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Short-term responses of littoral phytoplankton in a large shallow subtropical lake

Abstract

The littoral zone is an essential compartment for lake biota because of its high productivity and diversity. Moreover, phytoplankton is expected to have non-equilibrium dynamics on it. The study’s aimed to explore phytoplankton in the littoral zone of a shallow lake over a short-term scale. Daily sampling was conducted for 25 consecutive summer days in 2016, at two marginal points of a continuously warm, polymictic, and oligo-mesotrophic subtropical lake (Lake Mangueira, Brazil). Cyanobacteria and Chlorophyta contributed 86% of total biomass. We observed high variability in phytoplankton structure, with species turnover over diel cycles. Redundancy analysis indicated spatial differentiation for phytoplankton structure in relation to abiotic conditions. Nutrient dynamics and humic substances were significant drivers for phytoplankton variability. Phytoplankton was positively correlated with SRP and negatively with humic substances. Our results showed a non- equilibrium state for the littoral phytoplankton of Lake Mangueira, given the high variability of abiotic conditions, even at short distances. Due to its high temporal and spatial variability, the littoralzone seems to contribute to the recruitment and maintenance of phytoplankton biodiversity in shallow lakes. Further studies should consider the functional attributes of species and the complex biological interactions of phytoplankton and macrophytes along the littoral zone.

Key words
mixed lake; non-equilibrium theory; phytoplankton diel variation; phytoplankton littoral zone

INTRODUCTION

The littoral zone of lakes is generally overlooked in limnological research, with most ecological studies in these ecosystems being in pelagic habitats (Cattaneo et al. 2011CATTANEO A, DE SÈVE M, MORABITO G, MOSELLO R & TARTARI G. 2011. Periphyton changes over 20 years of chemical recovery of Lake Orta, Italy: differential response to perturbation of littoral and pelagic communities. J Limnol 70(2): 177-185., Vadeboncoeur et al. 2011VADEBONCOEUR Y, MCINTYRE PB & VANDER ZANDEN MJ. 2011. Borders of Biodiversity: Life at the Edge of the World’s Large Lakes. BioScience 61(7): 526-537., Jurca et al. 2012JURCA T, DONOHUE L, LAKETIĆ D, RADULOVIĆ S & IRVINE K. 2012. Importance of the shoreline diversity features for littoral macroinvertebrate assemblages. Fundam Appl Limnol 180(2): 175-184.). This zone is a lake boundary, as an interface zone acts a buffer between the watershed and landscape of the lake ecosystem (Loeb et al. 1983LOEB SL, REUTER JE & GOLDMAN CR. 1983. Littoral zone production of oligotrophic lakes. In: WETZEL R (Ed). Periphyton of freshwater ecosystems. Dr. W. Junk Publishers, The Hague, p. 161-167.). The environmental dynamics of the littoral zone experience a high effect of both direct and indirect mechanisms (Carmignani & Roy 2017CARMIGNANI JR & ROY AH. 2017. Ecological impacts of winter water level drawdowns on lake littoral zones: a review. Aquat Sci 79: 803-824.), such as climatic factors (Vadeboncoeur et al. 2014VADEBONCOEUR Y, DEVLIN SP, MCINTYRE PB & VANDER ZANDEN MJ. 2014. Is there light after depth? Distribution of periphyton chlorophyll and productivity in lake littoral zones. Freshw Sci 33(2): 524-536.), water level fluctuations (Hofmann et al. 2008HOFMANN H, LORKE A & PEETERS F. 2008. Temporal scales of water-level fluctuations in lakes and their ecological implications. Hydrobiologia 613: 85-96., Cantonati et al. 2014CANTONATI M, GUELLA G, KOMAREK J & SPITALE D. 2014. Depth distribution of epilithic cyanobacteria and pigments in a mountain lake characterized by marked water-level fluctuations. Freshw Sci 33(2): 537-547., Evtimova & Donohue 2016EVTIMOVA VV & DONOHUE I. 2016. Water-level fluctuations regulate the structure and functioning of natural lakes. Fresh Biol 61: 251-264.), the input of allochthonous nutrients (Janssen et al. 2014JANSSEN ABG, TEURLINCX S, AN S, JANSE JH, PAERL HW & MOOIJ WM. 2014. Alternative stable states in large shallow lakes? J Great Lakes Res 40: 813-826., Mäemets et al. 2018MÄEMETS H, LAUGASTE R, PALMIK K & HALDNA M. 2018. Response of primary producers to water level fluctuations of Lake Peipsi. Proc Estonian Acad Sci Biol Ecol 67(3): 231-245.) and interactions with the adjacent landscape (Schindler & Scheuerell 2002SCHINDLER DE & SCHEUERELL MD. 2002. Habitat coupling in lake ecosystems. Oikos 98: 177-189.). These peculiarities make the littoral zone a habitat with variable conditions and resources, which recruits specialized organisms that can live in such circumstances (Faria et al. 2015FARIA DM, CARDOSO LS & MOTTA-MARQUES D. 2015. Periphytic diatoms show a longitudinal gradient in a large subtropical shallow lake. Inland Waters 5: 117-124., Timoshkin 2018TIMOSHKIN OA. 2018. Coastal zone of the world’s great lakes as a target field for interdisciplinary research and ecosystem monitoring: Lake Baikal (East Siberia). Limnol Freshw Biol 1: 81-97.). Most of the species in lakes are restricted to this zone or completely depend on it for part of the life cycle, while the proportion of littoral habitats usually represents a small fraction of the total lake area (Strayer & Findlay 2010STRAYER DL & FINDLAY SEG. 2010. Ecology of freshwater shore zones. Aquat Sci 72: 127-163., Vadeboncoeur et al. 2011VADEBONCOEUR Y, MCINTYRE PB & VANDER ZANDEN MJ. 2011. Borders of Biodiversity: Life at the Edge of the World’s Large Lakes. BioScience 61(7): 526-537.). In addition, several studies point out that littoral bioindicators may serve as a primary sign of degradation of the littoral zone that cannot be efficiently detected within the pelagic portion (Rosenberger et al. 2008ROSENBERGER EE, HAMPTON SE, FRADKIN SC & KENNEDY B. 2008. Effects of shoreline development on the nearshore environment in large deep oligotrophic lakes. Fresh Biol 53: 1673-1691., Crossetti et al. 2013CROSSETTI LO, STENGER-KOVÁCS C & PADISÁK J. 2013. Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton. Hydrobiologia 716: 87-101., Cantonati & Lowe 2014CANTONATI M & LOWE RL. 2014. Lake benthic algae: toward an understanding of their ecology. Freshw Sci 33(2): 475-486., Rimet et al. 2016RIMET F, BOUCHEZ A & MONTUELLE B. 2016. Benthic diatoms and phytoplankton to assess nutrients in a large lake: complementary of their use in Lake Geneva (France-Switzerland). Ecol Indic 53: 231-239.). Thus, there is an increasing demand for monitoring the biological communities of the littoral zones of lakes.

The littoral zones of lakes are considered ecotones (Schiemer et al. 1995SCHIEMER F, ZALEWSKI M & THORPE JE. 1995. Land/Inland water ecotones: Intermediate habitats critical for conservation and management. Hydrobiologia 303: 259-264.) and are recognized as being important for the biota of shallow lakes (Wetzel 2001WETZEL RG. 2001. Limnology. Lake and River Ecosystems, Elsevier Academic Press, San Diego, 1006 p., Vadeboncoeur et al. 2011VADEBONCOEUR Y, MCINTYRE PB & VANDER ZANDEN MJ. 2011. Borders of Biodiversity: Life at the Edge of the World’s Large Lakes. BioScience 61(7): 526-537., Jurca et al. 2012JURCA T, DONOHUE L, LAKETIĆ D, RADULOVIĆ S & IRVINE K. 2012. Importance of the shoreline diversity features for littoral macroinvertebrate assemblages. Fundam Appl Limnol 180(2): 175-184.), providing feeding and breeding habitat for several communities (Rosenberger et al. 2008ROSENBERGER EE, HAMPTON SE, FRADKIN SC & KENNEDY B. 2008. Effects of shoreline development on the nearshore environment in large deep oligotrophic lakes. Fresh Biol 53: 1673-1691., Hampton et al. 2011HAMPTON SE, FRADKIN SC, LEAVITT PR & ROSENBERGER EE. 2011. Disproportionate importance of nearshore habitat for the food web of a deep oligotrophic lake. Mar Freshw Res 62: 350-358., Kosten & Meerhoff 2014KOSTEN S & MEERHOFF M. 2014. Lake Communities. Encyclopedia of Life Sciences (ELS) 15: 1-11.). Many organisms leave the pelagic region for resources or refuge, such as horizontal zooplankton migrations (Burks et al. 2002BURKS RL, LODGE DM, JEPPESEN E & LAURIDSEN TL. 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting littoral zones. Fresh Biol 47: 343-365., Meerhoff et al. 2007aMEERHOFF M, CLEMENTE JM, TEIXEIRA DE MELLO F, IGLESIAS C, PEDERSEN AR & JEPPESEN E. 2007a. Can warm climate-related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob Chang Biol 13: 1888-1897.) or fish seeking food (Carmignani & Roy 2017CARMIGNANI JR & ROY AH. 2017. Ecological impacts of winter water level drawdowns on lake littoral zones: a review. Aquat Sci 79: 803-824.). In addition, intense biological interactions are commonly observed in the littoral zone, such as periphyton-macrophyte connection (Faria et al. 2015FARIA DM, CARDOSO LS & MOTTA-MARQUES D. 2015. Periphytic diatoms show a longitudinal gradient in a large subtropical shallow lake. Inland Waters 5: 117-124.), zooplankton-macrophyte relationships (Šorf et al. 2015ŠORF M, DAVIDSON TA, BRUCET S, MENEZES RF, SØNDERGAARD M, LAURIDSEN TL, LANDKILDEHUS F, LIBORIUSSEN L & JEPPESEN E. 2015. Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels. Hydrobiologia 742: 185-203., Gebrehiwot et al. 2017GEBREHIWOT M, KIFLE D & TRIEST L. 2017. Emergent macrophytes support zooplankton in a shallow tropical lake: a basis for wetland conservation. Environ Manage 60: 1127-1138.), and negative interactions between macrophytes and phytoplankton (Švanys et al. 2014ŠVANYS A, PAŠKAUSKAS R & HILT S. 2014. Effects of the allelopathically active macrophytes myriophyllum spicatum Linn. on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737: 57-66., Hilt 2015HILT S. 2015. Regime shifts between macrophytes and phytoplankton – concepts beyond shallow lakes, unravelling stabilizing mechanisms and practical consequences. Limnetica 34(2): 467-480.). Commonly, lake littoral zone is extensively colonized by emergent and submersed macrophytes, which can perform important biogeochemical functions (Strayer & Findlay 2010STRAYER DL & FINDLAY SEG. 2010. Ecology of freshwater shore zones. Aquat Sci 72: 127-163.) and contribute with large amounts of organic carbon and yellow substances to the system (They et al. 2013THEY NH, MOTTA-MARQUES D, SOUZA RS & RODRIGUES LR. 2013. Short-Term Photochemical and Biological Unreactivity of Macrophyte-Derived Dissolved Organic Matter in a Subtropical Shallow Lake. J Ecosyst 316709: 1-9.), altering underwater light incidence (Barrow et al. 2019BARROW JL, BEISNER BE, GILES R, GIANI A, DOMAIZON I & GREGORY EAVES I. 2019. Macrophytes moderate the taxonomic & functional composition of phytoplankton assemblages during a nutrient loading experiment. Freshw Biol 64: 1369-1381.). Moreover, the competition for nutrients (Van Donk & Van de Bund 2002VAN DONK E & VAN DE BUND WJ. 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72(3-4): 261-274., Vanderstukken et al. 2014VANDERSTUKKEN M, DECLERCK SAJ, DECAESTECKER E & MUYLAERT K. 2014. Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii Planch. Fresh Biol 59: 930-941.) and the release of allelopathic substances by macrophytes (Gross et al. 2007GROSS EM, HILT S, LOMBARDO P & MULDERIJ G. 2007. Searching for allelopathic effects of submerged macrophytes on phytoplankton-state of the art and open questions. Hydrobiologia 584: 77-88., Mulderij et al. 2007MULDERIJ G, VAN NES EH & DONK EV. 2007. Macrophyte-phytoplankton interactions: the relative importance of allelopathy versus other factors. Ecol Modell 204: 85-92.), can cause significant reductions in phytoplankton biomass (Mulderij et al. 2005MULDERIJ G, MOOIJ WM & VAN DONK E. 2005. Allelopathic growth inhibition and colony formation of the green alga Scenedesmus obliquus by the aquatic macrophytes Stratiotes aloides. Aquatic Ecol 39: 11-21.) and specific functional forms (Finkler Ferreira et al. 2018FINKLER FERREIRA T, CROSSETTI LO, MOTTA-MARQUES D, CARDOSO LS, FRAGOSO CR JR & VAN NES EH. 2018. The structuring role of submerged macrophytes in a large subtropical shallow lake: clear effects on water chemistry and phytoplankton structure community along a vegetated pelagic gradient. Limnologica 69: 142-154.). These complex interactions can drive the biological dynamics of littoral communities (Cardoso et al. 2018CARDOSO LS, FARIA DM, CROSSETTI LO & MOTTA-MARQUES D. 2018. Phytoplankton, periphyton, and zooplankton patterns in the pelagic and littoral regions of a large subtropical shallow lake. Hydrobiologia 831: 119-132.).

The phytoplankton community is an essential primary producer in shallow lakes (Wetzel 2001WETZEL RG. 2001. Limnology. Lake and River Ecosystems, Elsevier Academic Press, San Diego, 1006 p.). Phytoplankton can closely track both short- and long-term environmental variation in lakes (Salmaso 2002SALMASO N. 2002. Ecological patterns of phytoplankton assemblages in Lake Garda: seasonal, spatial and historical features. J Limnol 61: 95-115.) and, with their short generations, they are sensitive indicators of environmental change in those ecosystems (Reynolds et al. 2002REYNOLDS CS, HUSZAR VLM, KRUK C, NASELLI FLORES L & MELO S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24(5): 417-428., Crossetti et al. 2013CROSSETTI LO, STENGER-KOVÁCS C & PADISÁK J. 2013. Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton. Hydrobiologia 716: 87-101., Weithoff & Gaedke 2017WEITHOFF G & GAEDKE U. 2017. Mean functional traits of lake phytoplankton reflect seasonal and inter-annual changes in nutrients, climate and herbivory. J Plankton Res 39(3): 509-517.). Given this fast response time, studies over short-time intervals provide a more accurate assessment of species recruitment due to resources variability (Nixdorf et al. 2003NIXDORF B, MISCHKE U & RÜCKER J. 2003. Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes – an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiologia 502: 111-121.). This approach is critical for recognizing phytoplankton’s stable states, which are, in some species, optimize resource consumption when they are constantly available (Sommer et al. 1993SOMMER U, PADISÁK J, REYNOLDS CS & JUHÁSZ-NAGY P. 1993. Hutchinson’s heritage: the diversity-disturbance relationship in phytoplankton. Hydrobiologia 249: 1-8.). Thus, due to the susceptibility to changes in the abiotic conditions of littoral zones of shallow lakes, non-equilibrium phytoplankton dynamics can be expected, assuming the recurrent disturbances affect this zone (i.e., high variability of nutrients and light), even though there is evidence that permanent circulation can be a low disturbance status (Reynolds et al. 1993REYNOLDS CS, PADISÁK J & SOMMER U. 1993. Intermediate disturbance in the ecology of phytoplankton and the maintenance of species diversity: a synthesis. Hydrobiologia 249: 183-188.), which enables steady states.

Studies on phytoplankton from the littoral zone of lentic ecosystems have been carried out using different approaches. For instance, comparative studies between the pelagic and littoral zones have explored the influence of the temperature and water level regimes on phytoplankton (Sakharova & Korneva 2018SAKHAROVA EG & KORNEVA LG. 2018. Phytoplankton in the littoral and pelagial zones of the Rybinsk Reservoir in years with different temperature and water-level regimes. Inland Water Biol 11: 6-12.), the variability of phytoplankton metabolism in both zones (Dunalska et al. 2013DUNALSKA JA, ZIELIŃSKI RA, BIGAJ I & SZYMAŃSKI D. 2013. Indicators of changes in the phytoplankton metabolism in the littoral and pelagial zones of a eutrophic lake. Rocz Ochr Sr 15(1): 621-636.) and the community structure and dynamics regarding the seasonality (Szelag-Wasielewska 1993SZELAG-WASIELEWSKA E. 1993. Phytoplankton in the littoral and pelagial of the Lake Miedwie. Verh Int Ver Theor Angew Limnol 25(1): 662-665.) or the system trophic state (Lemly & Dimmick 1982LEMLY AD & DIMMICK JF. 1982. Phytoplankton communities in the littoral zone of lakes: observations on structure and dynamics in oligotrophic and eutrophic systems. Oecologia 54: 359-369.). Beyond that, studies focusing on distribution transects between littoral and pelagic zones, exploring the interchange of phytoplankton community between both zones (Schweizer 1997SCHWEIZER A. 1997. From littoral to pelagial: comparing the distribution of phytoplankton and ciliated protozoa along a transect. J Plankton Res 19(7): 829-848.) and phytoplankton littoral monitoring for comparison purposes with long-term data (Bondarenko & Logacheva 2017BONDARENKO NA & LOGACHEVA NF. 2017. Structural Changes in Phytoplankton of the Littoral Zone of Lake Baikal. Hydrobiol J 53: 16-24.) and for ecological state assessment (Crossetti et al. 2013CROSSETTI LO, STENGER-KOVÁCS C & PADISÁK J. 2013. Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton. Hydrobiologia 716: 87-101.) have also been performed.

Whereas the littoral zone of lakes represents an important transitional area, integrating terrestrial and aquatic conditions, besides being heavily used by humans, and since phytoplankton dynamics should accurately reflect the high environmental variability of this zone, the study aim to assess phytoplankton structure and dynamics over a short term in a highly hydrodynamic system. Then, the following questions were addressed: (i) How do the indicators of phytoplankton structure (biomass, species richness and diversity) and dynamics (descriptor species) vary over a short time scale in the studied zone?, and (ii) What are the environmental drivers of the observed variability? It is expected to observe the non-equilibrium dynamics of phytoplankton and succession rate variability in the littoral zone, due to the fast-changing environmental conditions and resource availability to be seen in this compartment. This work seeks to contribute to a better understanding of the still little-studied littoral phytoplankton communities.

MATERIALS AND METHODS

Study site

Lake Mangueira is a large, shallow lake situated in a protected area (Taim Hydrological System - THS) on a narrow strip of land between the Atlantic Ocean and Mirim Lake (Fig. 1), on the southern coastal plain of the state of Rio Grande do Sul, South Brazil (33º31’22’’S; 53º07’48’’W). The region has a subtropical climate Cfa (Kottek et al. 2006KOTTEK M, GRIESER J, BECK C, RUDOLF B & RUBEL F. 2006. World Map of the Köppen-Geiger climate classification updated. Meteorol Z 15: 259-263.). The lake has mean depth of 2.6 m, a maximum depth of 6 m, and is 90 km long and 3–10 km wide with a total surface area of 820 km2. The main axis of the lake is oriented from north-east to south-west and corresponds to the direction of the prevailing winds (Fragoso et al. 2008FRAGOSO CR JR, MOTTA-MARQUES D, COLLISCHONN W, TUCCI C & VAN NES EH. 2008. Modelling spatial heterogeneity of phytoplankton in Lake Mangueira, a large shallow subtropical lake in South Brazil. Ecol Modell 219: 125-137.). Thus, the hydrodynamics of the lake is determined manly by strong and constant winds that frequently resuspend sediment in the water column (Cardoso et al. 2012CARDOSO LS, FRAGOSO CR JR, SOUZA RS & MOTTA-MARQUES D. 2012. Hydrodynamic control of plankton spatial and temporal heterogeneity in subtropical shallow lakes. Chapter 2. In: SCHULZ H (Ed). Hydrodynamics - Natural Water Bodies, p. 27-48.), directly affecting the plankton communities. The mixing regime of the lake is continuously warm and polymictic with daily mixing by strong winds, according to Lewis’ (1983) system.

Figure 1
Map of Lake Mangueira showing its location within Brazil and the location of the sampling stations.

Lake Mangueira’s trophic state varies from oligotrophic to mesotrophic. Mesotrophic conditions occur in spring and summer, when enormous volumes of water are drawn from it to irrigate rice fields (2 L.ha-1 s-1 for 100 days), decreasing the volume of water at the same time that high nutrient concentrations enter the lake from the watershed (Fragoso et al. 2008). This nutrient input drained from rice fields to the lake temporarily favors the increase in plankton production in the system. After this cultivation period, nutrient concentrations remain low, characterizing the lake as oligotrophic. Submerged, free-floating and emergent macrophytes cover large areas of the southern portion of the lake (Rodrigues et al. 2015RODRIGUES LR, MOTTA-MARQUES D & FONTOURA NF. 2015. Fish community in a large coastal subtropical lake: how an environmental gradient may affect the structure of trophic guilds. Limnetica 34: 495-506.). The predominant macrophyte species in this portion of the lake are Egeria densa Planchon, Myriophyllum spicatum Linnaeus, Nitella sp. C.Agardh, Potamogetonillinoensis Morong, Potamogeton pectinatus (Linnaeus) Börner, Schoenoplectus californicus (C.A.Meyer) Palla, Utricularia sp. Linnaeus, Zizaniopsis bonariensis (Balansa and Poitrasson) Spegazzini, Cabomba caroliniana A. Gray, Myriophyllum spicatumicatum Linnaeus, and Ceratophyllum demersum Linnaeus (Finkler Ferreira et al. 2018FINKLER FERREIRA T, CROSSETTI LO, MOTTA-MARQUES D, CARDOSO LS, FRAGOSO CR JR & VAN NES EH. 2018. The structuring role of submerged macrophytes in a large subtropical shallow lake: clear effects on water chemistry and phytoplankton structure community along a vegetated pelagic gradient. Limnologica 69: 142-154.).

Sampling

Water subsurface samples were collected in the morning of 25 consecutive summer days (January 2016) at two sampling sites located in the littoral zone of the southern portion of Lake Mangueira: Station 1 (S1) (33°30’03.6”S 53°08’33.7”W) and Station 2 (S2) (33°30’15.8”S 53°08’41.6”W). The stations presents a mean depth of 1,3 m, are located 500 m from each other and 250 m from the shoreline (Fig. 1). Neither sampling station was situated within macrophyte beds, although macrophytes densely inhabited the area. Physical, chemical, and biological samples were collected from the subsurface with polypropylene bottles. Conductivity (Cond), pH, dissolved oxygen (DO), and water temperature (Temp) were measured in situ with a portable multiparameter probe (YSI 6920). Water transparency was estimated with a Secchi disk (SD). Soluble reactive phosphorus (SRP), total nitrogen (TN), and total dissolved nitrogen (TDN) were analyzed using colorimetric methods according to Rice et al. (2012)RICE EW, BAIRD RB, EATON AD & CLESCERI LS. 2012. Standard Methods for Examination of Water and Wastewater. 22nd ed. American Public Health Association, American Water Works, Water Environment Federation, Washington DC, USA, 1360 p.. Total phosphorus (TP) analysis followed by Mackereth et al. (1989)MACKERETH FJH, HERON J & TALLING JF. 1989. Water analysis: some revised methods for limnologists. Freshwater Biological Association, 120 p.. Dissolved organic carbon (DOC) and dissolved inorganic carbon (DIC) were analyzed using specific equipment (Shimadzu VCPH). Soluble reactive silicon (SRSi) analysis followed by Rice et al. (2012)RICE EW, BAIRD RB, EATON AD & CLESCERI LS. 2012. Standard Methods for Examination of Water and Wastewater. 22nd ed. American Public Health Association, American Water Works, Water Environment Federation, Washington DC, USA, 1360 p.. Humic acid absorbance coefficient at 365 nm (Abs365) was measured using a Varian Cary 1 – Spectrophotometer (Strome & Miller 1978STROME DJ & MILLER MC. 1978. Photolytic changes in dissolved humic substances. Verh Internat Verein Limnol 20: 1248-1254.). Meteorological data (wind velocity and direction, precipitation) were collected from the conventional and automatic stations of Santa Vitória do Palmar and Chuí (INMETRO), about 23 km from the study area. Radiation values were derived from CERES data sets and downloaded through the web interface at https://ceres.larc.nasa.gov/index.php. CERES products consist of hourly radiation data (UTC time), based on Moderate Resolution Imaging Spectroradiometer (MODIS) (Data Quality Summary 2017). For this study, the average values of the morning period of each sampling day was considered for radiation (Rad) and wind velocity (WV) estimation, as well as the predominant wind direction (WD), was considered.

Data analysis

Samples of the phytoplankton community were fixed with 1% acetic Lugol immediately after collection for later quantitative analysis under an inverted microscope, following the method of Utermöhl (1958)UTERMÖHL H. 1958. Zur Vervollkommnung der quantitativen Phytoplankton: Methodik. Mitteilungen der Internationale Vereinigung für theoretische und angewandte Verh Int Ver Theor Angew Limnol 9: 1-38., and determination of settling time according to Lund et al. (1958)LUND JWG, KIPLING C & LECREN ED. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143-170.. At least 400 170 individuals were enumerated per sample (95% of confidence limit, Lund et al. 1958LUND JWG, KIPLING C & LECREN ED. 1958. The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11: 143-170.). Density was expressed in individuals/mL. The biovolume of each species was determined according to Hillebrand et al. (1999)HILLEBRAND H, DÜRSEKEN D, KIRSCHIEL D, POLLINGHER U & ZOHARY T. 1999. Biovolume calculation for pelagic and benthic microalgae. J Phycol 35: 403-424. based on geometric shapes, and converted in biomass following Wetzel & Likens (2000)WETZEL RG & LIKENS GE. 2000. Limnological Analysis. Springer, Berlin, 429 p., where mm³/L = mg/L. Biomass (mg/L) was considered the estimate of phytoplankton abundance. Descriptor species were considered as those that contributed a minimum of 1% to total biomass on at least one sampling occasion. The succession rate of phytoplankton was calculated using the sum of differences method (Lewis 1978):

σ = i | [ b i ( t 1 ) B ( t 1 ) ] [ b i ( t 2 ) B ( t 2 ) ] | ( t 2 t 1 )

where bi (t) is the abundance of the nth species; B(t) is the sum of individuals constituting the community sampled; t1 and t2 are the two successive days. Species richness was expressed in terms of the total number of taxa per sample. Ecological diversity was calculated using the Shannon index (Shannon 1948SHANNON CE. 1948. A mathematical theory of communication. Bell Syst Tech J 27(3): 379-423.), from phytoplankton biomass (mg/L), using PAST software 182 version 2.13 (Hammer et al. 2001HAMMER O, HARPER DAT & RAYAN PD. 2001. PAST. Palentological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4(1): 9.).

Environmental variability of the littoral zone was assessed by multivariate descriptive analysis using Principal Component Analysis (PCA) of covariance matrices. Spatial differences between sampling sites in biological and limnological data were tested using a non-parametric Wilcoxon test and p-values were adjusted using post-hoc Bonferroni correction. A Redundancy Analysis (RDA) (ter Braak & Smilauer 1998TER BRAAK CJF & SMILAUER P. 1998. CANOCO: Reference Manual and User’s Guide to CANOCO for Windows (Version 4). Centre for Biometry, Wageningen, 351 p.) was performed to determine the influence of abiotic variables on the phytoplankton assemblage, with the significance being tested by the Monte Carlo permutation test (999 permutations), after testing the data with Detrended Correspondence Analysis (DCA) (Hill & Gauch 1980HILL MO & GAUCH HG. 1980. Detrended Correspondence Analysis: An Improved Ordination Technique. Vegetatio 42: 47-58.), to select the most appropriate method to be applied. The environmental variables for the RDA were selected based on a PCA using a Pearson and Kendall correlation matrix. The environmental dataset was transformed to a 0–1 scale by ranging (Sneath & Sokal 1973SNEATH PHA & SOKAL RR. 1973. Numerical Taxonomy: The Principles and Practice of Numerical Classification. Freeman, San Francisco, 573 p.): first extracting the minimum observed for each variable and then dividing by the range (Legendre & Legendre 1998LEGENDRE P & LEGENDRE L. 1998. Numerical ecology. Elsevier, Amsterdam, 852 p.). The biological data (phytoplankton biomass) were transformed by log x + 1.

Correlation analyses (r - Pearson; p < 0.05) were also performed between phytoplankton total biomass, succession rate, diversity index, species richness, and environmental data to identify any relationships. All multivariate analyses were done using PC-ORD version 6.08 software (McCune & Mefford 2011MCCUNE B & MEFFORD MJ. 2011. PC-ORD. Multivariate analysis of ecological data – Version 6.08. MJM Software Design, Gleneden Beach.), while Wilcoxon’s test was performed using Statistica 7.1 software (StatSoft, Inc. 2005), and correlation analysis using PAST software version 2.13 (Hammer et al. 2001HAMMER O, HARPER DAT & RAYAN PD. 2001. PAST. Palentological Statistics Software Package for Education and Data Analysis. Palaeontol Electron 4(1): 9.).

RESULTS

Environmental conditions

No rainfall was recorded during the study period and the wind velocity remained between 3 and 7 m/s and the predominant direction swung between Northeast and South-Southwest (Fig. 2a). Radiation reached higher values above 200 W/m2 between days 5 and 19 (except for day 17) and had intermediate values at the beginning and end of the study (Fig. 2b). Wind direction did not present any significant correlation with any of the abiotic or biological variables.

Figure 2
Values of wind velocity and wind direction (a) and solar radiation (b) at Lake Mangueira, during the studied period. WV = Wind velocity (m/s), WD = Wind direction (°) and Rad = Radiation (W/m2). Wind direction categories tracked the degrees scale, as follows: North (338° to 22°); Northeast (23° to 67°); East (68° to 112°); Southeast (113° to 157°); South (158° to 202°); Southwest (203° to 247°); West (248° to 292°) and Northwest (293° to 337°).

The first three axes of the PCA explained 48% of the variability in the abiotic data (p < 0.05; Fig. 3). The positive side of the first axis (20%, p = 0.001; Fig. 3a) ordinated most sampling units of the beginning and middle of the time series (days 1 to 15) due to higher concentrations of SRSi (r = 0.55) and TN (r = 0.34). The negative side of this axis ordinated the final sampling units of the time series of both sampling stations due to higher values for TDN (r = -0.43), Cond (r = -0.40), DOC (r = -0.28), and TP (r = -0.26). The positive side of the second axis (17%, p = 0.001) grouped most S1 samples due to higher values for SRP (r = 0.62) and DO (r = 0.45). On the other hand, the negative side of this axis ordinated all the S2 sampling units due to higher values of Abs365 (r = -0.36), DOC (r = -0.28), DIC (r = -0.28), and TDN (r = 0.27). The positive side of the third axis (11%, p = 0.05; Fig. 3b) ordinated both S1 and S2 sampling units from different periods due to higher values of SRSi (r = 0.46), TDN (r = 0.43), DIC (r = 0.32), WV (r = 0.31), TN (r = 0.26), DOC (r = 0.24), and SRP (r = 0.21). The same tendency was observed on the negative side of this axis with sampling units from both stations being grouped especially due to the higher values of SD (r = -0.36) and Abs365 (r = -0.23). In general, the analysis evidenced a temporal distribution of environmental data, with most of the initial sampling units being separated from the later ones, followed by spatial segregation of S1 and S2. The variables DO, SRP, TN, DIC, and DOC differed significantly between sampling stations (Table I).

Figure 3
Principal Component Analysis (PCA) biplots of environmental variables of axes 1 and 2 (a) and axes 1 and 3 (b) in the littoral zone of Lake Mangueira during the studied period. Abs365 = humic acid 365 absorbances; Cond = conductivity; DIC = dissolved inorganic carbon; DO = dissolved oxygen; DOC = dissolved organic carbon; SD = Secchi depth; SRP = soluble reactive phosphorus; SRSi = soluble reactive silica; TP = total phosphorus; TN = total nitrogen; TDN = total dissolved nitrogen and WV = wind velocity.
Table I
Abiotic parameters, phytoplankton biomass, and ecological indices: minimum (min), maximum (max), mean, and standard deviation (sd), during the study at stations S1 and S2 (n = 25 per station). Bold values indicate significant differences (Wilcoxon, p < 0.05).

Phytoplankton

Phytoplankton total biomass (TB) did not differ significantly between the sampling stations (p > 0.05). Besides biomass peaks on days 15 and 22 (10.3 mg/L and 13.4 mg/L), S2 generally had lower TB than S1, which had its peak on day 14 (12.7 mg/L) (Fig. 4a). TB and Abs365 were negatively correlated at both sampling stations (r = -0.42 at S1 and r = -0.47 at S2, p < 0.05). At S1, TB was positively correlated with SRP (r = 0.60, p = 0.001) and TN (r = 0.46, p = 0.02), while at S2 TB was negatively correlated with TN (r = -0.46, p = 0.02), SRSi (r = -0.42, p = 0.04) and DIC (r = -0.41, p = 0.04). The succession rate (σ) of phytoplankton at both stations presented similar patterns of continuous variation throughout the studied period (Fig. 4b). Overall, the phytoplankton succession rate was higher at S2, being negatively correlated with SRSi (r = -0.39, p = 0.05) and Abs365 (r = -0.41, p = 0.04), and positively correlated with SRP at S1 (r = 0.67, p = 0.002).

Figure 4
Phytoplankton total biomass (a), succession rate (b), species richness (c), and Shannon diversity (d) in the littoral zone of Lake Mangueira during the studied period at stations S1 and S2.

A total of 97 phytoplankton species were found: 85 species at S1 (30 exclusive taxa) and 67 species at S2 (12 exclusive taxa). Phytoplankton species were sorted into eight major groups: Chlorophyceae (39.2% of the identified taxa), followed by Cyanobacteria (36.1%), and less than 10% for the other groups (Zygnemaphyceae, Bacillariophyceae, Euglenophyceae, Chrysophyceae, Dinophyceae, and Cryptophyceae). Chlorophyceae was the most abundant group (43.9% of TB), followed by Cyanobacteria (41.9%), and less than 10% for the other groups. The relative contribution of phytoplankton groups at each sampling site was very similar, being dominated most of the time by cyanobacteria (CYA) and chlorophytes (CHL). Lower biomass of those groups coincided with increased biomass of chrysophytes (CHR), which reached 32% of TB on day 23, when CYA and CHL had their lowest recorded relative abundances with 34% and 21%, respectively.

Species richness (S) did not differ significantly (p > 0.05) between the sampling stations (Fig. 4c) and varied from 14 to 29 (days 25 and 16, respectively) at S1, and from 11 to 28 (days 11 and 15, respectively) at S2. Phytoplankton richness was correlated with SRP (r = 0.61, p = 0.001), DOC (r = -0.45, p = 0.02) and DIC (r = -0.39, p = 0.05) at S1, while negatively correlated with Abs365 (r = -0.41, p = 0.02) at S2. Shannon diversity differed significantly between the sampling stations (p < 0.05), with higher values at S1 (Fig. 4d). Phytoplankton diversity was positively correlated with SRP (r = 0.39, p = 0.05) and negatively with DIC (r = -0.39, p = 0.05) at S1.

Thirty-two descriptive species were registered at the sampling stations throughout the time series, with 26 being shared between the stations (Table II). The descriptive species accounted for 85% of phytoplankton TB. The major contributors to TB were the cyanobacteria Aphanocapsa spp. and Planktolyngbya spp., as well as the chlorophytes Scenedesmus spp., Oocystis lacustris, Golenkinia radiata, Lagerheimia ciliata and Monoraphidium irregulare and the chrysophycean Dinobryon sertularia (Fig. 5).

Figure 5
Relative biomass contribution of the five most abundant phytoplankton species at sampling stations S1 (a) and S2 (b) in the littoral zone of Lake Mangueira during the studied period.
Table II
Descriptive species of the phytoplankton community in the littoral zone of Lake Mangueira during the studied period: values of relative contribution (%) of each taxon at sampling stations S1and S2. Bold values specify the descriptive species of each sampling station.

Integrated analysis of biological and abiotic data

The RDA resulted in high Pearson’s correlation between limnological and species data for the first two axes (0.784 and 0.782, respectively), indicating strong relationships among abiotic and phytoplankton variables of the sampling stations. The Monte Carlo test indicated that the orderings of the first two axes were significant (p=0.04), confirming that the analysis was not randomly generated. The biplot (Fig. 6) demonstrated a slight spatial differentiation of the phytoplankton community in relation to abiotic variables without clear temporal gradients. Most of S2 and some S1 sampling units were ordinated on the positive side of the first axis due to the higher values of Abs365 (r = 0.68), DOC (r = 0.47), TP (r = 0.35), TDN (r = 0.25) and DIC (r = 0.24), where the species Chroococcus minor and Aphanocapsa koordersii, also Peridiniopsis sp. and Oocystis borgeii were ordinated. The negative side of the first axis concentrated S1 and S2 sampling units with the higher values of SRP (r = -0.68), TN (r = -0.31) and WV (r = -0.16), with the species guild ordinated to that side being composed of several chlorophytes and desmids, and the cyanobacteria Aphanocapsa spp., Aphanothece spp. and Planktolyngbya spp. The positive side of the second axis sorted most of S2 due to higher WV values (r = 0.24), where Scenedesmus obtusus and Dinobryon sertularia were ordinated, as well some cyanobacteria species (Chroococcus spp., Merismopedia tenuissima, Radiocystis fernandoi and Eucapsis sp.). Greater values of SRSi (r = -0.62), SRP (r = -0.43) and DIC (r = -0.35) grouped most S1 sample units to the negative side of the second axis with the species guild composed of Dolichospermum circinale, Willea crucifera and Mucidosphaerium pulchellum, among others.

Figure 6
Redundancy analysis (RDA) biplot of environmental variables and descriptive species in the littoral zone of Lake Mangueira during the studied period at Stations 1 and 2. Abs365 = humic acid 365 absorbances; DIC = dissolved inorganic carbon; DOC = dissolved organic carbon; SRP = soluble reactive phosphorus; SRSi = soluble reactive silica; TP = total phosphorus; TN = total nitrogen and WV = wind velocity. For the species legend, see Table II.

DISCUSSION

Our results demonstrated high variability of littoral phytoplankton structure over short-time intervals during the evaluated summer period. No steady state of phytoplankton was recorded at either sampling station. Instead, we observed high variability of biomass and the relative contribution of species throughout the studied period related to constant environmental shifts, which lead to continuous species turnover, sometimes during a single diel cycle. Besides, oscillations in the phytoplankton succession rates were registered during all the studied period. Usually, equilibrium is not expected in aquatic ecosystems under very rapidly fluctuating conditions (O’Farrell et al. 2003O’FARRELL I, SINISTRO R, IZAGUIRRE I & UNREIN F. 2003. Do steady state assemblages occur in shallow lentic environments from wetlands? Hydrobiologia 502: 197-209.) or with intermittent mixing (Allende & Izaguirre 2003ALLENDE L & IZAGUIRRE I. 2003. The role of physical stability on the establishment of steady state in the phytoplankton community of two Maritime Antarctic lakes. Hydrobiologia 502: 211-224., Naselli-Flores et al. 2003NASELLI-FLORES L, PADISÁK J & DOKULIL M. 2003. Phytoplankton and the equilibrium concept: the ecology of steady state assemblages. Developments in Hydrobiology 172: 1-416. (Reprinted from Hydrobiologia, 502).). Non-equilibrium theories attribute a basic role to environmental disturbances occurring with sufficient frequency to disrupt the course of competitive exclusion (Harris 1986HARRIS GP. 1986. Phytoplankton ecology: structure, function and fluctuation. Chapman and Hall, London, UK, 384 p., Wilson 1990WILSON JB. 1990. Mechanisms of species coexistence: twelve explanations for Hutchinson’s ‘paradox of the plankton’: evidence from New Zealand plant communities. N Z J Ecol 13: 17-42., Sommer et al. 1993SOMMER U, PADISÁK J, REYNOLDS CS & JUHÁSZ-NAGY P. 1993. Hutchinson’s heritage: the diversity-disturbance relationship in phytoplankton. Hydrobiologia 249: 1-8., Padisák 1994PADISÁK J. 1994. Identification of relevant time-scales in nonequilibrium community dynamics: conclusions from phytoplankton surveys. N Z J Ecol 18(2): 169-176., Krebs 2001KREBS CH. 2001. Ecology: Experimental Analysis of Distribution and Abundance. Addison Wesley, San Francisco, 695 p., Lengyel et al. 2015LENGYEL E, PADISÁK J & STENGER-KOVÁCS C. 2015. Establishment of equilibrium states and effect of disturbances on benthic diatom assemblages of the Torna-stream, Hungary. Hydrobiologia 750: 43-56.). These recurrent perturbations in the littoral zone of shallow lakes are generally related to climatic variation (Cantonati & Lowe 2014CANTONATI M & LOWE RL. 2014. Lake benthic algae: toward an understanding of their ecology. Freshw Sci 33(2): 475-486.), or processes resulting from terrestrial-aquatic interaction (Meerhoff & Jeppensen 2009MEERHOFF M & JEPPESEN E. 2009. Shallow lakes and ponds. In: LIKENS G (Ed). Encyclopedia of inland waters. Oxford, Elsevier, p. 343-353.). These may be one of the explanations to the species turnover verified in the present study (Fig. 5). For instance, D. sertularia and S. obtusus were benefited by wind action as evidenced by the RDA, in the same way that SRP drove the O. lacustris development. Furthermore, the fast environmental dynamics of the littoral zone added to the fast response time of phytoplankton and the biotic interactions not considered in the present study may also have contributed to that.

Studies on the phytoplankton of Lake Mangueira have been carried out using different approaches. Most of these studies were performed in the pelagic zone and showed that changes in both monthly (Crossetti et al. 2007CROSSETTI LO, CARDOSO LS, CALLEGARO VLM, SILVA SA, WERNER V, ROSA Z & MOTTA-MARQUES D. 2007. Influence of the hydrological changes on the phytoplankton structure and dynamics in a subtropical wetland-lake system. Acta Limnol Bras 19: 315-329.) and seasonal (Crossetti et al. 2013CROSSETTI LO, STENGER-KOVÁCS C & PADISÁK J. 2013. Coherence of phytoplankton and attached diatom-based ecological status assessment in Lake Balaton. Hydrobiologia 716: 87-101., 2018, Freitas-Teixeira et al. 2016FREITAS-TEIXEIRA LM, BOHNENBERGER JE, RODRIGUES LR, SCHULZ UH, MOTTA-MARQUES D & CROSSETTI LO. 2016. Temporal variability determines phytoplankton structure over spatial organization in a large shallow heterogeneous subtropical lake. Inland Waters 6: 325-335.) temporal scales were strongly associated with environmental variation influenced by the lake’s hydrodynamics. Similarly, another study demonstrated a significant correlation between environmental dissimilarity and phytoplankton dissimilarity based on long-term monitoring data (12 years) (Bohnenberger et al. 2017BOHNENBERGER JE, RODRIGUES LR, MOTTA-MARQUES D & CROSSETTI LO. 2017 Environmental dissimilarity over time in a large subtropical shallow lake is differently represented by phytoplankton functional approaches. Mar Freshw Res 69: 95-104.). Then, even though short-term sampling has not been deeply explored, our experience led us to suppose that in the pelagic habitat of this lake phytoplankton steady states may be less frequent, but are not impossible to occur. An unpublished study carried out with samplings on every three days (for 60 days, in the summer of 2012) in Lake Mangueira showed phytoplankton steady states occurring both in the pelagic and littoral zones, but the equilibrium period had a shorter duration in the littoral. There is evidence that in shallow lakes the conditions for the establishment of phytoplankton steady states are more predictable than in deep lakes (Naselli-Flores et al. 2003NASELLI-FLORES L, PADISÁK J & DOKULIL M. 2003. Phytoplankton and the equilibrium concept: the ecology of steady state assemblages. Developments in Hydrobiology 172: 1-416. (Reprinted from Hydrobiologia, 502)., Nixdorf et al. 2003NIXDORF B, MISCHKE U & RÜCKER J. 2003. Phytoplankton assemblages and steady state in deep and shallow eutrophic lakes – an approach to differentiate the habitat properties of Oscillatoriales. Hydrobiologia 502: 111-121.). Besides, in a system adapted to perturbation, as in the case of continuously mixed systems (shallow lakes), this represents a sufficiently stable condition to allow phytoplankton steady state, while the calm phases would be the disturbance (Chorus & Schlag 1993CHORUS I & SCHLAG G. 1993. Importance of intermediate disturbances for the species composition and diversity of phytoplankton in two very different Berlin lakes. Hydrobiologia 249: 435: 67-92.).

The hydrodynamics of the littoral zone of shallow lakes can be complex due to a series of factors that influence the movement of the water mass in this zone. For instance, studies have already shown that wind-driven circulation or ship waves can lead to sediment resuspension in the littoral zone of large lakes (Hofmann et al. 2008HOFMANN H, LORKE A & PEETERS F. 2008. Temporal scales of water-level fluctuations in lakes and their ecological implications. Hydrobiologia 613: 85-96., 2011). Likewise, wind direction might be an important factor for horizontal transport, influencing the patchiness of phytoplankton in lakes (Verhagen 1994VERHAGEN JHG. 1994. Modeling phytoplankton patchiness under the influence of wind-driven currents inlakes, Limnol Oceanogr 39: 1551-1565.). Besides, horizontal convective exchanges flow between the littoral zone and open waters of shallow lakes may occur (Stefan et al. 1989STEFAN HG, HORSCH GM & BARKO JW. 1989. A model for the estimation of convective exchange in the littoral region of a shallow lake during cooling. Hydrobiologia 174: 225-234.), influencing, for example, the nutrient exchange (James & Barco 1991JAMES WF & BARKO JW. 1991. Estimation of phosphorus exchange between littoral and pelagic zones during nighttime convection circulation. Limnol Oceanogr 36(1): 179-187.). Not to mention the presence of macrophytes, which may attenuate surface-generated turbulence from penetrating the water column (Coates & Folkard 2009COATES MJ & FOLKARD AM. 2009. The effects of littoral zone vegetation on turbulent mixing in lakes. Ecol Modell 220: 2714-2726.). In the present study, although we have not observed the direct influence of wind (speed and direction) on the abiotic and biological variables, it may have influenced the dynamics of water masses, not only intensifying the effect of macrophytes on limnological features through transport processes but also justifying the wide environmental variability and the differences observed between the sampling stations. Then, for a better understanding of the environmental and biological dynamics in the littoral region of systems such as Lake Mangueira, the incorporation of variables related to the flow of water masses in this zone is recommended.

Although the extension or the effects of the macrophyte beds near the sampling sites was not quantified, other studies conducted in the southern region of Lake Mangueira have already reported the strong influence that the plants have on limnological processes (They et al. 2013THEY NH, MOTTA-MARQUES D, SOUZA RS & RODRIGUES LR. 2013. Short-Term Photochemical and Biological Unreactivity of Macrophyte-Derived Dissolved Organic Matter in a Subtropical Shallow Lake. J Ecosyst 316709: 1-9., Rodrigues et al. 2014RODRIGUES LR, FONTOURA NF & MOTTA-MARQUES D. 2014. Food-web structure in a subtropical coastal lake: how phylogenetic constraints may affect species linkages. Mar Freshw Res 65: 453-465., 2015, Faria et al. 2016FARIA DM, CARDOSO LS & MOTTA-MARQUES D. 2016. Epiphyton dynamics during an induced succession in a large shallow lake: wind disturbance and zooplankton grazing act as main structuring forces. Hydrobiologia 788: 267-280., Finkler Ferreira et al. 2018FINKLER FERREIRA T, CROSSETTI LO, MOTTA-MARQUES D, CARDOSO LS, FRAGOSO CR JR & VAN NES EH. 2018. The structuring role of submerged macrophytes in a large subtropical shallow lake: clear effects on water chemistry and phytoplankton structure community along a vegetated pelagic gradient. Limnologica 69: 142-154.). Macrophytes can affect both the dynamics of biological communities (Howard-Williams & Lenton 1975HOWARD-WILLIAMS C & LENTON G. 1975. The role of the littoral zone in the functioning of a shallow tropical lake ecosystem. Fresh Biol 5(5): 445-459., Muylaert et al. 2010MUYLAERT K ET AL. 2010. Influence of nutrients: submerged macrophytes and zoop lanktongrazing on phytoplankton biomass and diversity along a latitudinal gradient in Europe. Hydrobiology 653: 79-90., Thomaz & Cunha 2010THOMAZ SM & CUNHA ER DA. 2010. The role of macrophytes in habitat structuring in aquatic ecosystems: methods of measurement, causes and consequences on animal assemblages’ composition and biodiversity. Acta Limnol Bras 22 (2): 218-236., Teixeira de Mello et al. 2015TEIXEIRA DE MELLO F, OLIVEIRA VA DE, LOVERDE OLIVEIRA SM, HUSZAR VLM, BARQUÍN J, IGLESIAS C, SILVA TSF, DUQUE-ESTRADA CHE, SILIÓ-CALZADA A & MAZZEO N. 2015. The structuring role of free-floating plants on the fish community in a tropical shallow lake: an experimental approach with natural and artificial plants. Hydrobiologia 778: 167-178., Iacarella et al. 2018IACARELLA JC, BARROW JL, GIANI A, BEISNER BE & GREGORY-EAVES I. 2018. Shifts in algal dominance in freshwater experimental ponds across differing levels of macrophytes and nutrients. Ecosphere 9(1): e02086.) and nutrient cycling (Havens et al. 2004HAVENS KE, SHARFSTEIN B, RODUSKY AJ & EAST TL. 2004. Phosphorus accumulation in the littoral zone of a subtropical lake. Hydrobiologia 517: 15-24., They et al. 2013THEY NH, MOTTA-MARQUES D, SOUZA RS & RODRIGUES LR. 2013. Short-Term Photochemical and Biological Unreactivity of Macrophyte-Derived Dissolved Organic Matter in a Subtropical Shallow Lake. J Ecosyst 316709: 1-9.) in shallow lakes, by acting as nutrient sinks in several ways (Carpenter 1981CARPENTER SR. 1981. Submersed vegetation: an internal factor in lake ecosystem succession. Am Nat 118: 372-383., Kufel & Kufel 2002KUFEL L & KUFEL I. 2002. Chara beds acting as nutrient sinks in shallow lakes - a review. Aquat Bot 72: 249-260.). In this sense, the analyses performed in this study indicated that the occurrence of macrophytes may have played an effective role for littoral phytoplankton structure of Lake Mangueira. Humic substances, which are released by macrophytes, proved to be one of the main drivers of phytoplankton dynamics.

As estimated by Abs365, these substances exhibited a negative correlation with phytoplankton biomass at both stations and were also related to succession rate and richness at S2. A negative interaction between macrophytes and phytoplankton had already been registered for the littoral zone of Lake Mangueira (Finkler Ferreira et al. 2018FINKLER FERREIRA T, CROSSETTI LO, MOTTA-MARQUES D, CARDOSO LS, FRAGOSO CR JR & VAN NES EH. 2018. The structuring role of submerged macrophytes in a large subtropical shallow lake: clear effects on water chemistry and phytoplankton structure community along a vegetated pelagic gradient. Limnologica 69: 142-154.), when phytoplankton biomass was negatively influenced by humic substances and the presence of the plants. The authors concluded that the effects of the macrophytes on the phytoplankton structure and water quality could be seen beyond the boundaries of the vegetated area. In our survey, few species had high positive associations with humic substances: only C. minor, A. koordersii and Peridiniopsis sp. According to Wetzel (2001)WETZEL RG. 2001. Limnology. Lake and River Ecosystems, Elsevier Academic Press, San Diego, 1006 p., higher concentrations of humic substances can select only those species that are adapted to those conditions. These substances can make nutrients unavailable for primary producers (Lenard & Ejankowski 2017LENARD T & EJANKOWSKI W. 2017. Natural water brownification as a shift in the phytoplankton community in a deep hard water lake. Hydrobiologia 787: 153-166.), and affect not only underwater light intensity but also the penetration of photosynthetically active radiation into the water (Wetzel 2001WETZEL RG. 2001. Limnology. Lake and River Ecosystems, Elsevier Academic Press, San Diego, 1006 p., Ejankowski & Lenard 2015EJANKOWSKI W & LENARD T. 2015. Climate driven changes in the submerged macrophyte and phytoplankton community in a hard water lake. Limnologica 52: 59-66.). More specifically, they inhibit the development of cyanobacteria, which seem unable to use their accessory pigments in the reddish light caused by the higher concentration of yellow humic substances (Steinberg et al. 2006STEINBERG CEW ET AL. 2006. Dissolved humic substances - Ecological driving forces from the individual to the ecosystem level? Fresh Biol 51(7): 1189-1210.). Therefore, most of the species of cyanobacteria listed in the present study were negatively related to Abs365, demonstrating the negative interaction between this group and macrophytes, as widely reported in others studies (Gross et al. 2007GROSS EM, HILT S, LOMBARDO P & MULDERIJ G. 2007. Searching for allelopathic effects of submerged macrophytes on phytoplankton-state of the art and open questions. Hydrobiologia 584: 77-88., Mulderij et al. 2007MULDERIJ G, VAN NES EH & DONK EV. 2007. Macrophyte-phytoplankton interactions: the relative importance of allelopathy versus other factors. Ecol Modell 204: 85-92., Vanderstukken et al. 2014VANDERSTUKKEN M, DECLERCK SAJ, DECAESTECKER E & MUYLAERT K. 2014. Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii Planch. Fresh Biol 59: 930-941., They et al. 2015THEY NH, FINKLER FERREIRA T, MOTTA-MARQUES D, RODRIGUES LR, SILVEIRA SB, ARRIADA AA, CROSSETTI LO, CARDOSO LS, FRAGOSO CR JR. 2015. Allelopathic effects of macrophytes in subtropical shallow lakes. In: PRICE JE (Ed). New Developments in Allelopathy Research, Nova Publishers, New York, p. 89-134., Mohamed 2017MOHAMED ZA. 2017. Macrophytes-Cyanobacteria allelopathic interactions and their implications for water resources management − a review. Limnologica 63: 122-132.). Besides, species of blue green algae and diatoms are often significantly inhibited by allelochemicals (Hilt & Gross 2008HILT S & GROSS EM. 2008. Can allelopathically active submerged macrophytes stabilize clear-water states in shallow lakes? Basic Appl Ecol 9(4): 422-432., Reitsema et al. 2018REITSEMA RE, MEIRE P & SCHOELYNCK J. 2018. The future of freshwater macrophytes in a changing world: dissolved organic carbon quantity and quality and its interactions with macrophytes. Front Plant Sci 9: 629.), and some macrophytes species occur in Lake Mangueira possess such inhibitory capacities (They & Motta-Marques, 2019THEY NH & MOTTA-MARQUES D. 2019. The structuring role of macrophytes on plankton community composition and bacterial metabolism in a large subtropical shallow lake. Acta Limnol Bras 31: 1-20.).

Another particularity registered in the littoral zone of Lake Mangueira was the marked oscillation of nutritional conditions. Nutrient availability in the littoral zone can be strongly influenced by sediment destabilization (Kosten & Meerhoff 2014KOSTEN S & MEERHOFF M. 2014. Lake Communities. Encyclopedia of Life Sciences (ELS) 15: 1-11.), the action of fish (Meerhoff & Jeppensen 2009), high assimilation by macrophytes (They et al. 2014THEY NH, MOTTA-MARQUES D, CROSSETTI LO, BECKER V, CANTERLE E, RODRIGUES LR, CARDOSO LS & FRAGOSO CR JR. 2014. Phytoplankton ecological interactions in freshwater ecosystems - integrating relationships in subtropical shallow lakes. In: SEBASTIÁ MT (Ed). Phytoplankton. Nova Science Publishers, New Work, p. 73-129.) and bacterial activity (Wetzel 1983WETZEL RG. 1983. Attached algal-substrata interactions: fact or myth, and when and how? In: WETZEL R (Ed). Periphyton of freshwater ecosystems. Springer, Netherlands, p. 207-215.). Although these factors were not evaluated here, we recognized that their action could explain the rapid variation in nutrients during the studied period. Slight variation in nutrient levels within short sampling intervals result in a rapid change in the structure of an algae community (Dantas et al. 2008DANTAS EW, MOURA AN, BITTENCOURT OLIVEIRA MC, ARRUDA NETO JDT & CAVALCANTI ADC. 2008. Temporal variation of the phytoplankton community at short sampling intervals in the Mundaú reservoir, Northeastern Brazil. Acta Bot Bras 22(4): 970-982.), as we found in the littoral zone of Lake Mangueira. In addition, more oligotrophic conditions stimulate greater competition among phytoplankton and bacteria for nutrients (They et al. 2014THEY NH, MOTTA-MARQUES D, CROSSETTI LO, BECKER V, CANTERLE E, RODRIGUES LR, CARDOSO LS & FRAGOSO CR JR. 2014. Phytoplankton ecological interactions in freshwater ecosystems - integrating relationships in subtropical shallow lakes. In: SEBASTIÁ MT (Ed). Phytoplankton. Nova Science Publishers, New Work, p. 73-129.). The positive correlations between SRP and phytoplankton total biomass, succession rate, species richness, and Shannon diversity at S1, and the biplot arrangement of the RDA, demonstrate that this resource was an important driver of species performance at this site, which was not recorded at S2, where humic substances were found at higher concentrations. The fact that S1 had substantially lower values of SRP, remaining below the overall limiting concentrations for phytoplankton growth during several periods (Reynolds 2006REYNOLDS CS. 2006. The ecology of phytoplankton: Ecology, Biodiversity and Conservation. Cambridge University Press, Cambridge, 564 p.), may represent a competitive advantage for the small cyanobacteria and chlorophytes present. Most species of these groups benefited from this nutrient, as demonstrated by the integrated analysis (RDA). These organisms possess high surface-volume ratios, which increases the capacity of nutrient absorption (Foy 1980FOY RH. 1980. The influence of surface to volume ratio on the growth rates of planktonic blue- green algae. Br Phycol J 15(3): 279-289., Negro et al. 2000NEGRO AI, DE HOYOS C & VEJA JC. 2000. Phytoplankton structure and dynamics in Lake Sanabria and Valparaíso reservoir (NW Spain). Hydrobiologia 424: 25-37., Passarge et al. 2006PASSARGE J, HOL S, ESCHER M & HUISMAN J. 2006. Competition for nutrients and light: stable coexistence, alternative stable states, or competitive exclusion? Ecol Monogr 76(1): 57-72., Reynolds 2006REYNOLDS CS. 2006. The ecology of phytoplankton: Ecology, Biodiversity and Conservation. Cambridge University Press, Cambridge, 564 p., Brasil & Huszar 2011BRASIL J & HUSZAR VLM. 2011. O papel dos traços funcionais na ecologia do fitoplâncton continental. Oecol Aust 15(4): 799-834.), and promote faster replication rates than those of larger algae (Raven 1998RAVEN JA. 1998. Small is beautiful: the picophytoplankton. Funct Ecol 12(4): 503-513.). This property is important in highly dynamic ecosystems where environmental variables are constantly changing (Palijan 2017PALIJAN G. 2017. Short-term response of the phytoplankton size structure to flooding. Inland Waters 7(2): 192-199.), such as the littoral zone of Lake Mangueira.

Our results showed that the littoral phytoplankton of Lake Mangueira is inserted in a highly stochastic and dynamic compartment with high environmental variability. Furthermore, mixing shallow lakes are traditionally considered fast-changing and fluctuating ecosystems featuring quick and unpredictable phytoplankton changes (Naselli-Flores et al. 2003NASELLI-FLORES L, PADISÁK J & DOKULIL M. 2003. Phytoplankton and the equilibrium concept: the ecology of steady state assemblages. Developments in Hydrobiology 172: 1-416. (Reprinted from Hydrobiologia, 502).). The non-steady state found for the littoral phytoplankton of the present study was influenced by the nutritional availability in Lake Mangueira. The nearby presence of macrophytes seemed to have influenced the environmental conditions by contributing to species turnover on a short-time scale, demonstrating that the littoral phytoplankton assemblage in Lake Mangueira experiences a constant redefinition of community structure. Further studies of littoral phytoplankton regarding a functional approach, and broader efforts to explore the complex dynamics of biological interactions found in this compartment, should be considered. Finally, the littoral zone of shallow lakes should be included in ecological studies in order to provide enhanced scientific support about the importance of this compartment for overall lake dynamics and lake conservation and management programs.

ACKNOWLEDGMENTS

The authors thank Erik Russell Wild (University of Wisconsin-Stevens point) for English revision and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) of Brazil for financial support.

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Publication Dates

  • Publication in this collection
    01 July 2024
  • Date of issue
    2024

History

  • Received
    10 Oct 2022
  • Accepted
    16 Oct 2023
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