Phytoplankton variation and its relation to nutrients and allochthonous organic matter in a coastal lagoon on the Gulf of Mexico

Estuarine, Coastal and Shelf Science 78 (2008) 705–714

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Phytoplankton variation and its relation to nutrients and allochthonous organic matter in a coastal lagoon on the Gulf of Mexico Jose´ A. Ake´-Castillo*, Gabriela Va´zquez ´n el Haya, 91070 Xalapa, Veracruz, Mexico Ecologı´a Funcional, Instituto de Ecologı´a, A. C., Carretera Antigua a Coatepec No. 351, Congregacio

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 August 2006 Accepted 19 February 2008 Available online 4 March 2008

In tropical and subtropical zones, coastal lagoons are surrounded by mangrove communities which are a source of high quantity organic matter that enters the aquatic system through litter fall. This organic matter decomposes, becoming a source of nutrients and other substances such as tannins, fulvic acids and humic acids that may affect the composition and productivity of phytoplankton communities. Sontecomapan is a coastal lagoon located in the southern Gulf of Mexico, which receives abundant litter fall from mangrove. To study the phytoplankton composition and its variation in this lagoon from October 2002 to October 2003, we evaluated the concentrations of dissolved folin phenol active substances  3 (FPAS) as a measure of plant organic matter, salinity, temperature, pH, O2, N-NHþ 4 , N-NO3 , P-PO4 , SiSiO2, and phytoplanktonic cell density in different mangrove influence zones including the three main rivers that feed the lagoon. Nutrients concentrations depended on freshwater from rivers, however these þ varied seasonally. Concentrations of P-PO3 4 , N-NH4 and FPAS were the highest in the dry season, when maximum mangrove litter fall is reported. Variation of these nutrients seemed to depend on the internal biogeochemical processes of the lagoon. Blooms of diatoms (Skeletonema spp., Cyclotella spp. and Chaetoceros holsaticus) and dinoflagellates (Peridinium aff. quinquecorne, Prorocentrum cordatum) occurred seasonally and in the different mangrove influence zones. The high cell densities in these zones and the occurrence of certain species and its ordination along gradient of FPAS in a canonical correspondence analysis, suggest that plant organic matter (i.e. mangrove influence) may contribute to phytoplankton dynamics in Sontecomapan lagoon. Ó 2008 Elsevier Ltd. All rights reserved.

Keywords: diatoms dinoflagellates organic matter nutrients coastal lagoon Mexico

1. Introduction Coastal lagoons are shallow systems where the hydrological dynamics depend on affluent rivers and their connection with the sea, which in some cases can be temporally blocked by a sand bar (Lankford, 1977). Phytoplankton communities can be very diverse as these ecotones represent complex systems where phytoplankton species from freshwater and marine environments converge, and form a mixed community that varies spatially, mainly along a salinity gradient (Emery and Stevenson, 1957). Although studies of phytoplankton communities indicate that patterns in structure and succession depend on the changes in environmental parameters (particularly salinity, temperature, light and nutrient availability), these patterns also vary with geographical region: tropical, temperate and polar (Wetzel, 2001). In tropical and subtropical zones, coastal lagoons are surrounded by mangrove communities, which represent a source of

* Corresponding author. E-mail address: [email protected] (J.A. Ake´-Castillo). 0272-7714/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2008.02.012

high quantity organic matter that enters the aquatic system through litter fall (Rivera-Monroy et al., 1995). This organic matter becomes a source of nutrients and other substances through decomposition processes that affect the composition and productivity of phytoplankton communities (Herrera-Silveira and Ramı´rezRamı´rez, 1996; Rivera-Monroy et al., 1998). The main fraction of organic matter from mangroves is leaf litter, and as it decomposes it liberates carbon, nitrogen and phosphorous compounds (Tam et al., 1990). Besides these inorganic substances, organic compounds such as humic material are liberated (Herrera-Silveira and Ramı´rez-Ramı´rez, 1996). The chemical nature of humic substances is poorly understood and different pathways, involving lignins, polyphenols and sugar condensation, contribute to their formation (Weber, 2005). In natural environments, humic matter has been shown to affect phytoplankton primary production both negatively (Jackson and Hecky, 1980; Guildford et al., 1987) and positively (Rivera-Monroy et al., 1995; Conzonno and Ferna´ndez, 1996; Danilov and Ekelund, 2001). Bioassays with species of microalgae exposed to the different compounds which are part of humic substances (i.e. tannins, fulvic acids and humic acids) have shown that the response is species-specific

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´zquez / Estuarine, Coastal and Shelf Science 78 (2008) 705–714 J.A. Ake´-Castillo, G. Va

(Toledo et al., 1980, 1982; Prakash and Rashid, 1968; Prakash et al., 1973; Herrera-Silveira and Ramı´rez-Ramı´rez, 1996), so the effect on natural systems may depend, in part, on the composition and physiological status of the phytoplankton community (Klug, 2002). Sontecomapan Lagoon is a coastal lagoon located in the south of the Gulf of Mexico, in an area of notable biodiversity, the Los Tuxtlas Biosphere Reserve. This lagoon receives abundant litterfall from Rhizophora mangle L. (1116 g m2 year1) and the leaf litter decomposes rapidly (Ake´-Castillo et al., 2006). The purpose of this study was to investigate the phytoplankton composition and its variation related to some environmental variables through time in this lagoon. Besides considering basic physicochemical and biological parameters, we evaluated the concentrations of dissolved folin phenol active substances (tannins and lignins) as a measure of the plant organic matter (Kalesh et al., 2001) that enters the lagoon. In addition, we evaluated the same environmental parameters for three rivers that feed the lagoon in order to estimate their contribution to nutrient input. The hypothesis in which we based this investigation was that phytoplankton dynamics responded besides the salinity variation and nutrient availability, to variation of dissolved folin phenol active substances derived from plant organic matter. By analyzing the relationship between these biological and environmental parameters we attempt to understand the relative importance of the environmental factors on this tropical phytoplankton community. 2. Study site and methods Sontecomapan Lagoon is a small (12 km long and 1.5 km wide) shallow coastal lagoon that is permanently connected to the Gulf of Mexico. It is located in the Los Tuxtlas Biosphere Reserve between 18 300 –18 340 N and 94 590 –95 040 W (Fig. 1). This region is characterized by three seasons: the dry season commonly from March to May, the rainy season from June to September, and the ‘‘nortes’’ season from October to February. The latter is characterized by strong winds coming from north and intense sporadic rainfall which sometimes could extend to the end of March or beginning of April. This lagoon is bordered by a mangrove forest that covers an area of 533.8 ha, and is comprised of Rhizophora mangle, Laguncularia racemosa, and Avicennia germinans; the first being the dominant species in the system (Ake´-Castillo et al., 2006). The mean depth of the lagoon is about 1.5 m with a semidiurnal tidal regime (<0.60 m). Three permanent rivers drain into the lagoon and it is also fed by small creeks during the rainy season. The lagoon is a brackish water system and its salinity varies spatially and temporally from 0 to 35 PSU (Ake´-Castillo et al., 1995). 2.1. Sampling design The study was conducted from October 2002 to October 2003. According to the morphology of the lagoon and influence of covering mangrove area (Twilley, 1988), calculated from mangrove area: open water ratios (MA:OW), four zones were identified: high influence zone (HIZ), low influence zone (LIZ), channel and rivers (Fig. 1). Seven sampling stations were set up in the lagoon covering these zones with one station in each of the 3 main rivers that drain into the lagoon at a distance of approximately 100 m from the mouth (Fig. 1). Samples were obtained bimonthly from each station at two depths: surface and 20 cm above the bottom (0.70 m the shallowest station and 2.5 m the deepest except station 10 which reached 15 m). The sampling design considered samples taken from each station as replicates within each zone. All field sampling was done between 09:00 and 14:00 h, sampling the stations in the same order. Water samples were collected using a 2.5 l volume Van Dorn bottle. On collection, oxygen, temperature, salinity, and pH were

Fig. 1. The Sontecomapan Lagoon with sampling stations. Mangrove influence zone is indicated by symbols: HIZ, rhombus; LIZ, triangle; Channel, squared; and Rivers, circle.

measured using a YSI Mod. 30 portable meter and a pH meter respectively. Samples were stored in plastic containers for the analysis of ammonium, nitrate, silica, and dissolved folin phenol active substances, and in glass containers for orthophosphate analysis. Samples were kept at 4  C for transportation to the laboratory (APHA, 1998). From the water sample, 125 ml was fixed with lugolacetate solution to count the phytoplankton. Net hauls (54 mm mesh size) were done at each station during 5 min to obtain additional phytoplankton material only for taxonomic determination. These samples were fixed with formalin to a final concentration of 4%. 2.2. Laboratory analysis Ammonium (N-NHþ 4 ) was determined using the Nessler method; nitrate (N-NO 3 ) using a colorimetric method with brucin; orthophosphate (P-PO3 4 ) using a colorimetric method with ascorbic acid; and silica (Si-SiO2) using a colorimetric method with molybdate following the techniques in Strickland and Parsons (1977), Horwitz (1980) and APHA (1998). The dissolved folin phenol active substances (FPAS) were estimated following APHA (1998), using the sodium tungstate-phosphomolybdic acid method with the addition of trisodium citrate solution to prevent the interference of Mg and Ca hydroxides and the bicarbonates present in sea water (Kalesh et al., 2001).

´ zquez / Estuarine, Coastal and Shelf Science 78 (2008) 705–714 J.A. Ake´-Castillo, G. Va

2.3. Phytoplankton counts Prior to quantitative analyses, we did a preliminary taxonomic survey to identify phytoplankton species in each station. For this purpose we used the phytoplankton net collections using a light microscope and preparing permanent slides for diatoms (Hasle, 1978a) and semi-permanent slides (using glycerine jelly) for dinoflagellates. Additional preparations were made for observation with the scanning electron microscope (JEOL-5600) for abundant species that were hard to identify under the light microscope. Cells were counted following the Utermo¨hl method with an inverted Leica DMIL microscope (Hasle, 1978b). The lugol preserved samples were gently shaken and poured into 20 ml sedimentation chambers allowing them to settle for 24 h before to count cells. Phytoplankton cells were counted by species at two steps: cells larger than 20 mm were counted at 100; cells smaller than 20 mm were counted at 400. In both cases we counted two crossed diameter transects. When sparse cells occurred, additional strips were counted until the count reached 300 cells of the most frequent species. For identification we mainly consulted Cupp (1943), Hasle and Syvertsen (1997), Krammer and Lange-Bertalot (1991a, 1991b, 1999), Dodge (1985), Steidinger and Tangen (1997).

2.4. Data analysis In order to detect the effect of the mangrove influence zones and season a two way analysis of variance (ANOVA) was done for each parameter. Factors tested were zones (HIZ, LIZ, Channel and rivers), and season (nortes, dry and rainy). Data were transformed to log10 (x þ 1) to achieve normality (Zar, 1999). A LSD Fisher test followed the ANOVA to reveal which groups differed in each analysis. We used the Statistica software package, version 7.0, (StatSoft, 2004) for these analyses. In order to determine whether there was a pattern of cell density in the lagoon, we did a two way ANOVA on cell density data, with month and zones as factors. A Tukey test followed this analysis to detect any groups that differed. To achieve normality, data were transformed to log10 (x þ 1) (Zar, 1999).

707

The Shannon–Wienner index for diversity was calculated for phytoplankton species quantified in the different mangrove influence zones. Statistical comparisons were made among indexes to find any significant differences (Zar, 1999). Canonical Correspondence Analysis (CCA) was used to investigate the relationship between the environmental parameters and phytoplankton abundance (Ter Braak, 1986). Species with a frequency of less than 5% of all samples were not included in the analysis in order to avoid the influence of rare species (Jongman et al., 1987). A code was assignated to the species used in the CCA analyses (Table 3). Species abundance data were log10 (x þ 1) transformed prior to analysis. A Monte Carlo test was performed to determine the significance of the correlations between the environmental and biological variables. The analyses were performed using the CANOCO software package, version 4.0 (Ter Braak and Smilauer, 1998). These analyses were done using all the data. 3. Results and discussion 3.1. Spatial variation Values of ratios of MA:OW are shown in Table 1. The ratios for the LIZ and channel zones were similar while in the HIZ the ratio was upper than 1. Total mean concentrations of FPAS were significatively higher in the HIZ and LIZ than the rivers, while mean concentration in the channel was similar to the LIZ and rivers. The concentrations of FPAS by zone support the classification of zones indicated by the ratio values of MA:OW. Salinity, temperature and pH were different according to the characteristics of marine or freshwater influence in the different zones. Total mean salinity was the highest in the channel, and the salt wedge reflect the hydrological condition of the lagoon related with the permanent connection to the sea, which had influence in all the lagoon and rivers establishing a gradient reflected in the different zones (Table 1). Temperature and pH were higher in the three zones in the lagoon than the rivers, reflecting the shallow condition of the lagoon, and the mixing of marine water and freshwater (Day et al., 1996). Oxygen was higher in HIZ, LIZ, and channel than the rivers, reflecting the high aquatic primary in the lagoon which is typical in coastal systems (Pennock et al., 1999).

Table 1 Ratio MA:OW and mean values of physicochemical parameters by mangrove influence, season and by season and influence zone. Nortes (N), dry (D), rainy (R), High influence zone (HIZ), Low influence zone (LIZ), Channel (CH), Rivers (RI). a, b, c, d, e and f indicate homogenous groups within factors of each physicochemical parameters after Fisher LSD test Factor

O2 mg l1

N-NHþ 4 mM

N-NO 3 mM

P-PO3 4 mM

Si-SiO2 mM

a b a b

7.70 a 7.18 a 7.06 a 5.67 b

21.45 a 26.77 ab 38.90 b 29.42 ab

2.46 a 3.88 b 2.08 a 4.76 b

0.832 a 1.102 a 1.161 ab 1.447 b

184.2 a 234.3 a 143.6 b 228.3 a

26.70 a 27.84 a 30.78 b

7.22 a 7.39 a 7.60 b

6.02 a 7.48 b 7.20 b

26.71 a 35.68 b 25.02 ab

4.53 a 2.43 a 2.92 a

0.861 a 1.831 b 0.714 a

229.7 a 177.1 a 186.0 a

MA:OW

FPAS mg l1

Salinity

T C

pH

1.61 0.31 0.37 –

0.113 a 0.104 ab 0.087 bc 0.071 c

10.41 ab 9.93 b 18.62 c 8.33 a

29.80 a 28.77 a 28.37 a 26.82 b

7.66 7.26 7.62 7.09

0.075 a 0.124 b 0.082 a

7.57 a 14.07 b 13.83 b

Mangrove influence zone

HIZ LIZ CH RI

Season

N D R

Season  Mangrove influence zone

N

HIZ LIZ CH RI

0.113 bd 0.077 abc 0.048 c 0.063 ac

6.92 de 3.09 def 14.94 abcf 5.33 d

27.52 abc 26.99 ab 26.85 abe 25.46 e

7.49 ab 7.06 cf 7.42 ad 6.90 f

6.73 abc 6.11 bd 6.12 bcd 5.11 e

9.68 b 30.16 a 35.82 a 31.18 a

3.66 a 5.40 ab 2.14 a 6.92 b

0.473 a 0.756 ab 1.044 abcd 1.170 bcd

219.0 ab 275.4 ab 160.5 d 263.7 b

D

HIZ LIZ CH RI

0.122 abd 0.155 d 0.145 d 0.074 abc

12.41 abc 13.45 ac 21.18 a 9.24 bdef

29.62 cdf 27.98 bc 27.72 abc 26.03 ae

7.61 abe 7.23 acd 7.60 abe 7.13 cdf

8.61 a 7.89 a 7.08 abc 6.32 abcd

36.47 a 34.72 a 36.33 a 35.19 a

1.49 ab 3.45 ab 1.56 a 3.23 ab

1.693 cde 1.659 ce 1.831 ce 2.142 e

164.2 abcd 212.0 abc 139.7 acd 192.6 abc

R

HIZ LIZ CH RI

0.105 abd 0.080 abc 0.068 abc 0.075 abc

11.91 abc 13.25 abc 19.75 a 10.41 bcef

32.27 d 31.35 d 30.53 df 28.98 cf

7. 88 e 7.49 ab 7.83 be 7.22 acd

7.75 abc 7.53 abc 7.98 ac 5.56 de

18.21 ab 15.42 ab 44.56 a 21.88 ab

2.23 ab 2.79 ab 2.53 ab 4.14 ab

0.329 a 0.891 abd 0.608 ab 1.030 abcd

169.4 abc 215.6 abc 130.7 cd 228.5 abc

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Differences in total mean nutrient concentrations per zones 3 were notorious for N-NO 3 , P-PO4 , being these nutrients dependent on freshwater supply, as shown by the highest concentrations in the rivers (Table 1). There were significant differences in N-NHþ 4 between HIZ and channel, having this last zone the highest concentration. This fact indicates that this nutrient is being incorporated more efficiently into the biogeochemical processes in the inner part of the lagoon than towards the sea (Gu¨rel et al., 2005). Concentration of Si-SiO2 did not show significant differences among rivers, HIZ and LIZ and these were very high compared to other tropical coastal lagoons in Yucatan on the Gulf of Mexico (1.8– 105.1 mM, Pennock et al., 1999). The concentration of Si-SiO2 in the streams of the Los Tuxtlas region, where Sontecomapan Lagoon is located, have been shown to be high (439–979.5 mM; RamosEscobedo and Va´zquez, 2001), so the concentrations recorded for Sontecomapan Lagoon show that this nutrient is also dependent on rivers influence. 3.2. Temporal variation The values of the physicochemical parameters evaluated over time varied seasonally according to the climatic characterization of this zone of the Gulf of Mexico i.e. nortes, dry and rainy season (Day et al., 1996). According to the pattern observed in all physicochemical variables in Fig. 2, and based mainly in salinity values, for the period of our study, February represented the

transition between nortes and dry season, while June represented the transition between the dry and the rainy season. The progression of the lagoon stratified by the salt wedge during October, December and February to well mixed lagoon in April indicated a recovery phase typical of wet tropical estuaries (Eyre, 1998). Variation of FPAS concentration was the same in the different zones with the least concentrations in the river and channel zones (Fig. 2a). Mean concentration of FPAS through time was higher in February, April, June and October 2003 than October 2002, December 2002 and August, being higher in HIZ, LIZ and channel than the rivers indicating a noticeable influence of plant organic matter in these zones. The peaks of FPAS concentration in water occurred in the dry and rainy season (Table 1) when maxima litter fall production from Rhizophora mangle is reported for this lagoon (Ake´Castillo et al., 2006). In October 2003 we detected high concentrations of FPAS but this sampling was done during a typical Norte event that caused turbulence (sediment resuspension) by the rain and marine currents caused by the strong winds as shown by salinity values (Fig. 2a,b). Salinity increased during April and June and during a Norte event in October 2003. Temperature was the highest during April, June and August, the hottest months of the years with low temperatures in December, February and October 2002 (Fig. 2b,c). The pH showed a seasonal pattern in HIZ, LIZ and channel but not in the rivers. The lowest values were recorded in April and October 2003

 Fig. 2. Variation in physicochemical parameters measured from October 2002 to October 2003. (a) FPAS; (b) salinity; (c) temperature; (d) pH; (e) O2; (f) N-NHþ 4 ; (g) N-NO3 ; (h) PPO3 4 ; and (i) Si-SiO2. Middle points represent the mean, whiskers are 95% confidence intervals. The square indicates the HIZ; circle the LIZ; rhombus the channel; triangle the rivers.

´ zquez / Estuarine, Coastal and Shelf Science 78 (2008) 705–714 J.A. Ake´-Castillo, G. Va

(Fig. 2d). Oxygen did not show a seasonal pattern (Fig. 2e) but in February a peak was detected in HIZ. Variation of nutrients was the same for all zones except for N-NO 3 (Fig. 2f–i). April the driest month of the year made the differences among the months (Table 1), and contrary to the decrease of concentration of nutrients that we expected as a result of 3 diminution of freshwater supply, N-NHþ 4 and P-PO4 concentrations were the highest. In addition, the differences in concentration among zones showed higher values in HIZ and LIZ than in the rivers 3 such as N-NHþ in LIZ in April 4 in April and June and P-PO4 (Fig. 2h,f). This pattern and differences among zones indicated that besides of the concentrations of these nutrients depending on freshwater supply, these depend also on other sources. These high concentrations might have been produced by biogeochemical cycles including sediment-water column exchange and decomposition processes (Perkins, 1974; Twilley et al., 1999). Nitrate showed peaks only in the channel and rivers in December 2002 (Fig. 2g). The silicate concentration followed the freshwater supply being high in the rainy and nortes season (Fig. 2i). 3.3. Cell density Total mean cell density was different among zones (Table 2). Highest concentration were recorded in HIZ and LIZ followed by the channel and rivers. However, variation in cell density depended on the influence zone and month (significative interaction month * influence zone F ¼ 2.24, P ¼ 0.005). Two peaks of cell densities were detected: one in December having the HIZ the highest density, and one in August having LIZ and HIZ the highest cell densities (Fig. 3). Cell concentration in rivers did not show a significant pattern along time. Phytoplankton growth dynamics corresponded to that pointed out by Eyre (2000) in which high biomass is a response to runoff events. The peak in December was related to small floods while the peak in August was related to larger floods. The peak in December occurred in a low or medium flow stage during the recovery phase as observed in subtropical and tropical estuaries in Australia (Eyre, 2000). The highest peak occurred in August during floods following the dry season. This phytoplankton growth, besides to be associated to runoff events (Eyre, 2000), seems to be associated to warm temperatures of the rainy season in this tropical region of the Gulf of Mexico (Pennock et al., 1999). Blooms of different species (more than 1000 cells ml1) were recorded in all sampled months except in April (Table 2). Most of the blooms were mainly recorded in HIZ and LIZ, although in October 2003, when sampling was done in a typical ‘‘norte’’ event, high densities of Skeletonema subsalsum and Skeletonema pseudocostatum were found in one river. Table 2 Total mean cell density by zones and species causing blooms. a, b, c, indicate homogenous groups after Tukey test

Total mean cell/ml Cyclotella cryptica and C. meneghiniana Skeletonema subsalsum Peridinium aff. quinquecorne Prorocentrum cordatum Chaetoceros holsaticus S. pseudocostatum

HIZ

LIZ

Channel

Rivers

2226.47 (215.51) a October 2002 August 2003

2015.40 (289.14) a October 2002 August 2003 October 2003 December 2002 October 2003 –

1048.86 (261) b October 2002 August 2003 October 2003 December 2002

327.39 (208.20) c –

–

–

December 2002 October 2003 February 2003

October 2003

–

June 2003

–

–

–

August 2003

–

–

October 2003

October 2003

–

October 2003

709

Table 3 List of species found in the Sontecomapan Lagoon in the different mangrove influence zones. The species that were used in the CCA analyses are indicated by the code Code Bacillariophyceae Achnanthes cf. curvirostrum J. Brun Achnanthes exigua Grunow in Cleve & Grunow Achnanthes sublaevis Hustedt Achnanthes sp. Amphipleura sp. Amphora sp. Asterionellopsis glacialis (Castracane) Round Azpeitia nodulifera (Schmidt) Fryxell et Sims Bacillaria paxillifera (O.F. Mu¨ller) Hendey Bacteriastrum elegans Pavillard Bacteriastrum elongatum Cleve Biddulphia pulchella S.F. Gray Biddulphia sp. Caloneis sp. Chaetoceros affinis Lauder Chaetoceros curvisetus Cleve Chaetoceros danicus Cleve Chaetoceros diversus Cleve Chaetoceros heterovalvatus Proschkina-Lavrenko Chaetoceros holsaticus Schu¨tt Chaetoceros laciniosus Schu¨t Chaetoceros lorenzianus Grunow Chaetoceros mulleri var subsalsum (Lemmermann) Johansen et Rushforth Chaetoceros peruvianus Brightwell Chaetoceros simplex Ostenfeld Chaetoceros subtilis var. abnormis f. abnormis Proschkina-Lavrenko Chaetoceros subtilis var. abnormis f. simplex Proschkina-Lavrenko Chaetoceros throndsenii var. throndsenia (Marino, Montresor & Zingone) Marino, Montresor & Zingone Chaetoceros throndsenii var. trisetosa Zingone in Marino et al. Cocconeis scutellum Ehrenberg Coscinodiscus concinnus Wm. Smith Coscinodiscus granii Gough Coscinodiscus radiatus Ehrenberg Cyclotella cf. austriaca (M. Peragallo) Hustedt Cyclotella cryptica Reimann Lewin et Guillard Cyclotella meneghiniana Ku¨tzing Cyclotella striata (Ku¨tzing) Grunow Cylindrotheca closterium (Ehrenberg) Reimann et Lewin Cymatopleura sp. Cymatosira sp. Cymbella sp. Diploneis bombus Ehrenberg Diploneis sp. Ditylum brightwelli (West) Grunow Entomoneis alata (Ehrenberg) Ehrenberg Eucampia zodiacus Ehrenberg Fragilaria counstruens f. counstruens (Ehrenberg) Hustedt Fragilaria ulna var. goulardii (Bre´b. Ex Cleve et Grunow) Lange-Bertalot Fragilaria ulna var. ulna (Nitzsch) LangeBertalot Fragilaria sp. Gomphoneis olivacea (Lyngbye) Dawson Gomphonema parvulum (Ku¨tzing) Ku¨tzing Guinardia flaccida (Castracane) Peragallo Guinardia striata (Stolterfoth) Hasle Gyrosigma balticum (Ehrenberg) Rabenhorst

Achsu

HIZ

LIZ

* *

* *

* *

* *

Channel

* *

Amphi Asgla

*

*

Rivers

*

** ** * **

Bapa

*

*

*

*

* *

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** * ** * * * *

* * * *

* * * *

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Chsim

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* * *

Chabsim

*

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*

Coscu Cossp1

* * *

* * *

Cyaus

*

*

Cycplx

*

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*

*

Cycplx Cystr Cylclos

* * *

* * *

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* * *

* *

* *

Enala

* * * * *

* * * * *

Fugou

*

*

*

*

Fuuln

*

*

*

*

Gooli Gopar

* * * *

* * * *

Gybal

*

*

Chhet Chhol

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Cymsp1

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(continued on next page)

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´zquez / Estuarine, Coastal and Shelf Science 78 (2008) 705–714 J.A. Ake´-Castillo, G. Va Table 3 (continued )

Table 3 (continued ) Code Gyrosigma fasciola (Ehrenberg) Griffith & Henfrey Gyrosigma robustum (Grunow in Cleve & Grunow) Cleve Gyrosigma cf. terryanum (H. Peragallo) Cleve Gyrosigma sp. Hemiaulus sinensis Greville Hyalodiscus sp. Leptocylindrus danicus Cleve Licmophora sp. Lithodesmium undulatum Ehrenberg Luticula mutica (Ku¨tzing) D.G. Mann in Round et al. Luticula sp. Lyrella impercepta (Hustedt) Moreno Lyrella sp. Melosira nummuloides Agardh Minidiscus comicus Takano Navicula cryptocephala Ku¨tzing Navicula soehrensis Krasske Navicula pelliculosa (Ku¨tzing) Hilse Navicula cf. pennata Schmidt in Schmidt Navicula cf. peregrina (Ehrenberg) Ku¨tzing Navicula cf. takoradiensis Hendey Navicula sp. 1 Navicula sp. 2 Neidium cf. iridis (Ehr.) Cleve Neidium sp. Neocalyptrella robusta (Norman ex Ralfs) Herna´ndez-Becerril & Meave Nitzschia amphibia Grunow Nitzschia constricta (Ku¨tzing) Ralfs Nitzschia frustulum (Ku¨tzing) Grunow Nitzschia hantzschiana Rabh Nitzschia longissima (Bre´bisson in Ku¨tzing) Ralfs in Pritchard Nitzschia ovalis Arnott Nitzschia palea (Ku¨tzing) Wm. Smith Nitzschia sigma (Ku¨tzing) Wm. Smith Nitzschia triblyonella Hantzsch Nitzschia cf. linearis W. Smith Nitzschia sp. Odontella longicruris (Greville) Hoban Opephora martiyi He´ribaud Paralia sulcata (Ehrenberg) Cleve Petrodyction gemma (Ehr.) D.G. Mann Petroneis humerosa (Breb. Ex Smith) Stickle & Mann Pinnularia sp. Plagiotropis sp. Pleurosigma acuminatum (Ku¨tzing) Grunow Pleurosigma angulatum (Quekett) W. Smith Pleurosigma formosum W. Smith Pleurosira laevis (Ehr.) Compe`re Proboscia alata (Brightwell) Sundstro¨m Psammodictyon constrictum (Gregory) D.G. Mann Pseudonitzschia sp. Pseudosolenia calcar-avis (Schultze) Sundstro¨m Rhizosolenia imbricata Brightwell Rhizosolenia setigera Brightwell Rhizosolenia sp. Sellophora pupula (Ku¨tzing) Mereschkowsky Skeletonema costatum (Greville) Cleve Skeletonema pseudocostatum Medlin Skeletonema subsalsum (A. Cleve) Bethge Surirella biseriata Bre´bisson Surirella fastuosa Ehrenberg Surirella febigerii Lewis Surirella linearis W. Smith Surirella robusta Ehrenberg Terpsinoe musica Ehrenberg

HIZ

LIZ

*

*

Gyrob

*

*

*

*

Gyterr

*

*

*

*

* * * *

* * * *

* * *

* * *

Hyasp

Channel

Rivers

** ** ** * *

* *

* * *

* * *

* * *

* * *

* * **

* *

*

*

*

** *

Nitamp Nitcon Nitfru Nithan Nitlo

* * * * *

* * * * *

* * * * *

Nitsig Nittry

* * * *

* * * *

* * ** * * *

* *

Menum

* * ** * * *

Navpe

Pasul Pegem

* * *

*

* * *

* * * **

* *

* * * * **

* * *

* *

** *

* **

*

*

*

*

*

*

*

*

* *

* *

* ** * *

* *

* *

* *

*

*

*

*

Skcos Skpse Sksub

* * *

* * *

Sufas Sufeb

* *

* *

* *

* *

Plfor

*

* * *

** * **

* * * ** * * ** * *

Thalassionema nitzschiodez (Grunow) Mereschkowsky Thalassiosira cedarkeyensi A.K.S.K. Prasad Thalassiosira eccentrica (Ehrenberg) Cleve Thalassiosira lineata Jouse´ Thalassiosira oestrupii (Ostenfeld) Hasle Thalassiosira simonsenii Hasle & Fryxell Thalassiosira decipiens (Grunow) Jo¨rgensen Thalassiosira weissflogii (Grunow) G. Fryxell & Hasle Thalassiotrhirx longissima Cleve & Grunow Trachyneis aspera (Ehrenbegr) Cleve Tryblionella cocconeiformis (Grunow) D.G. Mann Tryblionella parvula (W. Smith) Ohtsuka & Fujita Tryblionella punctata Wm. Smith Tryblionella cf. calida (Grunow) D.G. Mann Chlorophyceae Scenodesmus armatus Chad Scenodesmus dispar (Breb.) Rabenhorst Scenedesmus cf. pecsensis Uherk. Closterium sp. Cosmarium sp. 1 Cosmarium sp. 2 Mougeotia sp. Ocystis sp. Euglenophyceae Lepocinclis acus Ehrenberg Phacus caudatus Huebner

Code

HIZ

LIZ

Channel

Rivers

Tmanit

*

*

*

*

Thace

*

*

* * **

* *

Thasim

*

* **

**

Other flagellates Chlamydomonas sp. Pyramimonas sp. Phytoflagellate sp. 1 Phytoflagellate sp. 2 *Indicates the occurrence. **Indicates exclusive in that zone.

*

*

*

*

** *

*

*

*

* *

* *

*

* * *

* * *

Traas

Trypun

Scedis

Lepacu

* *

* *

*

*

* ** ** ** *

**

Cyanophyceae Chroccocus sp. Komvophoron sp. Merismopedia tenussima Lemmermann Nostoc sp. Oscillatorial nigro-viridis Thwaites in Harvey Oscillatoria cf. limosa Agardh ex Gomant Oscillatoria sp. Planktolyngbya sp. Synechococcus sp. Dinophyceae Amphidinium sphenoides Wulff Amphidinium sp.1 Amphidinium sp. 2 Ceratium furca var. hircus (Scho¨der) Margalef ex Sournia Dinophysis caudata Saville-Kent Gonyaulax digitale (Pouchet) Kofoid Gymnodinium sp. Heterocapsa sp. Noctiluca scintillans (Macartney) Ehrenberg Oxytoxum sp. Peridinium aff. quinquecorne Peridinium sp. 1 Peridinium sp. 2 Prorocentrum cordatum (Ostenfeld) Dodge Prorocentrum gracile Schu¨tt Prorocentrum lima (Ehrenberg) Dodge Prorocentrum micans Ehrenberg Protoperidinium crassipes (Kofoid) Balech Protoperidinium sp. Scrippsiella sp.

** *

*

*

*

*

* * *

* * *

*

** * *

*

*

*

* * **

Amsph

Cefuhir

Godig

* ** ** *

*

*

*

*

*

*

* * * *

* * * *

*

*

**

Pequi Pesp1 Pesp2 Procor Progra Prolim

Scrsp

* * * * * * * * * * * *

* * * * * * * * * * *

*

*

* *

*

*

* * * ** ** **

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711

June when cell densities were the lowest in these zones. In April, when no bloom of any species occurred, the diversity index values in HIZ, channel and rivers were the highest, indicating that species were equally abundant in this month. 3.5. Species composition A total of 179 taxa were recorded in both the lagoon and the three rivers draining into it. There were 5 species exclusively

Fig. 3. Cell density for each month in the different influence zone: square indicates the HIZ; circle the LIZ; rhombus the channel; triangle the rivers. The middle point represents the mean and whiskers are 95% confidence intervals. Note Y scale is logarithmic.

Blooms of Skeletonema species have been recorded elsewhere (Nikulina, 2003). The dinoflagellates Peridinium aff. quinquecorne and Prorocentrum cordatum have been reported forming blooms in coastal systems (Phlips et al., 2002; Baro´n-Campis et al., 2005; Coelho et al., 2007). Moreover, the latter species has been recorded as toxic (Grzebyk et al., 1997) and has spread worldwide (Hajdu et al., 2000). To our knowledge Chaetoceros holsaticus is recorded here for the first time as causing blooms. Owing to the high cell densities throughout the seasons and the records of all these species, Sontecomapan Lagoon can be considered a eutrophic aquatic system (Livingstone, 2001).

3.4. Diversity The diversity indexes calculated for the different zones resulted in the rivers having the highest values (Fig. 4). Within the lagoon, the diversity index values in HIZ, LIZ and channel differed among them in each month without a clear pattern. Variation of diversity index in all zones through time was contrarily to cell density peaks, having low values in December and August when the highest cell densities were recorded, and high values in February, April and

Fig. 4. Variation of Shannon–Wienner diversity index for each mangrove influence zone. (a, b, c) Indicate significative differences (P < 0.05) among zones within each month.

Fig. 5. Dynamics of dominant phytoplankton species. (a) Nortes season; (b) dry season; and (c) rainy season. Middle points represent the mean, whiskers show the minimum and maximum values. Note Y scale is logarithmic.

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Fig. 6. Correlation biplot based on CCA analyses. The Monte Carlo test showed that first axis was significant (F ¼ 6.3, P ¼ 0.005), as were all canonical axes (F ¼ 2.7, P ¼ 0.005). (a) Environmental-species biplot of the lagoon. (b) Environmental-site biplot of the lagoon. Environmental variables are indicated by arrows. Environmental scores were multiplied by 2 to fit the coordinate system. In figure (a) abbreviations of species are given in Table 3. In figure (b) empty circle represents October 2002; plus symbol December 2002; asterisk February 2003; solid rhombus April 2003; solid triangle June 2003; solid square August 2003; and solid circles October 2003.

recorded in the HIZ, 5 in the channel, and 31 in the rivers while in the LIZ there were not exclusive species recorded (Table 3). The phytoplankton assemblages were mainly comprised of Bacillariophyceae (76% lagoon, 79% rivers), followed by Dinophyceae (14% lagoon, 7% rivers), Cyanophyceae (5% lagoon, 6% rivers), Chlorophyceae (3% lagoon, 4% rivers), Euglenophyceae (1% lagoon, 1% rivers) and other phytoflagellates (1% lagoon, 3% rivers). Species that dominated the phytoplankton composition were spread out in the lagoon and rivers and comprised mainly diatoms (Fig. 5). In October 2002, December 2002 and October 2003 (nortes season) the most abundant species were the diatoms Chaetoceros subtilis var. abnormis f. simplex and different species of Skeletonema (Fig. 5a) with affinities for freshwater, brackish water, and marine salinities (Ake´-Castillo et al., 1995, 2004). In February (transition from the nortes to the dry season) the dinoflagellates Peridinium aff. quinquecorne and Prorocentrum cordatum, dominated the assemblage, then in April (dry season) Ceratium furca var. hircus and the diatom Thalassiosira cedarkeyensis dominated. These dinoflagellates have been reported for brackish water and marine environments (Guerra-Martı´nez and Lara-Villa, 1996; Phlips et al., 2002; Baro´n-Campis et al., 2005) while the Thalassiosira has been recorded only in a marine environment (Prasad et al., 1993). June (transition dry–rainy season) was dominated by P. cordatum and

the dinoflagellate Scrippsiella sp. was also abundant (Fig. 5b). In this month solitary diatoms began occurring and in August (rainy season) their abundance increased. Different species of Cyclotella with affinities to freshwater and brackish water environments (Reimann et al., 1963) were dominant along with Chaetoceros simplex and Chaetoceros holsaticus (brackishwater species; Hasle and Syvertsen, 1997). These species persisted until October 2003 (beginning of the nortes season) when Skeletonema spp. dominated again. Variation in the phytoplankton community was characterized by season as follow: nortes season: freshwater, brackish water and marine diatom species; dry season: brackish water and marine dinoflagellates and the marine species Thalassiosira cedarkeyensis; and rainy season: freshwater and brackish water diatoms. 3.6. Relationship between environmental parameters and phytoplankton The analysis of CCA was a tool that let us explore the relationship between species composition and the physicochemical parameters considering the abundance of species through the studied period of time. The result of this analysis is a plot in which ordination of species show their relationship along the different gradients of parameters evaluated (Ter Braak, 1986; Jongman et al., 1987), so

Fig. 7. Ranking of dominant species along FPAS vector gradient from CCA.

´ zquez / Estuarine, Coastal and Shelf Science 78 (2008) 705–714 J.A. Ake´-Castillo, G. Va

each species can be analyzed in relation of the variable of particular interest. Under this approach, ordination of species along the FPAS gradient, which was the variable of our interest as indicative of plant organic matter influence, showed an interesting pattern that support the results presented above. The long line of FPAS shows the strong influence of this variable in the phytoplankton community apart of salinity and silicate (Fig. 6a), which were the variables that influence the most in the seasonal characterization of Sontecomapan lagoon shown in Fig. 6b. The ranking of the dominant species response to this variable (Fig. 7) shows that dinoflagellates were associated to high concentration of FPAS while diatoms were associated to medium and low concentrations with exception of Thalassiosira cedarkeyensis. Response of phytoplankton to dissolved organic matter can result in stimulating or inhibiting growth through different mechanisms i.e. quelation of heavy metals, controlling availability of nutrients, blocking light (Jackson and Hecky, 1980; Guildford et al., 1987; Conzonno and Ferna´ndez, 1996; Danilov and Ekelund, 2001) and although we do not know the mechanisms controlling the response in Sontecomapan lagoon, the correlation of species with FPAS indicated that dinoflagellates and T. cedarkeyensis have their higher-than-average optimum growth than the other species when concentration of FPAS is high. Experimental evidence of positive effect of humic substances in the growth of Prorocentrum minimum (¼Prorocentrum cordatum) (Grane´li et al., 1985), and negative effect of high concentration as well as positive effect of low concentration of tannic acid in the growth of Skeletonema costatum (Herrera-Silveira and Ramı´rez-Ramı´rez, 1996), support the observed results of the ordination of the dominant dinoflagellates and diatoms related with FPAS vector gradient in the different seasons. Although ordination precludes showing a spatial pattern (different influence zones), it was successful in showing the temporal pattern of data ordination along gradients of environmental factors þ (Fig. 6b). The gradients of P-PO3 4 , N-NH4 and FPAS reflected the plant organic matter input mainly in the dry season. The dynamics of community structure among the diatoms and dinoflagellates is similar to that reported for estuaries with a strong relationship to the salinity gradient and changes in temperature (Trigueros and Orive, 2001). However, values of MA:OW ratio, the records of phytoplankton blooms in HIZ and LIZ and occurrence of certain species and its ordination along gradient of FPAS in CCA biplot, suggest that plant organic matter (i.e. mangrove influence) may contribute to phytoplankton dynamics in Sontecomapan lagoon. Acknowledgements The Instituto de Ecologı´a, A. C. (projects 902-17 and 902-11-280) and CONACYT (32732-T) provided financial support. We thank Ricardo Madrigal, Javier Tolome and Olivia Herna´ndez for providing support in the field. Ariadna Martı´nez helped with the laboratory analyses of water samples. Ange´lica Herna´ndez made valuable suggestions regarding the statistical analyses. Mario Favila kindly read and improved an earlier manuscript. We thank B. Delfosse for helping with the English. Anonymous reviewers improved this paper. The first author gratefully acknowledges the support of CONACYT (scholarship 90031) during his doctoral studies as this work is part of his Ph.D. thesis. References Ake´-Castillo, J.A., Meave, M.E., Herna´ndez-Becerril, D.U., 1995. Morphology and distribution of species of the diatom genus Skeletonema in a tropical coastal lagoon. European Journal of Phycology 30, 107–115. Ake´-Castillo, J.A., Guerra-Martı´nez, S.L., Zamudio-Rese´ndiz, M.E., 2004. Observation on some species of Chaetoceros (Bacillariophyceae) with reduced number of setae from a tropical coastal lagoon. Hydrobiologia 524, 203–213.

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