Structure of microphytoplankton community and environmental variables in a macrotidal estuarine complex, São Marcos Bay, Maranhão - Brazil

Cavalcanti, Lisana Furtado; Azevedo-Cutrim, Andrea Christina Gomes; Oliveira, Amanda Lorena Lima; Furtado, Jordana Adorno; Araújo, Bethânia de Oliveira; Sá, Ana Karoline Duarte-dos-Santos; Ferreira, Francinara Santos; Santos, Nágela Gardênia Rodrigues; Dias, Francisco José Silva; Cutrim, Marco Valério Jansen

doi:10.1590/S1679-87592018021906603

person Lisana Furtado Cavalcanti

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Andrea Christina Gomes Azevedo-Cutrim

schoolDepartamento de Química e Biologia da Universidade Estadual do Maranhão (Cidade Universitária Paulo VI, Av. Lourenço Vieira da Silva, nº 1000 - Jardim São Cristovão - 65055-310 - São Luís - MA - Brazil)

person Amanda Lorena Lima Oliveira

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Jordana Adorno Furtado

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Bethânia de Oliveira Araújo

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Ana Karoline Duarte-dos-Santos Sá

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Francinara Santos Ferreira

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Nágela Gardênia Rodrigues Santos

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Francisco José Silva Dias

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

person Marco Valério Jansen Cutrim *

schoolDepartamento de Oceanografia e Limnologia da Universidade Federal do Maranhão (Av. dos Portugueses, 1966 - Bacanga - 65080-805 - São Luís - MA Brazil)

0000-0002-7442-2121

person*Corresponding author:
emailcutrim@ufma.br

Hydrological Variables	Rainy				Dry
	Flood		Ebb		Flood		Ebb
	Mean ± SD	Min/Max	Mean ± SD	Min/Max	Mean ± SD	Min/Max	Mean ± SD	Min/Max
Temperature (ºC)	29.45±0.61	28.56/30.24	29.42±0.46	28.72/30.0	28.74±0.19	28.4/29.04	28.92±0.25	28.6/29.4
Salinity	28.91±4.05	20.7/34.78	29.45±3.95	21.09/34.8	35.40±1.81	31.76/37.3	35.63±1.85	32.07/37.4
Dissolved Oxygen (ml L^-1)	3.55±0.37	3.08/4.5	3.69±0.28	3.4/4.16	5.42±0.68	4.5/6.3	5.65±0.68	4.7/6.5
Oxygen Saturation (%)	47.33±5.03	40/60	48.58±4.10	40/55	71.25±9.07	59/83	74.38±9.02	62/86
Secchi depth (cm)	35±13	6/50	43±23	8/77	42±9	27/56	36±15	22/72
Turbidity (NTU)	91.29±101.35	32/390	74.08±51.85	14.8/190	102.22±67.11	62.1/260	72.50±37.57	29.9/130
pH	7.66±0.44	6.7/8.15	7.7±0.35	7.0/8.11	7.52±0.18	7.3/7.8	7.69±0.13	7.43/7.8
NH₄⁺ (µmol L^-1)	0.33±0.17	0.07/0.61	0.31±0.12	0.17/0.61	0.50±0.30	0.15/0.98	0.16±0.06	0.09/0.25
NO₂^- (µmol L^-1)	0.10±0.03	0.06/0.16	0.11±0.05	0.05/0.26	0.33±0.74	0.03/2.16	0.11±0.06	0.06/0.26
NO₃^- (µmol L^-1)	1.16±0.05	1.08/1.24	1.06±0.35	0.13/1.35	1.19±0,05	1.10/1.27	1.23±0.04	1.13/1.29
PO₄^-3 (µmol L^-1)	1.32±0.11	0.03/0.46	0.23±0.04	0.17/0.33	0.23±0.10	0.03/0.34	0.25±0.04	0.17/0.33

Taxonomy Category	TO (%)	CI	Occurence by season
Taxonomy Category	TO (%)	CI	Dry	Rainy
Cyanobacteria
Oscillatoria spp.	53	R	*	*
Spirulina sp.	3	A		*
Euglenophyta
Euglena sp.	3	A		*
Miozoa
Ceratium sp.	5	A	*	*
Peridinium sp.	8	A	*	*
Prorocentrum sp.	5	A		*
Protoperidinium conicum	13	A	*	*
Protoperidinium spp.	40	V	*	*
Pyrophacus steinii	10	A	*	*
Tripos furca	20	A	*	*
T. fusus	5	A		*
T. lineatus	33	V	*	*
T. macroceros	3	A		*
Bacillariophyta
Achnanthes brevipes	3	A	*
Actinocyclus curvatulus	3	A		*
Actinocyclus sp.	3	A	*
Actinoptychus annulatus	85	R	*	*
A. aster	5	A		*
A. minutus	5	A		*
A. octonarius	10	A	*	*
A. senarius	78	R	*	*
A. splendens	60	R	*	*
A. vulgaris	10	A		*
Actinoptychus sp.	10	A	*	*
Alveus marinus	3	A	*
Amphora sp.	3	A		*
Asterionellopsis glacialis	58	R	*	*
Asteromphalus sp.	3	A	*
Aulacodiscus margaritaceus	3	A	*
Bacillaria paxillifera	63	R	*	*
Bacteriastrum delicatulum	35	V	*	*
B. hyalinum	45	V	*	*
Bellerochea malleus	80	R	*	*
Biddulphia biddulphiana	3	A	*
B. tridens	8	A	*	*
Caloneis permagna	38	V	*	*
Cerataulina sp.	3	A	*
Chaetoceros aequatorialis	15	A	*	*
C. affinis	38	V	*	*
C. atlanticus	3	A		*
C. atlanticus f. audax	10	A	*	*
C. brevis	5	A		*
C. coarctatus	8	A	*	*
C. compressus	15	A	*	*
C. curvisetus	13	A	*	*
C. didymus	5	A		*
C. gracilis	8	A	*
C. lorenzianus	40	V	*	*
C. pendulus	20	A	*	*
C. peruvianus	55	R	*	*
C. simplex	25	V	*	*
C. subtilis	3	A		*
C. subtilis var. abnormis	53	R	*	*
C. teres	5	A		*
Chaetoceros sp.	5	A		*
Coscinodiscopsis jonesiana	3	A	*
Coscinodiscus asteromphalus	40	V	*	*
C. centralis	70	R	*	*
C. concinnus	23	A	*	*
C. curvatulus	3	A		*
C. gigas	33	V	*	*
C. granii	15	A	*	*
C. oculus-iridis	98	R	*	*
C. radiatus	85	R	*	*
C. rothii	60	R	*	*
Coscinodiscus sp.	28	V	*	*
Craticula cuspidata	8	A	*	*
Cyclotella meneghiniana	10	A	*	*
C. striata	43	V	*	*
C. stylorum	60	R	*	*
Cylindrotheca closterium	23	A	*	*
Diploneis bombus	20	A	*	*
D. gruendleri	30	V	*	*
D. interrupta	5	A	*
D. weissflogii	13	A	*	*
Ditylum brightwellii	98	R	*	*
Entomoneis alata	35	V	*	*
Entomoneis sp.	3	A	*
Eupodiscus antiquus	18	A	*	*
E. radiatus	10	A		*
Eupodiscus sp.	3	A	*
Fragilaria sp.	8	A	*
Frustulia interposita	33	V	*	*
F. rhomboides	15	A	*	*
Grammatophora marina	5	A	*
G. oceanica	5	A	*	*
Guinardia flaccida	13	A	*	*
Gyrosigma attenuatum	10	A		*
G. balticum	83	R	*	*
G. hippocampus	13	A	*	*
Gyrosigma sp.	3	A		*
Hantzschia amphioxys	3	A		*
Helicotheca tamesis	88	R	*	*
Hemiaulus indicus	3	A		*
Leptocylindrus danicus	18	A	*	*
L. minimus	3	A		*
Lithodesmium undulatum	88	R	*	*
Lyrella lyra	3	A	*
Melchersiela hexagonalis	50	V	*	*
Melosira moniliformis	23	A	*	*
M. nummuloides	73	R	*	*
Navicula sp.	13	A	*	*
Neocalyptrella robusta	10	A		*
Nitzschia fasciculata	23	A	*	*
N. longa	18	A	*	*
N. longissima	20	A	*	*
N. longissima f. parva	3	A	*
N. obtusa	5	A		*
N. obtusa var. scalpelliformis	85	R	*	*
N. palea	8	A	*	*
N. sigma	48	V	*	*
N. tryblionella	5	A	*	*
Nitzschia sp.	18	A	*	*
Odontella aurita	55	R	*	*
O. longicruris	60	R	*	*
O. turgida	15	A	*	*
Odontella spp.	23	A	*	*
Paralia sulcata	60	R	*	*
Petroneis humerosa	13	A	*	*
Pleurosigma angulatum	10	A	*	*
P. formosum	3	A	*
P. normanii	8	A	*	*
Pleurosigma spp.	50	V	*	*
Pleurosira laevis	3	A	*
Podocystis adriatica	3	A	*
Proboscia alata	3	A		*
Psammodictyon constrictum	8	A	*	*
P. panduriforme	8	A	*	*
Pseudo-nitzschia pungens	30	V	*	*
Pseudo-nitzschia spp.	28	V	*
Pseudosolenia calcar-avis	10	A	*	*
Rhaphoneis amphiceros	50	V	*	*
Rhizosolenia hebetata	8	A	*	*
R. imbricata	8	A		*
R. imbricata var. shrubsolei	3	A		*
R. setigera	70	R	*	*
R. styliformis	5	A		*
Skeletonema costatum	68	R	*	*
S. tropicum	75	R	*	*
Surirella fastuosa	5	A	*	*
S. febigeri	45	V	*	*
S. gemma	25	V	*	*
S. minuta	3	A	*
Synedra ulna	30	V	*	*
S. ulna var. ulna	28	V	*	*
Synedra sp.	20	V	*	*
Tabularia fasciculata	45	V	*	*
Terpsinoe americana	8	A	*	*
T. musica	30	V	*	*
Thalassionema frauenfeldii	100	R	*	*
T. nitzschioides	35	V	*	*
T. nitzschioides var. capitulatum	5	A	*	*
T. nitzschioides var. claviforme	3	A		*
T.nitzschioides var. lanceolatum	3	A		*
Thalassionema sp.	20	A		*
Thalassiosira eccentrica	80	R	*	*
T. leptopus	85	R	*	*
T. lineata	13	A	*	*
T. rotula	13	A	*	*
T. simonsenii	3	A		*
T. subtilis	98	R	*	*
Thalassiosira sp.	38	V	*	*
Triceratium dubium	3	A	*
T. favus	90	R	*	*
T. favus f. quadrata	48	V	*	*
T. pentacrinus	3	A		*
T. robertsianum	5	A		*
Triceratium sp.	15	A	*	*
Trieres mobiliensis	100	R	*	*
T. regia	100	R	*	*
T. sinensis	60	R	*	*
Tryblionella angustata	3	A	*
Tryblioptychus cocconeiformis	23	A	*	*
Zygoceros ehrenbergii	93	R	*	*
Chlorophyta
Oedogonium sp.	3	A		*
Dimorphococcus sp.	33	V	*	*
Scenedesmus sp.	5	A		*
Charophyta
Staurastrum sp.	3	A		*

s

	Rainy							Dry
Species	apr./10		jan./11		mar./11			aug./10		nov./10
Species	F	E	F	E	F	E	Y	F	E	F	E	Y	∑
Nitzschia sp.	99530	17525	13289	60390	46312	4039	0.162	27297	15853	16902	16591	0.064	3.2 x 10⁵
Synedra sp.	32144	5708	9874	18512	58561	6381	0.068	11780	4039	4258	15791	0.022	1.6 x 10⁵
Diploneis weissflogii	4376	4011	3725	20167	31379	7742	0.044	34736	22753	13046	14768	0.062	1.6 x 10⁵
Thalassiosira sp.	4376	6017	5862	16661	15180	7405	0.030	2188	2188	5890	0	0.003	6.6 x 10⁴
Cyclotella stylorum	14002	3702	4011	5862	4012	6045	0.020	2188	0	4193	2188	0.002	4.6 x 10⁴
Thalassiosira leptopus	0	0	10028	10757	4011	4039	0.014	4813	6564	4376	0	0.004	4.5 x 10⁴
Coscinodiscus sp.	9626	18543	4011	18822	9626	6381	0.014	4376	6227	0	2188	0.004	7.9 x 10⁴
Eupodiscus radiatus	0	2006	0	2006	19253	1851	0.003	12218	4376	0	8751	0.008	5.0 x 10⁴

Taxa	Av. dissim	Contrib. %	Cumulative %	Mean abund. 1	Mean abund. 2
Nitszchia sp.	14.16	29.12	29.12	4.02E+04	1.92E+04
Diploneis weissflogii	8.981	18.47	47.59	1.19E+04	2.13E+04
Synedra sp.	7.764	15.97	63.56	2.19E+04	8.97E+03
Coscinodiscus sp.	5.053	10	73.95	1.12E+04	3.20E+03
Eupodiscus radiatus	3.946	8.117	82.07	4.19E+03	6.34E+03
Thalassiosira sp.	3.707	7.625	89.69	9.25E+03	2.57E+03
Thalassiosira leptopus	2.644	5.437	95.13	4.81E+03	3.94E+03
Cyclotella stylorum	2.368	5	100	6.27E+03	2.14E+03

	Prec.	T ºC	Sal.	pH	Secchi	Turb.	DO	NH₄⁺	NO₂^-	PO₄^-3	NO₃^-	Micro	Nano	Chl-a	Abund.	Wind	Nitzs.	Syned.	Dipl.
Prec.
T ºC	0.32
Sal.	-0.52	-0.84
pH	0.40	-0.49	0.24
Secchi	0.06	-0.34	0.40	0.20
Turb.	-0.13	0.25	-0.30	-0.39	-0.58
DO	-0.81	-0.53	0.62	-0.11	0.07	0.04
NH₄⁺	0.02	-0.13	0.06	0.12	0.03	0.15	-0.06
NO₂^-	-0.15	-0.10	0.06	0.01	0.07	-0.05	0.28	-0.06
PO₄^-3	0.11	0.38	-0.30	-0.29	-0.09	0.06	-0.13	-0.31	-0.11
NO₃^-	-0.25	-0.07	0.07	-0.14	-0.05	-0.01	0.17	0.06	0.01	-0.14
Micro	-0.24	0.20	-0.01	-0.44	-0.28	0.47	0.03	-0.09	-0.07	-0.03	0.18
Nano	0.18	-0.01	0.00	0.04	0.10	0.00	-0.30	0.04	-0.07	-0.11	-0.05	0.34
Chl-a	-0.02	0.10	-0.01	-0.22	-0.10	0.27	-0.18	-0.03	-0.09	-0.09	0.06	0.79	0.84
Abund.	0.53	0.21	-0.24	-0.09	0.16	-0.20	-0.18	-0.13	0.07	0.09	0.08	-0.15	-0.12	-0.16
Wind	-0.95	-0.39	0.57	-0.23	-0.11	0.07	0.78	0.03	0.09	-0.16	0.25	0.22	-0.22	-0.02	-0.38
Nitzs.	0.17	0.25	-0.21	-0.17	-0.06	0.41	-0.17	-0.19	0.02	0.35	-0.39	0.27	0.18	0.28	0.16	-0.23
Syned.	0.20	0.10	-0.18	0.04	-0.09	-0.07	-0.22	-0.23	-0.01	0.27	-0.27	-0.09	-0.03	-0.07	0.54	-0.17	0.50
Dipl.	-0.22	-0.24	0.10	0.08	-0.04	0.15	0.43	0.19	0.04	0.07	-0.10	-0.15	0.00	-0.08	0.06	0.21	0.24	0.21
Thal.	0.13	-0.07	-0.01	0.13	0.13	-0.06	-0.02	-0.12	-0.03	0.02	-0.33	-0.10	-0.15	-0.15	0.54	-0.10	0.43	0.67	0.31