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Effect of seasonality and estuarine waters on the phytoplankton of the Guamá River (Belém, Amazon, Brazil)

Abstract

This study aimed to analyze the application of the Phytoplankton Community Index-PCI and Functional Groups-FG in determining the water quality of the Guamá River (Pará, Amazônia, Brazil). Samplings occurred monthly for analyses of phytoplankton and physical and chemical parameters, for two years, at the station where water was collected for human supply consumption. Seasonality influenced electrical conductivity, total suspended solids, dissolved oxygen, transparency, winds, true color, and N-ammoniacal. The ebb tide showed high turbidity and suspended solids. The density varied seasonally with the highest values occurring in September and December (61.1 ind mL-1 and 60.2 ind mL-1, respectively). Chlorophyll-a was more elevated in December (21.0 ± 4.7 µg L-1) and chlorophyll-c higher in relation to clorophyll- b indicated the dominance of diatoms. Functional Group P prevailed in the study months. Through the PCI índex the waters of Guamá River varied from reasonable to excellent and the TSI ranged from oligo to mesotrophic. The use of Functional Groups proved to be a promising tool in the determination of water quality since it covered the most abundant species in the Environment, but the PCI is not adequate to characterize Amazonian white-waters rivers, which have diatoms as the leading dominant group.

Key words
bioindicators; diatoms; functional groups; water

INTRODUCTION

Eutrophication is one of the greatest threats to aquatic environments in the world. It comprises the increase of nutrients, mainly nitrogen and phosphorus, in environments with the consequent increase of primary producers, such as clorophytes, euglenophytes, diatoms, dinoflagellates, and cyanobacteria, the latter being important in public health studies due to the production of harmful toxins to humans (Lewis et al. 2011LEWIS WM, WURTSBAUGH WA & PAERL HW. 2011. Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environ Sci Technol 45: 10300-10305., Wurtsbaugh et al. 2019WURTSBAUGH WA, PAERL HW & DODDS WK. 2019. Nutrients, eutrophication and harmful algal blooms along the freshwater to marine continuum. Wiley Interdisciplinary Reviews: Water 6: 1-27.).

Eutrophication is a process associated with punctual and diffuses sources of nutrients, with urban sewage being the most significant contributor to its occurrence among underdeveloped countries (Suwarno et al. 2014SUWARNO D, LÖHR A, KROEZE C & WIDIANARKO B. 2014. Fast increases in urban sewage inputs to rivers of Indonesia. Environ Dev Sustain 16: 1077-1096.). In the Metropolitan Region of Belém (Pará), only 15.7% of the population receives sewage collection services, and only 2.8% are treated, overall, there are 1.2 million people without sewage services (Trata Brasil 2020TRATA BRASIL. 2020. Painel de Saneamento Brasil. https://www.painelsaneamento.org.br/explore/localidade?SE%5Bl%5D=151 (acessed: February/2021).
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), and all the sewage goes to the creeks and rivers in the region, including the mouth of the Guamá River.

The mouth of the Guamá River is a fluvial-estuarine hydric system that converges, together with the Acará River and the Guajará Bay, into the Pará River estuary and the Marajó Bay, which communicates with the Atlantic Ocean (Silva et al. 2020SILVA LG, SILVA GEL, SILVA AB & MENEZES RS. 2020. Modelagem da dinâmica evolutiva da qualidade da água na Baía do Guajará - Belém-PA. Braz J Dev 6: 4649-4660.). The hydrodynamics suffers variations linked mainly to seasonal rainfall patterns, along with astronomical tidal forcing, river discharge, and winds (Böck et al. 2010BÖCK CS, ASSAD LPF & LANDAU L. 2010. Variabilidade hidrodinâmica em um estuário relacionada com mudanças batimétricas Mecánica Computacional XXIX: 8047-8071.).

It has social and economic importance for the Metropolitan Region of Belém and the insular riverside population because it is essential for fishing, navigation, leisure, industry, tourism, and trade. Its waters are abstracted for the water supply system of Belém, being pumped continuously to the reservoirs Água Preta and Bolonha , which are inside the floodplain forest in a State Park (E.B. Sousa, unpublished data).

Phytoplankton is used as an indicator of water quality and changes in the aquatic environment by many countries around the world and is included in legal monitoring tools; that is, they are water quality assessment tools required by the legislation of some countries (Vadrucci et al. 2007VADRUCCI MR, CABRINI M & BASSET A. 2007. Biovolume determination of phytoplankton guilds in transitional water ecosystems of mediterranean ecoregion. Transit Waters Bull 2: 83-102., Kelly et al. 2007KELLY M, JUGGINS S, GUTHRIE R, PRITCHARD S, JAMIESON J, RIPPEY B, HIRST H & YALLOP M. 2007. Assessment of ecological status in U.K. rivers using diatoms. Freshw Biol 53: 403-422., Lobo et al. 2015LOBO EA, SCHUCH M, HEINRICH CG, COSTA AB, DÜPONT A, WETZEL CE & ECTOR L. 2015. Development of the Trophic Water Quality Index (TWQI) for subtropical temperate Brazilian lotic systems. Environ Monit Assess 187: 354., Kozak et al. 2020KOZAK A, BUDZYŃSKA A, DONDAJEWSKA-PIELKA R, KOWALCZEWSKA-MADURA K & GOŁDYN R. 2020. Functional groups of phytoplankton and their relationship with environmental factors in the restored Uzarzewskie Lake. Water 12: 1-14.), although they get different approaches, such as indexes, species list, taxonomic groups, functional groups (Gharib et al. 2011GHARIB SM, EL-SHERIF ZM, ABDEL-HALIM AM & RADWAN AA. 2011. Phytoplankton and environmental variables as a water quality indicator for the beaches at Matrouh, south-eastern Mediterranean Sea, Egypt: an assessment. Oceanologia 53: 819-836., Miao et al. 2019MIAO X, WANG S, LIU M, MA J, HU J, LI T & CHEN L. 2019. Changes in the phytoplankton community structure of the Backshore Wetland of Expo Garden, Shanghai from 2009 to 2010. Aquac Fish 4: 198-204.), among others.

Among the different uses of phytoplankton, it is possible to identify, with greater or lesser effectiveness, the attributes or structures altered as a result of environmental changes, which lead to interpretations about the environment, especially the trophic state of rivers, lakes, and reservoirs (Rott et al. 2006ROTT E, CANTONATI M, FÜREDER L & PFISTER P. 2006. Benthic algae in high altitude streams of the Alps - A neglected component of the aquatic biota. Hydrobiologia 562: 195-216., Rodrigues et al. 2019RODRIGUES EHC, VICENTIN AM, MACHADO LS, POMPÊO MLM & CARLOS VM. 2019. Phytoplankton Trophic State and Ecological Potential in reservoirs in the State of São Paulo, Brazil. Ambiente & Água 14: 1-12., Meng et al. 2020MENG F, LI Z, LI L, LU F, LIU Y, LU X & FAN Y. 2020. Phytoplankton alpha diversity indices response the trophic state variation in hydrologically connected aquatic habitats in the Harbin Section of the Songhua River. Scientific Reports-UK 10: 1-13.). For this purpose, there are advances in methodologies and standards on the use of phytoplankton as a bioindicator (Vadrucci et al. 2007VADRUCCI MR, CABRINI M & BASSET A. 2007. Biovolume determination of phytoplankton guilds in transitional water ecosystems of mediterranean ecoregion. Transit Waters Bull 2: 83-102., Varkitzi et al. 2018VARKITZI I ET AL. 2018. Pelagic habitats in the Mediterranean Sea: A review of Good Environmental Status (GES) determination for plankton components and identification of gaps and priority needs to improve coherence for the MSFD implementation. Ecol Indic 95: 203-218., Francé et al. 2021FRANCÉ J ET AL. 2021. Large-scale testing of phytoplankton diversity indices for environmental assessment in Mediterranean sub-regions (Adriatic, Ionian and Aegean Seas). Ecol Indic 126: 2-19.) based on local realities and international experiences to more clearly interpret the conditions of aquatic environments and assist public managers in decision making.

Brazilian health and environment agencies and councils do not use phytoplankton as a direct bioindication tool, suggesting the use of organisms and biological communities in general (Pires et al. 2015PIRES DA, TUCCI A, CARVALHO MC & LAMPARELLI MC. 2015. Water quality in four reservoirs of the metropolitan region of São Paulo, Brazil. Acta Limnol Bras 27: 370-380.) for this purpose in paragraph § 3, article 8, of Resolution 357/2005 of the National Council for the Environment- CONAMA (CONAMA 2005CONAMA - CONSELHO NACIONAL DO MEIO AMBIENTE. 2005. Resolução n 357, 18 de março de 2005. Diário Oficial 053: 58-63.). In addition, due to the increase in blooms, the monitoring of planktonic cyanobacteria receives constant updates, such as the current ordinance of the Ministry of Health n. 888/2021, aimed at monitoring water quality for human consumption.

In this context, the aim of this study was to evaluate the dynamics of phytoplankton and analyze the application of the Phytoplankton Community Index-PCI, which classifies water quality from phytoplankton groups, as an example of a local approach used in reservoirs and rivers from the state of São Paulo (CETESB 2019CETESB - COMPANHIA AMBIENTAL DO ESTADO DE SÃO PAULO. 2019. MARTINS MHRB, MENEGON JR, LAMPARELLI MC, MORENO FN, MIDAGLIA CLV & MEDEIROS LA. Qualidade das águas interiores no estado de São Paulo. São Paulo, 284 p.), and the Phytoplankton Functional Groups-FG, which describes the trophic conditions of the environment, used in many countries (Reynolds et al. 2002REYNOLDS SC, HUSZAR V, KRUK C, NASELLI FLORES L & MELO S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24: 417-428., Padisák et al. 2009PADISÁK J, CROSSETTI LO & NASELLI FLORES L. 2009. Use and misuse in the application of the phytoplankton functional classification: A critical review with updates. Hydrobiologia 621: 1-19.) as tools in determining the environmental conditions of the Guamá River.

There are few studies in this region on phytoplankton, where we cite Moreira Filho et al. (1974)MOREIRA FILHO H, VALENTE MOREIRA IM & TRIPPIA CECY II. 1974. Diatomáceas do Rio Guamá, Foz do rio - Belém - Estado do Pará. Leandra 3/4: 123-135. with the first survey on the phytoplankton composition of this river, identifying the predominance of diatoms. Paiva et al. (2006)PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146. describe the dominance, in terms of biomass, of phytoplagellates followed by diatoms.

More recent studies cite diatoms as the main components of phytoplankton, such as Monteiro et al. (2009)MONTEIRO MDR, MELO NFAC, ALVES MAMS & PAIVA RS. 2009. Composição e distribuição do microfitoplâncton do rio Guamá no trecho entre Belém e São Miguel do Guamá, Pará, Brasil Composition and distribution of the microphytoplankton from Guamá River between Belém and São Miguel do Guamá, Pará, Brazil. Bol Mus Par Emílio Goeldi Ciênc Nat 4: 341-351. and Rocha Neto et al. (2017)ROCHA NETO OD, SILVA BM & PAIVA RS. 2017. Variação Dos Parâmetros Físico-Químicos, Composição E Biomassa Fitoplanctônica Em Uma Estação Fixa Na Foz Do Rio Guamá, Belém, Pará-Brasil. Boletim Técnico Científico do CEPNOR 16: 19.; the latter indicated a seasonal variation with higher phytoplankton biomass in the less rainy period. Thus, the studies are insipient and do not bring the relationship of phytoplankton with physical and chemical parameters and water quality, which vary seasonally and between tides (Silva et al. 2020SILVA LG, SILVA GEL, SILVA AB & MENEZES RS. 2020. Modelagem da dinâmica evolutiva da qualidade da água na Baía do Guajará - Belém-PA. Braz J Dev 6: 4649-4660.).

The following questions guide the present study: (i) there is seasonal variation in phytoplankton? (ii) what are the main physical and chemical parameters that influence phytoplankton dynamics? and (iii) what are the trophic conditions and water quality of the Guamá River based on the PCI and FG of phytoplankton?

MATERIALS AND METHODS

Sample design and study area

The Guamá River is located in the state of Pará (Eastern Amazon, Brazil). It is approximately 700 km long, its mouth flows into the Pará and Acará rivers, suffering the influence of oceanic tides and receiving constant inputs of sediments from the Guajará Bay, and it may become oligohaline at the height of the less rainy season (Paiva et al. 2006PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146., Monteiro et al. 2009MONTEIRO MDR, MELO NFAC, ALVES MAMS & PAIVA RS. 2009. Composição e distribuição do microfitoplâncton do rio Guamá no trecho entre Belém e São Miguel do Guamá, Pará, Brasil Composition and distribution of the microphytoplankton from Guamá River between Belém and São Miguel do Guamá, Pará, Brazil. Bol Mus Par Emílio Goeldi Ciênc Nat 4: 341-351.).

This rivercrosses 13 cities until it flows into Belém, Ananindeua, and Marituba, the most densely urbanized municipalities in the Metropolitan Region of Belém, from which it receives the discharge from many urban drainage channels and other streams in the region, during the floods and ebbs of the river tides and by the surface runoff of continental waters through rains (Santos et al. 2012SANTOS SN, LAFONI JM, CORRÊA JAM, BABINSK M, DIAS FF & TADDEI MHT. 2012. Distribuição e assinatura isotópica de Pb em sedimentos de fundo da Foz do Rio Guamá e da Baía do Guajará (Belém - Pará). Quim Nova 35: 249-256.). The average annual temperature is 25 °C, air humidity above 80%, and rainfall of 2,889 mm year-1 (Bezerra et al. 2011BEZERRA MO, MEDEIROS C, KRELLING APM, ROSÁRIO RP & ROLLNIC M. 2011. Physical oceanographic behavior at the Guama/Acara-Moju and the Paracauari river mouths, Amazon Coast (Brazil). J Coast Res 64: 1448-1462., INMET 2021INMET- INSTITUTO NACIONAL DE METEOROLOGIA. 2021. http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep. (acessed: May/2021).
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).

Samples were collected in the Guamá River at the point where the water is taken from the river for the Água Preta and Bolonha reservoirs (1º27’15’’S- 4º24’08’’W) (Figure 1), monthly from May/2019 to April/2021, covering two seasonal cycles of the region, during flood and ebb tides. Water samples were collected for phytoplankton analyses, and the physical and chemical parameters were measured. The rainy months are from January to May, and the less rainy (or dry) from July to November, with June being considered a rainy-dry transition and December a dry-rainy transition, according to Moraes et al. 2005MORAES BC, COSTA JMN, COSTA ACL & COSTA MH. 2005. Variação espacial e temporal da precipitação no estado do Pará. Acta Amaz 35: 207-214..

Figure 1
Map of the study area (Guamá River), showing the adduction point in front of the water catchment station for the public supply reservoirs in the Metropolitan Region of Belém (Pará, Brazil).

Sampling and analyses of physical and chemical parameters

The data from precipitation and winds were collected from the Belém meteorological station (code 82191, latitude -1.43, longitude -48.42, and altitude 10 m) and provided by INMET (2021)INMET- INSTITUTO NACIONAL DE METEOROLOGIA. 2021. http://www.inmet.gov.br/portal/index.php?r=bdmep/bdmep. (acessed: May/2021).
http://www.inmet.gov.br/portal/index.php...
. Water transparency was estimated using a Secchi disk. The water temperature (°C), hydrogenic potential (pH), salinity, electrical conductivity (EC), total dissolved solids (TDS), and dissolved oxygen (DO) were measured in situ by the multiparametric probe HI 9828 - HANNA. For the other variables (turbidity, true color, total suspended solids (TSS), and nutrients), water samples were collected with bottles according to the 1060 B method (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.).

Turbidity and true color were determined by the nephelometric method 2130 B and 2120 D, respectively (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.), and the TSS by the photometric method (Krawczyk & Gonglewski 1969KRAWCZYK D & GONGLEWSKI N. 1969. Determining suspended solids using a spectrophotometer. Sewage Ind Wastes 31: 1159-1164.). N-ammoniacal (N-NH3), nitrate (NO3 -), and total phosphorus (TP) were determined by ion chromatography (ICS Dual 2000) method 4110 B (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.).

Sampling and analyses of biotic variables

Water samples were collected directly from the subsurface in amber bottles and refrigerated for the clorophyll analyses. For the phytoplanktonic samples water were collected directly from the subsurface.

In the laboratory, phytoplanktonic samples were fixed with neutral formaldeide (4%), methodology 10200 B (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.). Chlorophyll -a, b, and c samples were analyzed using spectrophotometry (D2000 HANNA®) according to the 10200 H method (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.). Methods 10200 C and 10200 F were used for sedimentation and quantification of phytoplankton (ind mL-1), respectively (APHA 2017APHA - AMERICAN PUBLIC HEALTH ASSOCIATION. 2017. Standard Methods for the Examination of Water and Wastewater. 23 ed., Washington, 1545 p.), through an optical invertoscope (AXIOVERT.A1) with camera-attached eyepieces for measuring samples (AXIOCAM ICC5) with measurement software, under a magnification of 400x. The identification, nomenclature, and taxonomic classification of phytoplankton were performed according to specialized literature: Round et al. (2007)ROUND FE, CRAWFORD RM & MANN DG. 2007. Diatoms: Biology and Morphology of the Genera 5 ed., Cambridge: Cambridge University Press, 760 p., Komárek & Anagnostidis (2005KOMÁREK J & ANAGNOSTIDIS K. 2005. Cyanoprocaryota 2. Teil: Oscillatoriales. In: MOESTRUP Ø & CALADO A. Süßwasserflora von Mitteleuropa freshwater flora of central Europa. Berlim: Spektrum Akademischer Verlag, 759 p., 2008KOMÁREK J & ANAGNOSTIDIS K. 2008. Cyanoprocaryota 1. Teil: Chroococcales. In: MOESTRUP Ø & CALADO A. Süßwasserflora von Mitteleuropa freshwater flora of central Europa. Berlim: Spektrum Akademischer Verlag, 548 p.), Komárek (2013)KOMÁREK J. 2013. Cyanoprocaryota 3. Teil: Heterocytous genera. In: Süßwasserflora von Mitteleuropa freshwater flora of central Europe. Berlim: Spektrum Akademischer Verlag, 1748 p. and Bicudo & Menezes (2017)BICUDO C & MENEZES M. 2017. Gêneros de algas de águas continentais do Brasil. 3 ed., Rima, 552 p..

Phytoplankton was classified into Functional Groups- FG (Reynolds et al. 2002REYNOLDS SC, HUSZAR V, KRUK C, NASELLI FLORES L & MELO S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24: 417-428., Padisák et al. 2009PADISÁK J, CROSSETTI LO & NASELLI FLORES L. 2009. Use and misuse in the application of the phytoplankton functional classification: A critical review with updates. Hydrobiologia 621: 1-19.) and the Phytoplankton Community Index- PCI, which is based on phytoplankton density (ind mL-1), Trophic state index (TSI) and dominance of large phytoplankton groups, weighted, which assesses water quality in the following classes: Poor (cyanobacterial dominance or total density > 10000 ind mL-1; chlorophyll- a > 10 µg L-1), Regular (dominance of chlorophytes (Chlorococcales) or total density > 5000 and < 10000 ind mL-1; chlorophyll- a > 10 µg L-1), Good (dominance of chlorophytes (Desmidaceae) or diatoms or total density > 1000 and < 5000 ind mL-1; chlorophyll- a > 4 µg L-1 and < 10 µg L-1) and Excellent (there is no dominance between the groups, total density < 1000 ind mL-1; chlorophyll- a < 4 µg L-1) (CETESB 2019CETESB - COMPANHIA AMBIENTAL DO ESTADO DE SÃO PAULO. 2019. MARTINS MHRB, MENEGON JR, LAMPARELLI MC, MORENO FN, MIDAGLIA CLV & MEDEIROS LA. Qualidade das águas interiores no estado de São Paulo. São Paulo, 284 p.).

The TSI classification for lotic environments was calculated according to Carlson (1977)CARLSON RE. 1977. A trophic state index for lakes. Limnology and Oceanography 22: 361-369., modified by M.C. Lamparelli et al. (unpublished data), using chlorophyll and total phosphorus data, separated into classes: Ultraoligotrophic (≤ 47), Oligotrophic (47 < TSI ≤ 52), Mesotrophic (52 < ETI ≤ 59), Eutrophic (59 < ETI ≤ 63), Supereutrophic (63 < ETI ≤ 67) and Hypereutrophic (> 67).

Statistical analyses

The permutational multivariate analyses of variance (Two-way PERMANOVA) was performed using the Euclidean distance matrix to verify the temporal difference (months and seasonality) and between the tides (ebb and flood) of the physical and chemical parameters of the Guamá River. Two-way analysis of variance (Two-way ANOVA) was performed to verify the variations in density and concentrations of chlorophylls- a, b, and c throughout the seasonal period and tidal cycle. The data were transformed into square roots for all tests, and a significantly lower than 5% (p< 0.05) was considered. For these analyses, software PAST 4.06 was used (Hammer et al. 2001HAMMER O, HARPER DAT & RYAN PD. 2001. Paleontological Statistics Software Package for Education and Data Analysis. Paleontologia Electronica.).

Principal Component Analyses: PCA was applied to verify the distribution pattern of the physical and chemical parameters collected during the period of study. Canonical Redundancy Analyses-RDA was performed to evaluate the relationship between phytoplankton and physical and chemical parameters, considering the abiotic data matrix and the matrix with the density of the most abundant species with the elimination of species with less than 5% abundance (Chorus & Bartram 1999CHORUS I & BARTRAM J. 1999. Toxic cyanobacteria in water: A guide to their public health consequences, monitoring, and management. 1 ed., Routledge, London and New York, 400 p.), the biological matrix was transformed via Hellinger transformation (Legendre & Gallagher 2001LEGENDRE P & GALLAGHER ED. 2001. Ecologically meaningful transformations for ordination of species data. Oecologia 129: 271-280.), for ordering the Euclidean distance from the biological matrix. The abiotic matrices were standardized by ranging, and the PCA and RDA analyses were performed in the CANOCO 4.5 for Windows software (Ter Braak & Smilauer 2002TER BRAAK C & SMILAUER P. 2002. CANOCO Reference manual and CanoDraw for Windows user’s guide: Software for Canonical Community Ordination (version 4.5). Microcomputer Power. https://www.canoco.com. https://edepot.wur.nl/405659 (acessed: May/2022).
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).

RESULTS

Physical and chemical parameters

During the study period, the waters of the Guamá River were considered slightly acidic (6.3 ± 1.0), with an average temperature of 29.4 ± 1.5 °C, an average phosphorus concentration of 0.03 ± 0.039 µg L-1, turbid waters (48.4 ± 41.3 NTU), with low salinity (0.02 ± 0.003 mg L-1) and moderate values of EC (31.4 ± 14.7 mg L-1) and TDS (17.0 ± 9.4 mg L-1) (Table SI - Supplementary Material). There was a seasonal (PERMANOVA F= 4.3; df= 3; p= 0.0001) and monthly (PERMANOVA F= 2.3; df= 11; p= 0.0001) effect on the physical and chemical parameters of the Guamá River, with the distribution pattern of the factors concerning the months of study evidenced in the PCA.

In Axis 1 (PC1) (27.4%) grouped in the positive quadrant all samples from the dry months (July to November) and from the transition from dry to rainy season (December), while in the negative quadrant were grouped those from the rainy months (January to May) and transition from rainy to dry (June). The factors most influenced by seasonality were EC (0.40), TDS (0.50), DO (0.40), winds (0.34) being higher in the dry season, and the real color (-0.33) and rainfall (-0.31), in the rainy season.

In Axis 2 (PC2) (17.7%), the influence of seasonal variation was represented by rainfall (0.50), N-ammoniacal (0.53), and transparency (-0.42) (Figure 2). The effect of tides was observed on turbidity (F= 5.7; DF= 1; p= 0.02) and TSS (F= 8.8; DF= 1; p= 0.004), which were higher during the ebb tides (48 ± 40 NTU and 29.5 ± 19.0 mg L-1, respectively). Turbidity was above the limit allowed by environmental legislation (CONAMA 2005CONAMA - CONSELHO NACIONAL DO MEIO AMBIENTE. 2005. Resolução n 357, 18 de março de 2005. Diário Oficial 053: 58-63.) in September (> 100 NTU).

Figure 2
Principal Component Analyses of the physical and chemical parameters of the Guamá River (Pará, Brazil). Legend: DO: Dissolved Oxygen; EC: Electrical Conductivity; N-Ammon: Ammoniacal Nitrogen; TC: True Color; TP: Total Phosphorus; TDS: Total Dissolved Solids; TSS: Total Suspended Solids.

Biotic variables

A total of 113 species distributed in 62 genera and eight divisions were recorded. The most representative divisions were Bacillariophyta (77 spp.), Cyanobacteria (10 spp.), and Chlorophyta (10 spp.). The minimum density was 2.83 ind mL-1 (March/2021, flood tide), and the maximum density was 110.7 ind mL-1 (December/2019, ebb tide). Significant variations in density occurred between months (F= 3.5; df= 11; p= 0.0006) March presented the lowest density (3.0 ± 0.8 ind mL-1), September and December the highest densities with 61.1 ind mL-1 and 60.2 ind mL-1, respectively. Chlorophyll- a concentration followed the variations in densities but was significantly (p< 0.05) higher in December (21.0 ± 4.7 µg L-1), and the concentration of chlorophyll- c was higher than chlorophyll- b, indicating the dominance of diatoms with more than 80% during the entire study period (Figure 3).

Figure 3
Temporal variation of density (ind mL-1) and phytoplankton biomass (µg L-1) of the Guamá River (Pará, Brazil).

Only 49 species were classified in 21 phytoplankton FG (Table SII), representing 43.4% of the identified species. There was no visualization of seasonality in the FG, as the P group dominated in all months (Figure 4); this FG groups the species of Aulacoseira, abundant throughout the study period.

Figure 4
Temporal variation of the density of the Functional Groups-FG of the phytoplankton (ind mL-1) of the Guamá River (Pará, Brazil).

The phytoplankton community índex: PCI allowed the classification of the water quality of the Guamá River, ranging from excellent (rainy months) to good (less rainy) in terms of environmental quality, during the two years of investigation. Evaluating the three criteria addressed, following considerations were made: low density, diatoms invariably dominate the environment, and the TSI ranges from ultraoligotrophic (March) to mesotrophic (September).

The RDA performed 19.4% of the species variation concerning physical and chemical parameters. Axis 1 (7.0%) showed N-ammoniacal (-0.57) as the main factor influencing part of the rainy and less rainy months, especially March, October, and December. It favored the non-specific group Aulacoseira spp., and Actinocyclus normanii (Gregory) Hustedt. Contrary to the species Coscinodiscus rothii (Ehrenberg) Grunow and Polymyxus coronalis L. W. Bailey that were in opposite influence to N- ammoniacal being dominant in the dry period and under the direct result of estuarine waters.

In axis 2 (8.3%), the estuarine influence was also present, where the species Coscinodiscus spp. were associated with high TSS (0.48), unlike the freshwater species Thalassiosira oestrupii (Ostenfeld) Hasle and Scenedesmus sp., which were associated with more transparent waters and higher true color in the months of June and May (Figure 5).

Figure 5
Redundancy Analyses (RDA) showing the temporal variation of the relationships between phytoplankton and physical and chemical parameters in the Guamá River (Pará, Brazil). Legend: Acno- Actinocyclus normanii, Acsp- Actinoptychus splendens., Acti- Actinocyclus sp., Ausp- Aulacoseira spp., Augr- Aulacoseira granulata, Coscr-Coscinodiscus rothii, Coscp- Coscinodiscus spp., Cyst-Cyclotella striata, Cyclo- Cyclotella stylorum, Cycls- Cyclotella sp., Cymas- Cymatosira sp., Pasu- Paralia sulcata, Poly- Polymyxus coronalis, Scens- Scenedesmus sp., Thalp-Thalassiosira spp., Thoe- Thalassiosira oestrupii; N-Ammon: Ammoniacal Nitrogen; TC: True Color; TSS: Total Suspended Solids.

DISCUSSION

The seasonal behavior of physical and chemical parameters evidenced that in the Axis 1 of PCA is characteristic of the Guamá River and was also observed by Paiva et al. (2006)PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146. and Alencar et al. (2019)ALENCAR VESA, ROCHA EJP, SOUZA JÚNIOR JA & CARNEIRO BS. 2019. Análise de parâmetros de qualidade da água em decorrência de efeitos da precipitação na baia de Guajará – Belém– PA. Revista Brasileira de Geografia e Física 12: 661-680. in this river and by Gomes et al. (2021)GOMES AL, CUNHA CJS, LIMA MO, SOUSA EB, COSTA TAVARES VB & MARTINELLI LEMOS JM. 2021. Biodiversity and interannual variation of cyanobacteria density in an estuary of the brazilian Amazon. An Acad Bras Cienc 93: 1-12. in the Pará River which is connected to the study area. Rocha Neto et al. (2017), studying the Guamá River, did not identify a significant effect of seasonality on the physical and chemical parameters but cited the increase in salinity, EC, nitrate, and silicate during the less rainy months, coinciding with the present study.

Varela et al. (2020)VARELA AWP, SOUZA AJN, AVIZ MD, PINFILDI GV, SANTOS RM, SOUSA PHC & SANTOS MLS. 2020. Qualidade da água e Índice de Estado Trófico no Rio Guamá, município de Belém (Pará, Brasil). Revista Gestão & Sustentabilidade 9: 695-715. also did not identify a significant effect of seasonality on the physical and chemical parameters of the Guamá River but showed higher pH, TSS, turbidity, and total phosphorus fluctuations in the less rainy months.

The presence of N- ammoniacal can be associated with natural sources of vegetal decomposition, since the river is bordered, but also, evidence the occurrence of anthropogenic influence in the river due to its association with the freshly dumped organic matter, usually containing nitrogenous excreta and industrial effluents (Souza Filho et al. 2020VARKITZI I ET AL. 2018. Pelagic habitats in the Mediterranean Sea: A review of Good Environmental Status (GES) determination for plankton components and identification of gaps and priority needs to improve coherence for the MSFD implementation. Ecol Indic 95: 203-218., Dey et al. 2021DEY S, HARIPAVAN N, BASHA SR & BABU GV. 2021. Removal of ammonia and nitrates from contaminated water by using solid waste bio-adsorbents. Current Research in Chemical Biology 1: 100005.); however, its relationship with the intensity of rainfall is associated with the runoff provided by the rainy season, which contributes to the increase of this compound in water bodies. Although, the concentrations of N- ammoniacal did not exceed the limits tolerated by the legislation (CONAMA 2005CONAMA - CONSELHO NACIONAL DO MEIO AMBIENTE. 2005. Resolução n 357, 18 de março de 2005. Diário Oficial 053: 58-63.).

Regarding the high turbidity and the TSS during the ebb tide, can be associated with the fact that the region does not have adequate sanitation coverage, where urban drainage channels, considered “open sewers” cross the entire city of Belém and that during the ebb tide are dumped in the Guajará Bay and Guamá River. Drainage channels have considerable concentrations of organic and inorganic pollutants (Cavalcante et al. 2007CAVALCANTE LM, CRUZ FM & LIMA WN. 2007. Avaliação De Impactos Ambientais Em Microbacias Da Região Metropolitana De Belém (Pa). XVII Simpósio Brasileiro de Recursos Hídricos 1-7.), contributing to greater turbidity and suspended solids concentrations.

The estuarine influence on the Guamá River comes from the Pará River estuary, which receives oceanic discharges that are stronger during the rainy season, leaving the waters with salinity ranging from 0.5 g kg to 1.6 g kg (Bezerra et al. 2011BEZERRA MO, MEDEIROS C, KRELLING APM, ROSÁRIO RP & ROLLNIC M. 2011. Physical oceanographic behavior at the Guama/Acara-Moju and the Paracauari river mouths, Amazon Coast (Brazil). J Coast Res 64: 1448-1462.) such discharges are capable of entering the tributaries of this estuary, reaching up to 120 km from the mouth of this river to the city of Belém (R.P. Rosário et al. unpublished data, Rosário et al. 2009ROSÁRIO RP, BEZERRA MO & VINZÓN SB. 2009. Dynamics of the saline front in the northern channel of the Amazon River - influence of fluvial flow and tidal range (Brazil). J Coast Res SI56: 1414-1418.).

This oceanic influence also acts on the tidal regimes at the mouth of the Guamá River, which is reflected in the composition of phytoplankton species, since it is formed mainly by marine diatoms (Paiva et al. 2006PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146.), which predominate in estuarine environments (Moser et al. 2002MOSER GAO, GIANESELLA SMF, CATTENA CO, DAVID CJ, BARRERA ALBA JJ, SALDANHA CORRÊA FMP & BRAGA ES. 2002. Influência das Marés sobre o Fitoplâncton no Sistema Estuarino de São Vicente e Santos. Instituto Oceanográfico- USP 1-5., Paiva et al. 2006PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146., Leão et al. 2008LEÃO BM, PASSAVANTE JZO, SILVA CUNHA MGG & SANTIAGO MF. 2008. Ecologia do microfitoplâncton do estuário do rio Igarassu, PE, Brasil. Acta Bot Bras 22: 711-722., Monteiro et al. 2009MONTEIRO MDR, MELO NFAC, ALVES MAMS & PAIVA RS. 2009. Composição e distribuição do microfitoplâncton do rio Guamá no trecho entre Belém e São Miguel do Guamá, Pará, Brasil Composition and distribution of the microphytoplankton from Guamá River between Belém and São Miguel do Guamá, Pará, Brazil. Bol Mus Par Emílio Goeldi Ciênc Nat 4: 341-351., Sousa et al. 2009SOUSA EB, COSTA VB, CARNEIRO L & PEREIRA C. 2009. Variação temporal do fitoplâncton e dos parâmetros hidrológicos da zona de arrebentação da Ilha Canela (Bragança, Pará, Brasil). Acta Bot Bras 23: 1084-1095., Vilhena et al. 2014VILHENA MPSP, COSTA ML, BERRÊDO JF, PAIVA RS & ALMEIDA PD. 2014. Chemical composition of phytoplankton from the estuaries of Eastern Amazonia. Acta Amazonica 44: 513-526., Reis et al. 2020REIS FN, BELÚCIO LF, PAMPLONA FC, REIS LTL, VEIGA GD & MELO NFAC. 2020. Microphytoplankton dynamics in Curuperé Estuary at the amazonian mangrove ecosystem. Bol Inst Pesca 46: 1-15., Cereja et al. 2021CEREJA R, BROTAS V, CRUZ JPC, ROSRIGUES M & BRITO AC. 2021. Tidal and physicochemical effects on phytoplankton community variability at Tagus Estuary (Portugal). Front Mar Sci 8: 1-21., Sá et al. 2022SÁ AKDS, FEITOSA FAN, CUTRIM MVJ, FLORES MONTES MJ, COSTA DS & CAVALCANTI LF. 2022. Phytoplankton community dynamics in response to seawater intrusion in a tropical macrotidal river estuary continuum. Hydrobiologia 1-33.). Amazonian white-water rivers (Sioli & Klinge 1962SIOLI H & KLINGE H. 1962. Solos, Tipos de Vegetação e Águas na Amazônia. Bol Mus Para Emílio Goeldi 1: 1-18.) have low density, and diatoms are the leading phytoplankton group (Sousa et al. 2013SOUSA EB, GOMES AL, CUNHA CJS, FAIAL KCF & COSTA VB. 2013. Dinâmica Sazonal do Fitoplâncton do Parque Estadual do Charapucu (Afuá, Arquipélago do Marajó, Pará, Brasil). Biota Amazônia 5: 34-41.).

In the aquatic environment, suspended particles of organic or inorganic material can attenuate the penetration of light. Diatoms have different pigment compositions from other phytoplankton groups because, in addition to chlorophyll- a they have chlorophyll- c and carotenoids such as β- carotene and fucoxanthins, which gives them more significant advantages over other algae in environments with less light incidence, since the accessory chlorophyll- c works mainly in the absorption of attenuated light (blue light). Furthermore, this type of light significantly impacts diatoms, producing more cells with higher photosynthetic activity than direct (white) sunlight (Kuczynska et al. 2015KUCZYNSKA P, JEMIOLA-RZEMINSKA M & STRZALKA K. 2015. Photosynthetic Pigments in Diatoms. Mar Drugs 13: 5847-5881.). Freshwater environments rich in N- ammoniacal, such as the Guamá River, confer advantages on diatoms since they act directly in the cycling of nitrogen compounds, which are essential for their growth and development (Allen et al. 2011ALLEN AE ET AL. 2011. Evolution and metabolic significance of the urea cycle in photosynthetic diatoms. Nature 473: 203-207.).

The variation in phytoplankton density in the Guamá River followed a seasonal pattern, with the lowest values occurring in the rainier months. Several studies point to lower phytoplankton concentration in rivers (Paiva et al. 2006PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146., Sousa et al. 2013SOUSA EB, GOMES AL, CUNHA CJS, FAIAL KCF & COSTA VB. 2013. Dinâmica Sazonal do Fitoplâncton do Parque Estadual do Charapucu (Afuá, Arquipélago do Marajó, Pará, Brasil). Biota Amazônia 5: 34-41., Rocha Neto et al. 2017, Wang et al. 2021WANG C, JIA H, WEI J, YANG W, GAO Y, LIU Q, GE D & WU N. 2021. Phytoplankton functional groups as ecological indicators in a subtropical estuarine river delta system. Ecol Indic 126: 1-9.) and reservoirs (Costa et al. 2010COSTA VB, SOUZA LR, SENA BA, COSTA SD, BEZERRA MFC & NAKAYAMA L. 2010. Microfitoplâncton do Lago Água Preta, Parque Ambiental de Belém (Pará, Brasil). Período mais chuvoso. Uakari 6: 75-86., Rodrigues et al. 2018RODRIGUES LC, PIVATO BM, VIEIRA LCG, BOVO-SCOMPARIN VM, BORTOLINI J C, PINEDA A & TRAIN S. 2018. Use of phytoplankton functional groups as a model of spatial and temporal patterns in reservoirs: a case study in a reservoir of central Brazil. Hydrobiologia 805: 147-161.) in the rainiest periods, since the interaction of rain and suspended solids in this period causes the attenuation of light in the aquatic environment (Sousa et al. 2020SOUSA EB, PINTO SLS, GOMES AL, CUNHA CJS, COSTA TAVARES VB & PINHEIRO SCC. 2020. Composition, richness and ecological index of phytoplankton of lake Bolonha (Belém, Pará). Brazilian Journal of Animal and Environmental Research 3: 3263-3275.), and therefore, interferes with the development of phytoplanktonic organisms, since they are entirely dependent on the availability of light (Stumpner et al. 2020STUMPNER EB ET AL. 2020. Spatial variability of phytoplankton in a shallow tidal freshwater system reveals complex controls on abundance and community structure. Sci Total Environ 700: 134392.).

Despite the low inclusion in functional groups of the species found in Brazilian rivers, especially the Amazon ones, the functional groups in this study were relatively successful, as they encompassed the species with higher densities, which are classified in the P group, which grouped the genus Aulacoseira, establishing itself as a promising approach for the Guamá River, since all species sufficiently counted (Chorus & Bartram 1999CHORUS I & BARTRAM J. 1999. Toxic cyanobacteria in water: A guide to their public health consequences, monitoring, and management. 1 ed., Routledge, London and New York, 400 p.) were included in the FG.

In addition, the number of functional groups found is consistent with other river studies (Wang et al. 2021WANG C, JIA H, WEI J, YANG W, GAO Y, LIU Q, GE D & WU N. 2021. Phytoplankton functional groups as ecological indicators in a subtropical estuarine river delta system. Ecol Indic 126: 1-9.). However, attention is drawn to a widespread species in the waters of the Guamá River, abundant from September to December, which was Polymyxus coronalis, but still does not have a classification into functional groups. In this case, further studies are suggested in the region to fit this species into FG.

In this criterion, the functional group P includes species that inhabit the eutrophic epilimnion that tolerates soft light and carbon-deficient water but are sensitive to stratification and silica depletion (Reynolds et al. 2002REYNOLDS SC, HUSZAR V, KRUK C, NASELLI FLORES L & MELO S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24: 417-428.). Reflecting the main characteristics present in the Guamá River environment, such as, turbid waters and high silicate presence (Santos et al. 2014SANTOS MLS, HOLANDA P, PEREIRA I, RODRIGUES S, PEREIRA JAR & MESQUITA K. 2014. Influência das Condições da Maré na Qualidade de Água do Rio Guamá e Baia do Guajará. Boletim Técnico Científico do CEPNOR 14: 17-25.), essential for developing diatoms, which need this component to form their frustules.

Regarding the PCI, the strong presence of diatoms and the relatively low densities consider the Guamá River to be a good quality environment. In this context, when compared to other studies in Brazilian rivers, the phytoplankton density of the Guamá River is very low (Soares et al. 2007SOARES MCS, HUSZAR VLM & ROLAND F. 2007. Phytoplankton dynamics in two tropical rivers with different degrees of human impact (Southeast Brazil). River Res Appl 23: 698-714., Leão et al. 2008LEÃO BM, PASSAVANTE JZO, SILVA CUNHA MGG & SANTIAGO MF. 2008. Ecologia do microfitoplâncton do estuário do rio Igarassu, PE, Brasil. Acta Bot Bras 22: 711-722., Sousa et al. 2009SOUSA EB, COSTA VB, CARNEIRO L & PEREIRA C. 2009. Variação temporal do fitoplâncton e dos parâmetros hidrológicos da zona de arrebentação da Ilha Canela (Bragança, Pará, Brasil). Acta Bot Bras 23: 1084-1095., 2013), since the conditions present in the environment act as species selectors and influence the phytoplankton population dynamics.

The Guamá River has a very striking feature, its high turbidity, which directly interferes with the phytoplankton community, preventing species sensitive to low light from prevailing (Stumpner et al. 2020STUMPNER EB ET AL. 2020. Spatial variability of phytoplankton in a shallow tidal freshwater system reveals complex controls on abundance and community structure. Sci Total Environ 700: 134392.); in this way, diatoms can dominate this environment to tolerate the lowest light incidence (Reynolds et al. 2002REYNOLDS SC, HUSZAR V, KRUK C, NASELLI FLORES L & MELO S. 2002. Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24: 417-428., Kruk & Segura 2012KRUK C & SEGURA AM. 2012. The habitat template of phytoplankton morphology-based functional groups. Hydrobiologia 698: 191-202.). In addition, the estuarine influence also acts on the environmental composition since a large part of the composition is estuarine organisms (Paiva et al. 2006PAIVA RS, ESKINAZI LEÇA E, PASSAVANTE JZO, SILVA CUNHA MGG & MELO NF AC. 2006. Considerações ecológicas sobre o fitoplâncton (Pará, da baía do Guajará e foz do rio Guamá (Pará, Brasil). Bol Mus Para Emílio Goeldi 1: 133-146.).

On the other hand, the dominance of diatoms does not always characterize the environment as good; for example, the most frequent species in the Guamá River, such as Aulacoseira granulata (Ehrenberg) Simonsen, wich despite being cosmopolitan occurs preferentially in eutrophicated environment ( Bicudo et al. 2016BICUDO DC ET AL. 2016. Ecology and distribution of Aulacoseira species (Bacillariophyta) in tropical reservoirs from Brazil. Diatom Res 31: 199-215., Wang et al. 2021WANG C, JIA H, WEI J, YANG W, GAO Y, LIU Q, GE D & WU N. 2021. Phytoplankton functional groups as ecological indicators in a subtropical estuarine river delta system. Ecol Indic 126: 1-9.), and in this way, the use of phytoplankton divisions in a generalized way by the PCI supposes a fragility of the index, since it does not take into account the specificities of the species or combined phytoplankton assemblages.

In this way, this approach becomes better usable in terms of detecting algal blooms that are generally known to be present in eutrophic environments, such as cyanobacteria (Oliver et al. 2020OLIVER SL, IKEFUTI PV & RIBEIRO H. 2020. Cyanobacteria bloom variations and atmospheric variables, an environmental health contribution. Ambiente & Água 15: 11.) and euglenophytes (Lopez et al. 2008LOPEZ CB, JEWETT EB, DORTCH Q, WALTON BT & HUDNELL HK. 2008. Scientific Assessment of Freshwater Harmful Algal Blooms. Interagency Working Group on Harmful Algal Blooms, Hypoxia, and Human Health of the Joint Subcommittee on Ocean Science and Technology. Washington, DC.), when used in the generalization of groups of diatoms and chlorophytes, analyses of the species present in the environment and their relationship with the trophic state is necessary.

Regarding the TSI, results contrary to studies performed in the region are described since Santos et al. (2014)SANTOS MLS, HOLANDA P, PEREIRA I, RODRIGUES S, PEREIRA JAR & MESQUITA K. 2014. Influência das Condições da Maré na Qualidade de Água do Rio Guamá e Baia do Guajará. Boletim Técnico Científico do CEPNOR 14: 17-25. and Varela et al. (2020)VARELA AWP, SOUZA AJN, AVIZ MD, PINFILDI GV, SANTOS RM, SOUSA PHC & SANTOS MLS. 2020. Qualidade da água e Índice de Estado Trófico no Rio Guamá, município de Belém (Pará, Brasil). Revista Gestão & Sustentabilidade 9: 695-715. show the variation in the trophic state of the Guamá River, ranging from mesotrophic to supereutrophic. This is probably due to the sampling stations of these studies, which are closer to the city’s drainage channels and dumped adjacent to Guajará Bay. In the present work, the water samples were collected close to the mouth of the Guamá River, with less influence on the sewage discharge the water body receives.

Analyzing the chemical variation of the most impacted drainage channels of the metropolitan region of Belém Cavalcante et al. (2007)CAVALCANTE LM, CRUZ FM & LIMA WN. 2007. Avaliação De Impactos Ambientais Em Microbacias Da Região Metropolitana De Belém (Pa). XVII Simpósio Brasileiro de Recursos Hídricos 1-7. concluded that, although these channels are polluted in the Guajarino estuary and Guamá River, these pollutants are dissipated due to the abundant rainfall and the semi-diurnal tidal dynamics. It is believed that this dissipation effect was felt at the collection point of the present study, hence the discrepant values when compared to other studies in the region. However, the increasing urbanization and waste production dumped in the watersheds can generate unmitigated harmful effects in the Amazon estuaries (Cavalcante et al. 2007CAVALCANTE LM, CRUZ FM & LIMA WN. 2007. Avaliação De Impactos Ambientais Em Microbacias Da Região Metropolitana De Belém (Pa). XVII Simpósio Brasileiro de Recursos Hídricos 1-7.).

The low percentage of explanation of the RDA was possibly due to the dominance of few species in the region from the estuarine waters of the Amazon River and Pará River that influence the Guamá River, mainly in the less rainy period, through the Estreito de Breves (Gregório & Mendes 2009GREGÓRIO AMS & MENDES AC. 2009. Batimetria e sedimentologia da Baía de Guajará, Belém, Estado do Pará, Brasil. Amazônia: Ciência & Desenvolvimento 5: 53-72.). On the other hand, the most notable species are diatoms, which require considerable concentrations of silicate from the environment to form their frustules. However, this factor was not analyzed in the present study, leaving a suggestion for future investigations since, during the two years of study, these microalgae composed more than 80% of the entire composition in all months. Thus, possibly the association of Coscinodiscus spp. They occurred with the silica present in the TSS components, as verified in the RDA.

In this scenario, we understand that N- ammoniacal marks the anthropic influence on the Guamá River, as its presence suggests recent contamination by organic matter, probably domestic sewage, which drastically reduced the density in March, when N- ammoniacal occurred with the highest concentration (0.5 ± 0.1 mg L-1) and low DO values (2.7 ± 1.4 mg L-1), below the limit established by environmental legislation (CONAMA 2005CONAMA - CONSELHO NACIONAL DO MEIO AMBIENTE. 2005. Resolução n 357, 18 de março de 2005. Diário Oficial 053: 58-63.), suggesting the presence of aerobic bacteria degrading organic matter. In this aspect, the DO was low (< 5.0 mg L-1) throughout the rainy season.

Vilhena et al. (2014)VILHENA MPSP, COSTA ML, BERRÊDO JF, PAIVA RS & ALMEIDA PD. 2014. Chemical composition of phytoplankton from the estuaries of Eastern Amazonia. Acta Amazonica 44: 513-526. found that 85% of the phytoplankton composition of the Pará and Mocajuba Rivers (Pará), near the Guamá River, constituted by diatoms and suggested that these algae are efficient in concentrating metals, mainly A. granulata, P. coronalis and A. normanii, in which high levels of Al, Fe, K, Ca and P were found, so it is suggested that future studies include these metals to verify the correlation with the abundance of these species.

CONCLUSION

The Guamá River phytoplankton presented seasonal dynamics mainly influenced by N- ammoniacal, transparency, and TSS. The Pará River influences the Guamá River’s phytoplankton through the intrusion of estuarine waters and, with them, estuarine and marine diatom species. The use of Functional Groups proved to be a promising tool in the determination of water quality since it covered the most abundant species in the environment, recommending that there be more studies to insert the species Polymyxus coronalis among the functional groups, better to understand the role of this species in the environment of the Guamá River. The PCI classified the waters ranging from good to great, but it is inadequate to characterize Amazonian white-waters, which have diatoms as the leading dominant group.

Through the trophic índex (TSI) the waters of Guamá River can be classified as oligo to mesotrophic, corroborating the results observed in the PCI. It is suggested that future works include the analyses of silica and metals in the water to understand the dynamics of diatoms in Amazonian rivers.

ACKNOWLEDGMENTS

The authors express their gratitude to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), CDP/IEC/FADESP (Covenant N°01/2017), Universidade Federal Rural da Amazônia and Instituto Evandro Chagas for funding the work and providing laboratory support for the research.

SUPPLEMENTARY MATERIAL

Tables SI-SII.

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Publication Dates

  • Publication in this collection
    08 Apr 2024
  • Date of issue
    2024

History

  • Received
    09 May 2022
  • Accepted
    06 July 2023
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