based on data older than 5 years. used for low-maintenance monitoring (e.g., water temperature)

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Fig. 4. Frequency distribution by study purpose.

Fig. 5. Temporal scales used in studies. Fig. 6. Temporal resolution by measurement interval (minutes). For personal use only.

quality variables (conductivity, pH, turbidity). Chlorophyll a was and collecting meteorological background data. Lake metabolism more common in HFM programs than other biological parame- studies using HF data have been growing in number in recent ters (e.g., phycocyanin or phycoerythrin). Measurements of chem- years and occupied the third position. There are still rare topics ical parameters (e.g., NO3,PO4) were rare. where HFM are applied (e.g., developing sampling strategies or Almost 60% of the studied lakes were described as thermally calibrating remote-sensing data). stratified and 24% as unstratified, while in 17% of the lakes the Most often studies were performed in time scales from >1 month stratification remained ambiguous. Among the lakes with trophic to 1 year, being about twice as frequent as multi-annual studies state indicated, eutrophic and oligotrophic lakes formed equally and those lasting from >1 day to 1 month (Fig. 5). Diurnal and 40% followed by mesotrophic (15%), hypereutrophic (5%), and dys- shorter time scales were least used. trophic (3%) lakes (Figs. 1e and 1f). Most of the studies were based on single point HFM in vertical profiles (2D vertical in a space–time scale), 31% on single point – 6. Explanation for the patterns revealed single depth time series (1D), followed by profile (3D) and single According to our meta-analysis, more than two-thirds of the HF depth measurements along transects (2D horizontal) (Fig. 1d). studies in lakes were carried out either in North America or Eu- Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 The length of the measurement interval used in studies had a rope (Fig. 1a) that, on one hand, reflects the global distribution of nearly bimodal distribution with peaks at <1 min and at 10 and lakes peaking in the northern temperate zone between 40°N and 15 min, but also 5, 30, and 60 minute intervals were widely used 70°N (Lehner and Döll 2004). Studies involving up to 25 lakes have (Fig. 6). In some papers HFM were aggregated, most often to 10 and been carried out both in the U.S.A. (Hanson et al. 2003; Langman 60 min or 24 h. et al. 2010) and in Europe (Staehr et al. 2012). On the other hand, Water temperature was the parameter most often measured, this distribution is strongly influenced by the global distribution while measurements of DO concentration took the second posi- of scientific research potential. As shown by King (2004) in a com- tion (Fig. 7). These two main parameters were followed by some prehensive review of the scientific impact of nations for the pe- meteorological (e.g., wind speed, air temperature, PAR) and water riod 1993–2001, USA and the EU15 of that time headed the list,

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Fig. 7. Parameters studied with HFM.

whereas Japan had the highest number of full-time researchers ment intervals <1 min (Fig. 5) are often used to study dynamic per 1000 employed. Nowadays, the contribution of China to world hydrological processes using sensitive water temperature sensors. science is in a fast growing phase (Zhou and Leydesdroff 2006). MacIntyre et al. (2002) measured water temperature every 30 s Among HF studies in lakes that we analyzed, Asian papers occu- with 14 sensors to study surface layer deepening and lateral ad- pied a decisive third position with 18%. Studies including data vection in Lake Victoria (Africa). Internal waves with periods of from several continents (termed by us as ‘Global’, e.g., Read et al. 5–45 min were generated during relaxation from wind forcing 2012; Solomon et al. 2013) constituted 5% of studies. and as the thermocline rapidly downwelled. HF water tempera- As our analysis revealed, more studies used 2D vertical mea- ture measurements have also been used in other large lakes for surements compared to just single depth sensors. One could ex- studying internal waves (e.g., Boegman et al. 2003; Lorke et al. pect the latter to be more common given their likely lower cost 2006; Lorke 2007), benthic boundary mixing (Hondzo and Haider, and greater reliability due to the lack of a cable winding system 2004) and to develop circulation models for lakes (Laval et al. often used to raise and lower sensors in the water column. Verti- 2003). Using HFM of temperature profiles for studying lake mixing For personal use only. cal 2D measurements involve not only profiling buoys (that are (Kulbe et al. 2008; Shade et al. 2010; Read et al. 2011a; Kimura et al. really expensive and therefore not so widely used), but also simple 2014; Pernica et al. 2014; Bertone et al. 2015) and stratification sensor chains (e.g., thermistor chains) and all cases where sensors processes (Pernica and Wells 2012; Song et al. 2013; Sullivan et al. were deployed at more than one depth, being a common practice 2013) has been common practice. in stratified lakes strongly predominating in the selected studies. Besides hydrological processes, HF temperature data allow cal- Another reason explaining the predominance of 2D studies is that culating heat flux and energy balance of lakes. Lakes affect the if some parameters were measured vertically and some at a single climate at scales ranging from local to global, but these effects are depth, we indicated the spatio-temporal dimension as 2D. Analys- often neglected in models (Ljungemyr et al. 1996). To improve the ing the use of 1D and 2D vertical data in lake metabolism calcula- understanding of the intra- and inter-annual dynamics of the heat tions, Staehr et al. (2012) pointed out that measurements with a balance components on a boreal lake, Nordbo et al. (2011) studied single sensor in the surface layer tend to overestimate gross pri- the thermal structure of a small lake in Finland over several years mary production and community respiration while measure- using HF temperature profile measurements to calculate the heat ments in two layers give more truthful results. A single sensor storage change of the lake. Heat and mass balance calculations are may overlook important heterogeneity within lake processes and also important for monitoring volcanoes with heated crater lakes, may not accurately represent system-wide values of metabolism as they reflect the mass and thermal fluxes from the volcanic (Van de Bogert et al. 2012). vents into the bottom of the lake, as an indication of the state of 6.1. Versatile and universal use of simple parameters the underlying volcano (Hurst et al. 2012). Because evaporation Our review of the published literature found that HFM of water can be substantially affected by the lake’s influence on the air- temperature were most common. High reliability, long auton- mass above it, HF air and water temperature measurements can omy, low maintenance need, and reasonable prices of tempera- help to specify the seasonality of evaporation in crater lakes ture sensors have certainly contributed to their wide application; (Redmond 2007; Hurst et al. 2012). Climate warming increases the Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 however, the main reasons lie in the possibility of using temper- thermal stability of lakes with implications for chemical and ature as a marker of water masses and in the universal nature of biological processes (Weinberger and Vetter 2014). Using HF temperature as a controlling factor of chemical and biological moored thermistor records and meteorological data, Churchill processes. and Kerfoot (2007) studied the impact of surface heat flux and Because of the high specific heat content of water, it warms up wind on thermal stratification in Portage lake, Michigan. Pierson and cools down relatively slowly, which allows using water tem- et al. (2011) developed a simple method to automatically detect the perature as a marker of water masses to study various water move- presence of ice cover by continuously recording water tempera- ments (currents, internal waves, and seiches), but also mixing, ture just below the ice–water interface and just above the lake stagnation, and stratification of water masses. HFM with measure- bottom using moored temperature sensors.

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Only by applying HF measurements has it become possible to nighttime mixing (Branco and Torgersen 2009). Other examples follow in detail the effects of extreme weather events on lakes. For of using HF DO data in lakes include its application as an indicator example, Jennings et al. (2012) analyzed the effects of weather- of the presence of biodegradable organic pollution (Ansa-Ansare related episodic events in seven lakes from Europe, USA, and et al. 2000), studying the efficiency of artificial destratification Taiwan based on high- and moderate-frequency data. They distin- (Read et al. 2011b), describing temporal dynamics of DO in a float- guished two classes of abiotic effects of weather events: the gen- ing leaved macrophyte bed (Goodwin et al. 2008), and assessing erally short-lived effects of storms affecting lake thermal the effect of summer warming on DO conditions (Wilhelm and structure and the more prolonged effects of high rainfall events Adrian 2008). on dissolved organic matter levels and water clarity. Episodic Other sensors often included in a standard set of water moni- events, such as hurricanes and storms have a great impact on both toring probes are pH and conductivity sensors. The relationship coastal areas (Chang and Dickey 2001) and lakes (Tsai et al. 2008, between DO and pH depends upon the system and the time scale: 2011; Shade et al. 2010) by disrupting the thermal stratification in bottom waters of relatively deep regions in Lake Victoria structure and redistributing biogenic and nonbiogenic matter. Alexander and Imberger (2013) found similar trends in these two Using a network of HF, in situ, automated sensors, Klug et al. variables, while Karakaya et al. (2011) and Reeder (2011) described (2012) document the regional effects of Tropical Cyclone Irene on strong correlation between diel changes in DO and pH, corre- thermal structure and ecosystem metabolism in nine lakes and spondingly, in a shallow lake in Turkey and in open-water habi- reservoirs in northeastern North America. The fast decline of ther- tats in the Beaver Creek Wetlands Complex in Kentucky (USA). mal stability was related to the amount of precipitation on the Data on pH are used as a background characteristic (e.g., Hemond lake and the catchment area while the temperature change pre- et al. 2008; Bertone et al. 2015), as an environmental factor (e.g., dicted the change in primary production across all systems. HF Rubbo et al. 2006; Karakaya 2011) or used in equations for car- temperature measurements have also provided important details bonate balance (e.g., Rudorff et al. 2011), redox calculations of the effects of the 2003 and 2006 heatwaves in Europe on the (Hamilton-Taylor et al. 2005) or the proportion of toxic unionized thermal structure of lakes (Choin´ ski and Łyczkowska 2008; Jöhnk ammonia (Gelda and Effler 2003). Conductivity data often col- et al. 2008; Kulbe et al. 2008; Wilhelm and Adrian 2008). lected within a standard water quality monitoring program Water temperature is a ubiquitous factor affecting most chem- belong mostly to descriptive background data and have been ical and biological processes in aquatic environments (Regier et al. addressed independently in few lake studies. Conversely, in 1990; Poff et al. 2002), and thus combining chemical or biological brackish environments, such as estuaries, conductivity is the measurements with HFM of temperature opens up new perspec- main parameter to distinguish between different water masses tives for interpretation. Jones et al. (2008) explored patterns of (Trevethan et al. 2007; Smith et al. 2008). Temporally and spatially change in bacterioplankton and phytoplankton community com- dynamic salinity levels in a reservoir resulting from the mixing of position in response to typhoons in a freshwater humic lake in waters from two different tributaries, were reported by Atkinson Taiwan and found that after each typhoon-induced mixing event, and Mabe (2006) using a mobile water quality probe from a small the bacterial community composition revealed a deterministic boat and recording the sampling trajectory by the global position- pattern of recovery with distinct bacterial assemblages being as- ing satellite (GPS) system. Also Lindfors et al. (2005) used a flow- sociated with epilimnion and hypolimnion. In contrast, phyto- through system operated from a boat to map the water masses in plankton communities did not recover in a predictable way after their study area. typhoons. Baulch et al. (2005) studied whether warming could HF recordings of dissolved nutrient levels, such as nitrates

For personal use only. stimulate respiration and light-saturated photosynthetic rates in (NO −) and phosphates (PO 3−), in lakes are scarce, although ni- the epilithon. Water temperatures were monitored every 15 min 3 4 trate levels are often measured in rivers (Sherson 2012; Feng et al. in experimental enclosures and in the lake using continuously 2013; Sherson et al. 2015). The advantage of using continuous mea- recording thermocouples. Good agreement found between long- surements for nitrates stems from their remarkable diurnal vari- term and experimental results suggests that increased tempera- ability (Feng et al. 2013) that can be easily overlooked with discrete tures will increase metabolic rates of the epilithon. measurements (Schwientek et al. 2013). The detection limit of Fishes often exhibit clear temperature preferences. Comparing temperature profiles with fish distribution data in Lake Lesjask- phosphate sensors is mostly around 50–100 ppb but has been ogsvatnet (Norway), Bass et al. (2014) showed that during stratifi- lowered to 5 ppb (Karube and Nomura 2000) or likely even more cation, European grayling, Thymallus thymallus preferred to stay (Ohio Lake Erie Protection Fund 2010) and that of nitrate to withina2mzone around the thermocline supposedly driven by 6.2 ppb (Myers et al. 2012) making them potentially applicable for foraging opportunity. lakes. Nitrate measurements with an optical sensor in a reservoir DO was the second most often measured parameter using HFM where nitrate concentrations ranged from <0.1 mg N/l to >4 mg N/l, (Fig. 7). Continuous online DO measurements are routinely ap- gave highly consistent results with laboratory measurements. plied in aquaculture (e.g., Xu et al. 2006) and for effluent monitor- 7. HFM versus conventional sampling ing (e.g., Bourgeois et al. 2001), remaining, however, outside the scope of our review. In lakes, calculating lake metabolic variables HFM nicely illustrates Hegel’s dialectical principle of the (gross primary production, community respiration, and net eco- transition from quantity to quality. Increasing measurement system production) from diel DO curves in the open water has frequency has enabled accounting for natural variability in mon- become increasingly popular and has been used in a large number itoring data and selecting optimum sampling frequencies for cost- of studies (e.g., Cole et al. 2000; Lauster et al. 2006; Staehr et al. effective representative sampling (Anttila et al. 2012). Although 2010; Tsai et al. 2011; Laas et al. 2012; Klotz 2013; Alfonso et al. manual monitoring frequencies may prove sufficient for certain Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 2015). Recently, the uncertainty issues of lake metabolism mea- purposes, a comparison with HFM data enables an uncertainty surements have been addressed in a number of studies (Batt and estimate even for historical data that improves data reliability. Carpenter 2012; Cremona et al. 2014). Based on DO observations Besides the already mentioned studies on episodic events and the derived from in situ sensors in 25 northern temperate lakes, opportunities to register and follow dynamic processes at time Langman et al. (2010) showed that at scales, ranging from minutes scales of hours and minutes, there is clear evidence of HFM data to days DO patterns were affected by a number of physical and providing a greater understanding of certain processes, first of all biological processes, such as internal waves, mixing, and ecosys- in lake metabolism. Compared to bottle incubation techniques tem metabolism. In small, shallow, inland water bodies, a diurnal encompassing only processes in the plankton community, the DO pattern can be affected by daytime thermal stratification and freewater, depth-weighted approach in estimating ecosystem me-

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tabolism takes into account primary production of all autotrophs 9. New challenges and directions and respiration of all lake biota, including benthic and possibly 9.1. Broadening the spatial scale of HFM littoral habitats depending on the location of the buoy, however, Application of sensor technology has considerably shifted the accounting for the effects of turbulence within the water column lower-end boundaries of temporal resolution in limnological remains one of the largest methodological challenges (Sadro et al. studies, shedding light upon diurnal, hourly, and even shorter 2011a, 2011b). Furthermore, HFM can be used in remote locations scale processes. The length of time series from automated buoy and severe conditions where conventional measurements would stations has in places exceeded 10 years (e.g., Pierson et al. 2011) be complicated. For example, Sadro and MacIntyre (2014) mea- allowing assessment of year-to year variability of physical and sured spatial and temporal patterns in the ecosystem respiration chemical lake environments. However, as shown by Crawford of five Alaskan lakes that stay covered by up to3moficeandsnow et al. (2015), spatial variability is rarely documented with sensors for approximately two-thirds of the year, and described two mech- because of the high investment costs for the spatial replication of anisms operating in tandem accounting for the DO drawdown such infrastructure. Still the use of profiling buoys is an emerging patterns found within lake basins during the winter. trend over the past years that has likely been promoted by de- Applying HFM on boats or other moving vessels allows turning creasing instrumentation prices. A slow transition from one- the high temporal resolution into high spatial resolution provid- station measurements to multi-station measurements per lake in ing unique tools for studying horizontal distribution patterns of metabolism studies can also be seen (e.g., Van de Bogert et al. variables at scales never achievable by means of conventional 2007, 2012; Coloso et al. 2008; Sadro et al. 2011b) allowing to at least field measurements. These studies can address specific scientific partially include spatial variability aspects. Broader use of mobile issues, such as plankton patchiness (Anttila et al. 2008), elucidate on-board novel flow-through systems, such as the fast limnology basic hydrological mechanisms at relatively low costs of invest- automated measurement (FLAMe) platform (Crawford et al. 2015), ments and manpower (Schwientek et al. 2013) or can be used for equipped with various sensors and combined with GPS and an calibrating remote sensing data to produce a better picture of the acoustic eco-sounder, allows for fast surveys of extensive water processes taking place in the study area (Lindfors et al. 2005). bodies that can serve for calibrating remote sensing data (e.g., Combined with modelling, HF data can inform early warning sys- Östlund et al. 2001; Lindfors et al. 2005), studying patchiness, and tems of the occurrence of cyanobacteria in drinking water sources optimizing monitoring networks (Anttila et al. 2008). A combina- using phycocyanin probe (Izydorczyk et al. 2005; Zamyadi et al. tion of short-term mobile surveys with stationary buoy measurements together with sensor technologies developing towards 2012) or can be used as input data to follow the spread of sub- increasing sensitivity, reliability, and autonomy, will likely open stances in a water body (Abell and Hamilton 2015). new horizons for HF measurements in lakes. A comprehensive description of the advantages and limitations of HFM in surface water monitoring is given by Rinke et al. (2013) Acknowledgements based on Rappbode Reservoir, where a set of online-sensors for This research was supported by the target-financed projects the measurement of physical, chemical, and biological variables SF0170011s08 and IUT 21-2, and by personal research grant PUT777 was complemented by a biweekly limnological sampling sched- of the Estonian Ministry of Education and Research, by the Esto- ule. The authors note that the HFM provide a deeper insight into nian Science Foundation grants ETF8729 and ETF9102, by the EU ecosystem dynamics and lake metabolism and are a powerful tool through European Regional Development Fund, program Envi- For personal use only. for assessing matter fluxes and establishing precise biochemical ronmental Conservation and Environmental Technology R&D budgets. Online measurements offer data for developing and val- Programme project VeeOBS (3.2.0802.11-0043) and MARS project idating state-of-the-art lake models and to improve their predic- (Managing Aquatic ecosystems and water Resources under multi- tive capabilities. As a fundamental limitation, the authors point ple Stress) funded under the 7th EU Framework Programme, out the lack of reliable online sensors for several important water Theme 6 (Environment including Climate Change), Contract No. quality variables (e.g., phosphorus compounds) making it neces- 603378 (http://www.mars-project.eu). sary to realise lab-based measurements of these variables by means of regular field samplings. Besides this, the regular field References sampling was used for checking the measurement quality and Abell, J.M., and Hamilton, D.P. 2015. Biogeochemical processes and phytoplankton nutrient limitation in the inflow transition zone of a large eutrophic lake accuracy of the online sensors and for the identification of their during a summer rain event. Ecohydrology, 8: 243–262. doi:10.1002/eco.1503. calibration intervals. Rinke et al. (2013) conclude that the imple- Alexander, R., and Imberger, J. 2013. Phytoplankton patchiness in Winam Gulf, mentation of in situ sensors, therefore, can never fully substitute Lake Victoria: a study using principal component analysis of in situ fluores- classical field sampling approaches as the latter will remain im- cent excitation spectra. Freshwater Biol. 58: 275–291. doi:10.1111/fwb.12057. Alfonso, M.B., Vitale, A.J., Menendez, M.C., Perillo, V.L., Piccolo, M.C., and portant at least for calibration and quality control of the sensor Perillo, C.M. 2015. Estimation of ecosystem metabolism from diel oxygen data. technique in a saline shallow lake: La Salada (Argentina). Hydrobiologia, 752: 223–237. doi:10.1007/s10750-014-2092-1. 8. Have HFM applications in limnology reached a Ansa-Ansare, O.D., Marr, I.L., and Cresser, M.S. 2000. Evaluation of modelled and measured patterns of dissolved oxygen in a freshwater lake as an indicator of plateau after the boom? the presence of biodegradable organic pollution. Water Resour. Res. 34: The publication record of HF studies in lakes (Fig. 2) shows that, 1079–1088. doi:10.1016/S0043-1354(99)00239-0. Anttila, S., Kairesalo, T., and Pellikka, P. 2008. A feasible method to assess inac- over the last 2 years, the number of papers has not reached 2011– curacy caused by patchiness in water quality monitoring. Environ. Monit.

Environ. Rev. Downloaded from www.nrcresearchpress.com by Nanjing Institute of Geography and Limnology, CAS on 01/17/17 2012 levels. Although automatic HFM potentially can replace dis- Assess. 142: 11–22. doi:10.1007/s10661-007-9904-y. PMID:17891528. crete manual measurements in many ﬁelds of lake research and Anttila, S., Ketola, M., Vakkilainen, K., and Kairesalo, T. 2012. Assessing temporal management, the leveling off of the publication records can be a representativeness of water quality monitoring data. J. Environ. Monit. 14: 589–595. doi:10.1039/C2EM10768F. PMID:22159426. sign of conceptual stagnation, as hardly any new HFM applica- Atkinson, S.F., and Mabe, J.A. 2006. Near real-time monitoring and mapping of tions have reached a level comparable to that of lake metabolism speciﬁc conductivity levels across lake Texoma, U.S.A. Environ. Monit. As- studies. Partly the slowdown in the publication activity could be sess. 120: 449–460. doi:10.1007/s10661-005-9072-x. PMID:16741798. caused by the economic recession that has delayed advances, al- Bass, A.L., Haugen, T.O., and Vøllestad, L.A. 2014. Distribution and movement of European grayling in a subarctic lake revealed by acoustic telemetry. Ecol. though, it may just be a sign of “natural” variability as the publi- Freshw. Fish, 23: 149–160. doi:10.1111/eff.12056. cation record was very low also in 2009. Batt, R.D., and Carpenter, S.R. 2012. Free-water lake metabolism: addressing

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