On the occurrence and ecological features of deep chlorophyll maxima (DCM) in Spanish stratified lakes

Deep chlorophyll maxima (DCM) are absolute maxima of Chlorophyll-a concentration among the vertical profile that can be found in deep layers of stratified lakes. In this manuscript I review the principal mechanisms that have been argued to explain the formation of DCM, which include, among others, in situ growth of metalimnetic phototrophs, differential impact of grazing between the different lake strata, and passive sedimentation to the layers where water density and cell density are equalized. The occurrence of DCM in Spanish lakes, as well as the main ecology characteristics of the oxygenic phototrophs that form DCM in these lakes is also reported. Cyanobacteria, either filamentous or unicellular, and cryptophytes, are the main components of most DCM found in the reported Spanish lakes, although diatoms, chrysophytes, dinoflagellates, and chlorophytes also contribute to these chlorophyll maxima. These organisms cope with strong physical and chemical gradients, among which those of water density, light and inorganic nutrient availability, and sulphide concentrations appear to be the most determinant factors influencing planktonic community structure.

[1]  C. Goldman,et al.  Evidence for algal heterotrophy in Lake Tahoe, California-Nevada1 , 1980 .

[2]  J. Nolla,et al.  Distributional patterns of phytoplankton in Spanish reservoirs: First results and comparison after fifteen years , 1991 .

[3]  Maria Rosa Miracle,et al.  Sinking processes and their effect on the sedimentary record in the meromictic Lake La Cruz (Spain) , 2000 .

[4]  C. Pérez-Martínez,et al.  Temporal occurrence of Ceratium hirundinella in Spanish reservoirs , 2001, Hydrobiologia.

[5]  Lucas J. Stal,et al.  Fermentation in cyanobacteria , 1997 .

[6]  E. Rott Some aspects of the seasonal distribution of flagellates in mountain lakes , 1988, Hydrobiologia.

[7]  C. Reynolds The long, the short and the stalled: on the attributes of phytoplankton selected by physical mixing in lakes and rivers , 1994, Hydrobiologia.

[8]  S. Heaney,et al.  The control of sub-surface maxima of diatoms in a stratified lake by physical, chemical and biological factors , 1989 .

[9]  Maria Rosa Miracle,et al.  The role of light and concentration gradients in the vertical stratification and seasonal development of phototrophic bacteria in a meromictic lake , 2000 .

[10]  Maria Rosa Miracle,et al.  The physical, chemical and biological characteristics of the holomictic sulphated Lake Arcas-2 (Cuenca, Spain) , 2004, Hydrobiologia.

[11]  C. Pérez-Martínez,et al.  Winter dominance of Ceratium hirundinella in a southern north-temperate reservoir , 2022 .

[12]  E. Spijkerman,et al.  Fatty Acid Patterns in Chlamydomonas sp. as a Marker for Nutritional Regimes and Temperature under Extremely Acidic Conditions , 2004, Microbial Ecology.

[13]  Roger I. Jones,et al.  Advantages of diurnal vertical migrations to phytoplankton in sharply stratified, humic forest lakes , 1991, Archiv für Hydrobiologie.

[14]  L. Arvola,et al.  Vertical distributions of bacteria and algae in a steeply stratified humic lake under high grazing pressure from Daphnia longispina , 1992, Hydrobiologia.

[15]  F. Echevarría,et al.  The size structure of plankton during a deep bloom in a stratified reservoir , 1994, Hydrobiologia.

[16]  J. Barko,et al.  Contrasting Diel Patterns of Vertical Migration in the Dinoflagellate Ceratium hirundinella in Relation to Phosphorus Supply in a North Temperate Reservoir , 1988 .

[17]  Y. Huot,et al.  Quantifying the response of phytoplankton photosynthesis to ultraviolet radiation: Biological weighting functions versus in situ measurements in two Swiss lakes , 2001, Aquatic Sciences.

[18]  Distribución vertical y variación estacional del fitoplancton de una laguna cárstica meromíctica, la Laguna de la Cruz (Cuenca, España) , 1991, Limnetica.

[19]  Maria Rosa Miracle,et al.  Nitrogen limitation of phytoplankton in a Spanish karst lake with a deep chlorophyll maximum: a nutrient enrichment bioassay approach , 2003 .

[20]  Maria Rosa Miracle,et al.  Ecology of a deep-living Oscillatoria (= Plankto-thrix) population in the sulphide-rich waters of a Spanish karstic lake. , 2000 .

[21]  C. Montes,et al.  Limnological characterization of an evaporite karstic lake in Spain (Lake Arreo) , 2000, Limnetica.

[22]  Maria Rosa Miracle,et al.  Distribution of photosynthetic organisms in a temporal stratified karstic pond near Cuenca, Spain: With 7 figures and 1 table in the text , 1984 .

[23]  F. Gervais Diel vertical migration of Cryptomonas and Chromatium in the deep chlorophyll maximum of a eutrophic lake , 1997 .

[24]  T. Embley,et al.  New species double the diversity of anaerobic ciliates in a Spanish lake , 1993 .

[25]  H. Marchant,et al.  Flagellate nutritional versatility as a key to survival in two contrasting Antarctic saline lakes , 2005 .

[26]  J. Riera,et al.  Major ionic composition in the Spanish reservoirs , 1991 .

[27]  P. López,et al.  El lago de Montcortés, descripción de un ciclo anual. , 1976 .

[28]  Maria Rosa Miracle,et al.  Rotifer vertical distribution in a strongly stratified lake: a multivariate analysis , 2004, Hydrobiologia.

[29]  B. Jørgensen,et al.  Microbial Transformations of Sulfur-Compounds in a Stratified Lake (Solar Lake, Sinai) , 1979 .

[30]  E. Padan,et al.  Sulfide inhibition of photosystem II in cyanobacteria (blue-green algae) and tobacco chloroplasts. , 1979, Biochimica et biophysica acta.

[31]  K. Morgan,et al.  The winter dark survival of an algal flagellate — Cryptomonas erosa (Skuja): With 5 figures and 1 table in the text , 1975 .

[32]  M. Auer,et al.  Heterotrophic Bacterioplankton Dynamics at a Site off the Southern Shore of Lake Superior , 2004 .

[33]  Maria Rosa Miracle,et al.  Vertical distribution of planktonic rotifers in a karstic meromictic lake , 1993, Hydrobiologia.

[34]  M. Dokulil,et al.  Equilibrium/steady-state concept in phytoplankton ecology , 2003, Hydrobiologia.

[35]  M. Alonso Las lagunas de la España peninsular , 1998, Limnetica.

[36]  L. Margulis,et al.  Green Endosymbiont of Coleps from Lake Ciso Spain Identified as Chlorella Vulgaris , 1988 .

[37]  Maria Rosa Miracle,et al.  Rotifer vertical distributions in a meromictic basin of Lake Banyoles (Spain) , 1993, Hydrobiologia.

[38]  C. Williamson,et al.  Utilization of subsurface food resources for zooplankton reproduction: Implications for diel vertical migration theory , 1996 .

[39]  H. Schubert,et al.  Light acclimation of Chlamydomonas acidophila accumulating in the hypolimnion of an acidic lake (pH 2.6) , 2005 .

[40]  L. Tranvik,et al.  Occurrence of bacterivory in Cryptomonas, a common freshwater phytoplankter , 1989, Oecologia.

[41]  Antonio Camacho,et al.  Summer phytoplankton assemblages across trophic gradients in hard-water reservoirs , 1998, Hydrobiologia.

[42]  F. Niell,et al.  Description and mechanism of formation of a deep chlorophyll maximum due to Ceratium hirundinella (O. F. Müller) Bergh , 1988, Archiv für Hydrobiologie.

[43]  A. Walsby,et al.  Gas vesicles , 1994, Microbiological reviews.

[44]  Luigi Naselli-Flores,et al.  Distribution and seasonal dynamics of Cryptomonads in Sicilian water bodies , 2003, Hydrobiologia.

[45]  Maria Rosa Miracle,et al.  Spatio-temporal distribution and growth dynamics of phototrophic sulfur bacteria populations in the sulfide-rich Lake Arcas , 2000, Aquatic Sciences.

[46]  R. Castenholz,et al.  Adaptation to sulfide and to the underwater light field in three cyanobacterial isolates from Lake Arcas (Spain) , 1996 .

[47]  C. Pedrós-Alió,et al.  Role of Anaerobic Ciliates in Planktonic Food Webs: Abundance, Feeding, and Impact on Bacteria in the Field , 1994, Applied and environmental microbiology.

[48]  M. Tuchman,et al.  Results from the U.S. EPA's Biological Open Water Surveillance Program of the Laurentian Great Lakes: II. Deep Chlorophyll Maxima , 2001 .

[49]  L. Bañeras,et al.  Dynamics of Phototrophic Microbial Populations in the Chemocline of a Meromictic Basin of Lake Banyoles , 1993 .

[50]  Maria Rosa Miracle,et al.  Vertical distribution and rotifer concentrations in the chemocline of meromictic lakes , 1983, Hydrobiologia.

[51]  F. Bartumeus,et al.  Microbial plankton assemblages, composition and biomass, during two ice-free periods in a deep high mountain lake (Estany Redó, Pyrenees) , 1999 .

[52]  E. Fee The vertical and seasonal distribution of chlorophyll in lakes of the Experimental Lakes Area, northwestern Ontario: Implications for primary production estimates , 1976 .

[53]  W. Wurtsbaugh,et al.  The spatial and temporal dynamics of deep chlorophyll layers in high-mountain lakes: effects of nutrients, grazing and herbivore nutrient recycling as growth determinants , 2006 .

[54]  F. Gervais Fine-scale analysis of a deep chlorophyll maximum , 2000 .

[55]  Frederic Bartumeus,et al.  The main features of seasonal variability in the external forcing and dynamics of a deep mountain lake (Redó, Pyrenees) , 2000 .

[56]  E. Stoermer,et al.  Paleolimnologic evidence of rapid recent change in Lake Erie's trophic status , 1996 .

[57]  R. Sommaruga The role of solar UV radiation in the ecology of alpine lakes. , 2001, Journal of photochemistry and photobiology. B, Biology.

[58]  G. Fahnenstiel,et al.  Subsurface chlorophyll maximum and associated Cyclotella pulse in Lake Superior , 1983 .

[59]  E. Vicente,et al.  Vertical distribution of photosynthetic sulphur bacteria linked to saline gradients in Lake \'El Tobar\' (Cuenca, Spain) , 1999 .

[60]  Maria Rosa Miracle,et al.  Extreme meromixis determines strong differential planktonic vertical distributions , 1993 .

[61]  A. Konopka Physiological ecology of a metalimnetic Oscillatoria rubescens population1 , 1982 .

[62]  F. Pick Photosynthesis and respiration of a metalimnetic chrysophyte population: With 4 figures in the text , 1984 .

[63]  Maria Rosa Miracle,et al.  Diel vertical movements of zooplankton in lake La Cruz (Cuenca, Spain) , 2000 .

[64]  W. Kettle,et al.  Vertical Distribution of Zooplankton in an Experimentally Acidified Lake Containing a Metalimnetic Phytoplankton Peak , 1987 .

[65]  Equilibrium/steady-state concept in phytoplankton ecology , 2003 .

[66]  G. Laliberté,et al.  AUTO‐, HETERO‐, AND MIXOTROPHIC GROWTH OF CHLAMYDOMONAS HUMICOLA (CMLOROIMIYCKAK) ON ACETATE 1 , 1993 .

[67]  John J. Cullen,et al.  The deep chlorophyll maximum comparing vertical profiles of chlorophyll a , 1982 .

[68]  S. Heaney,et al.  Population dynamics of Ceratium spp. in three English lakes, 1945–1985 , 1988, Hydrobiologia.

[69]  J. Erez,et al.  Microbial microstratification, inorganic carbon photoassimilation and dark carbon fixation at the chemocline of the meromictic Lake Cadagno (Switzerland) and its relevance to the food web , 2001, Aquatic Sciences.

[70]  Maria Rosa Miracle,et al.  Summer phytoplankton assemblages across trophic gradients in hard-water reservoirs , 1998, Hydrobiologia.

[71]  C. Pedrós-Alió,et al.  Physiological ecology of a metalimnetic Cryptomonas population: relationships to light, sulfide and nutrients , 1993 .

[72]  J. Komárek,et al.  Modern approach to the classification system of Cyanophytes 4 - Nostocales , 1989 .

[73]  C. Hoyos,et al.  Relationships between diatoms and the environment in Spanish reservoirs , 2005, Limnetica.

[74]  Maria Rosa Miracle,et al.  Size distribution of Daphnia longispina in the vertical profile , 1997, Hydrobiologia.

[75]  C. Callieri,et al.  Effect of UV‐B and different PAR intensities on the primary production of the mixotrophic planktonic ciliate Stentor araucanus , 2005 .

[76]  C. Pedrós-Alió,et al.  Predation by ciliates on a metalimnetic Cryptomonas population: feeding rates, impact and effects of vertical migration , 1995 .

[77]  W. Wurtsbaugh,et al.  Importance of zooplankton for the persistence of a deep chlorophyll layer: A limnocorral experiment , 2003 .

[78]  Jordi Catalan,et al.  The relationship between phytoplankton biovolume and chlorophyll in a deep oligotrophic lake: decoupling in their spatial and temporal maxima , 2000 .

[79]  L. Krienitz,et al.  Phytoplankton succession in the oligotrophic Lake Stechlin (Germany) in 1994 and 1995 , 1998 .

[80]  J. Stockner,et al.  Picoplankton and other non-bloom forming Cyanobacteria in lakes , 2000 .

[81]  Sara M. Morata Asociaciones fitoplanctónicas y su periodicidad en un lago marcadamente estratificado , 2003, Limnetica.

[82]  L. Rogers Photosynthetic pigments of algae , 1990 .

[83]  Kent W. Thornton,et al.  Reservoir Limnology: Ecological Perspectives , 1990 .

[84]  Colin S. Reynolds,et al.  Towards a functional classification of the freshwater phytoplankton , 2002 .

[85]  W. Lampert,et al.  Fitness optimization of Daphnia in a trade-off between food and temperature , 2004, Oecologia.

[86]  C. Pedrós-Alió,et al.  Diel changes in the microstratification of the metalimnetic community in Lake Cisó , 1991, Hydrobiologia.

[87]  P. Falkowski,et al.  PHOTOADAPTATION AND THE “PACKAGE” EFFECT IN DUNALIELLA TERTIOLECTA (CHLOROPHYCEAE) 1 , 1989 .

[88]  E. Vicente,et al.  Spatial Dominance and Inorganic Carbon Assimilation by Conspicuous Autotrophic Biofilms in a Physical and Chemical Gradient of a Cold Sulfurous Spring: The Role of Differential Ecological Strategies , 2005, Microbial Ecology.

[89]  C. Pedrós-Alió,et al.  Impact of Daphnia pulex on a metalimnetic microbial community , 1994 .

[90]  F. Gervais,et al.  Trophic Characterization, Pelagic Food Web Structure and Comparison of Two Mesotrophic Lakes in Brandenburg (Germany) , 2000 .

[91]  D. Bird,et al.  Phagotrophic sustenance of a metalimnetic phytoplankton peak , 1989 .

[92]  R. Margalef,et al.  PHYTOPLANKTON COMPOSITION AND DISTRIBUTION AS AN EXPRESSION OF PROPERTIES OF RESERVOIRS , 1982 .

[93]  F. Niell,et al.  Sinking velocities of principal phytoplankton species in a stratified reservoir: Ecological implications , 1993 .

[94]  S. Heaney,et al.  Migration behaviour of three cryptophytes in relation to environmental gradients: an experimental approach , 1991 .

[95]  D. Lean,et al.  The origin of a metalimnetic chrysophyte peak , 1984 .

[96]  C. Pérez-Martínez,et al.  Winter dominance of Ceratiumhirundinella in a southernnorth-temperate reservoir , 2002 .

[97]  A. Konopka Epilimnetic and Metalimnetic Primary Production in an Indiana Hardwater Lake , 1983 .

[98]  M. Álvarez-Cobelas,et al.  Are there steady-state phytoplankton assemblages in the field? , 2003, Hydrobiologia.

[99]  C. Callieri,et al.  Picoplankton in Lake Maggiore, Italy , 1995 .

[100]  F. Gervais Ecology of cryptophytes coexisting near a freshwater chemocline , 1998 .

[101]  D. Galat Reservoir Limnology: Ecological Perspectives , 1992 .

[102]  W. Wurtsbaugh,et al.  Growth and survival of Daphnia in epilimnetic and metalimnetic water from oligotrophic lakes: the effects of food and temperature , 2002 .

[103]  Maria Rosa Miracle,et al.  Sedimentation Patterns of Photosynthetic Bacteria Based on Pigment Markers in Meromictic Lake La Cruz (Spain): Paleolimnological Implications , 2006 .

[104]  L. Krienitz,et al.  Phytoplankton succession in the oligotrophic Lake Stechlin (Germany) in 1994 and 1995 , 2004, Hydrobiologia.

[105]  K. Denman,et al.  Mixing and the dynamics of the deep chlorophyll maximum in Lake Tahoe , 1984 .

[106]  K. Porter Phagotrophic phytoflagellates in microbial food webs , 1988, Hydrobiologia.

[107]  Colin S. Reynolds,et al.  Vegetation processes in the pelagic : a model for ecosystem theory , 1997 .

[108]  Maria Rosa Miracle,et al.  Spatial distribution and temporal dynamics of picocyanobacteria in a meromictic karstic lake , 2003 .

[109]  Maria Rosa Miracle,et al.  Which factors determine the abundance and distribution of picocyanobacteria in inland waters? A comparison among different types of lakes and ponds , 2003 .

[110]  M. Vanni Nutrient Cycling by Animals in Freshwater Ecosystems , 2002 .

[111]  S. Carpenter,et al.  Predicting chlorophyll vertical distribution in response to epilimnetic nutrient enrichment in small stratified lakes , 1995 .

[112]  A. Almodóvar,et al.  Effects of a bloom of Planktothrix rubescens on the fish community of a Spanish reservoir , 2004, Limnetica.

[113]  Maria Rosa Miracle,et al.  Ecology of Cryptomonas at the chemocline of a karstic sulfate-rich lake , 2001 .

[114]  E. Rico,et al.  Batimetría y análisis morfométrico del lago de arreo (N. España) , 1995, Limnetica.

[115]  C. Callieri,et al.  Photosynthetic efficiency and seasonality of autotrophic picoplankton in Lago Maggiore after its recovery , 2002 .

[116]  T. Fenchel,et al.  The biology of free-living anaerobic ciliates. , 1991, European journal of protistology.

[117]  F. Gervais,et al.  Phytoplankton species composition in the chemocline of mesotrophic lakes , 2000 .

[118]  F. Bartumeus,et al.  The relative importance of the planktonic food web in the carbon cycle of an oligotrophic mountain lake in a poorly vegetated catchment (Redó, Pyrenees) , 1999 .

[119]  C. Pedrós-Alió,et al.  Components, structure and fluxes of the microbial food web in a small, stratified lake , 1996 .

[120]  Maria Rosa Miracle,et al.  Factors determining changes in the abundance and distribution of micro-, nano- and picoplanktonic phototrophs in Lake El Tobar (Central Spain) , 2002 .

[121]  J. Stockner,et al.  Contribution of Rhizosolenia eriensis and Cyclotella spp. to the Deep Chlorophyll Maximum of Sproat Lake, British Columbia, Canada , 1990 .

[122]  F. Gervais LIGHT‐DEPENDENT GROWTH, DARK SURVIVAL, AND GLUCOSE UPTAKE BY CRYPTOPHYTES ISOLATED FROM A FRESHWATER CHEMOCLINE , 1997 .

[123]  Roger I. Jones Phytoplankton migrations: patterns, processes and profits. , 1993 .

[124]  G. Nygaard Temporal and spatial development of individual species of plankton algae from European lakes , 1996, Hydrobiologia.

[125]  Are there steady-state phytoplankton assemblages in the field? , 2003 .

[126]  G. Ramón,et al.  Long term changes (after twelve years) in the composition of phytoplankton communities in the Gorg Blau Reservoir (Majorca, Spain) , 1993 .

[127]  G. Fahnenstiel,et al.  Biomass, Size Structure, and Composition of Phototrophic and Heterotrophic Nanoflagellate Communities in Lakes Huron and Michigan , 1989 .

[128]  W. Koste Anuraeopsis miraclei, a new planktonic rotifer species in karstic lakes of Spain , 1991, Hydrobiologia.

[129]  C. Pedrós-Alió,et al.  Spatial and temporal dynamics of a metalimnetic Cryptomonas peak , 1992 .

[130]  B. Modenutti,et al.  Symbiotic association of the ciliate Ophrydium naumanni with Chlorella causing a deep chlorophyll a maximum in an oligotrophic South Andes lake , 1999 .

[131]  M. Boersma,et al.  How do migrating daphnids cope with fish predation risk in the epilimnion under anoxic conditions in the hypolimnion , 2000 .

[132]  C. Callieri,et al.  Increase in photosynthetic efficiency as a strategy of planktonic organisms exploiting deep lake layers , 2004 .

[133]  Maria Rosa Miracle,et al.  Population dynamics of oxiclinal species in lake Arcas-2 (Spain) , 1995, Hydrobiologia.

[134]  R. Adrian,et al.  Trophic interactions between zooplankton and the microbial community in contrasting food webs: the epilimnion and deep chlorophyll maximum of a mesotrophic lake , 2001 .

[135]  R. Adrian,et al.  Bacterial and protozoan mass accumulation in the deep chlorophyll maximum of a mesotrophic lake , 2003 .

[136]  Maria Rosa Miracle,et al.  Microstratified vertical distribution and migration of phototrophic microorganisms during a diel cycle in Lake Arcas-2 (Spain) , 1999 .

[137]  A. Nicklisch,et al.  Small-scale vertical distribution of phytoplankton, nutrients and sulphide below the oxycline of a mesotrophic lake , 2003 .

[138]  F. Gervais,et al.  Do light quality and low nutrient concentration favour picocyanobacteria below the thermocline of the oligotrophic Lake Stechlin , 1997 .

[139]  A. Konopka Metalimnetic cyanobacteria in hard‐water lakes: Buoyancy regulation and physiological state , 1989 .

[140]  L. Stal Physiological ecology of cyanobacteria in microbial mats and other communities. , 1995, The New phytologist.

[141]  Katja Fennel,et al.  Subsurface maxima of phytoplankton and chlorophyll: Steady‐state solutions from a simple model , 2003 .

[142]  Roger I. Jones,et al.  Mixotrophy in planktonic protists: an overview , 2000 .

[143]  L. Arvola,et al.  Hypolimnetic phosphorus retrieval by diel vertical migrations of lake phytoplankton , 1984 .

[144]  Richard P. Barbiero,et al.  The Deep Chlorophyll Maximum in Lake Superior , 2004 .

[145]  K. J. Clarke,et al.  Anaerobic ciliates from a sulphide-rich solution lake in Spain. , 1991, European journal of protistology.

[146]  E. Stoermer,et al.  Response of a Lake Michigan coastal lake to anthropogenic catchment disturbance , 2005 .

[147]  C. Pedrós-Alió,et al.  On the ecology of a Cryptomonas phaseolus population forming a metalimnetic bloom in Lake Cisó, Spain: Annual distribution and loss factors , 1987 .

[148]  L. Vörös,et al.  Fluorometric Characterization of Two Picocyanobacteria Strains from Lakes of Different Underwater Light Quality , 1996 .

[149]  E. Vicente,et al.  Carbon photoassimilation by sharply stratified phototrophic communities at the chemocline of Lake Arcas (Spain) , 1998 .

[150]  C. E. King,et al.  Diel vertical migration by Daphnia longispina in a Spanish lake: Genetic sources of distributional variation , 1995 .