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Ecology of the Sontecomapan Lagoon, Veracruz

 | 
Maria Elena Castellanos-Páez
, 
Alfonso Esquivel Herrera
, 
Javier Aldeco-Ramírez
, 
et al.

Part 4. Primary producers

The effect of mangrove leaf litter extracts on primary productivity and phytoplankton growth

José Antolín Aké-Castillo et Gabriela Vázquez

Résumé

The relationship between dissolved organic matter and phytoplankton function has either a positive or a negative effect on primary productivity and phytoplankton growth. Sontecomapan is a coastal lagoon located at the south of Veracruz, Mexico, which is bordered by a mangrove forest where Rhizophora mangle is the dominant species. In the lagoon, the concentrations of folin phenol active substances (FPAS) are indicative of the high input of plant organic matter. Because of the different effects that organic matter can have on phytoplankton function, we performed bioassays to determine the effects of mangrove leaf litter extracts on primary productivity and phytoplankton growth within different seasons. The inhibitory and stimulatory effects observed on primary productivity and phytoplankton growth, are indicative that leachate mangrove is made off of a mixture of both, stimulatory and inhibitory substances. Results suggest that phytoplankton species’ tolerance to concentrations of FPAS in the extracts is important for the response. Chaetoceros muelleri var subsalsum, Cyclotella cryptica, and C. meneghiniana are sensitive to high concentrations of FPAS while Skeletonema subsalsum was able to tolerate moderate concentrations of FPAS. These responses support the hypothesis that tolerances to organic compounds in natural systems influence the dynamics of phytoplankton communities.

Texte intégral

Introduction

1Plant organic matter is a source of nutrients and humic substances that affect primary production and influence the phytoplankton dynamics in both, marine and freshwater environments (Herrera-Silveira & Ramírez-Ramírez, 1996; Rivera-Monroy et al., 1998; Danilov & Ekelund, 2001; Klug, 2002). The relationship between dissolved organic matter and phytoplankton function has either a positive or a negative effect on primary productivity and phytoplankton growth, so the net effect of dissolved organic matter is under debate (Klug, 2002; Sánchez-Marín & Beiras, 2014).

2Jackson & Hecky (1980) evaluated the effect of dissolved organic matter on the primary productivity of a lake and reservoirs in Canada and found an inverse relationship between primary productivity and dissolved organic carbon. In contrast, Rivera-Monroy et al. (1998) demonstrated the stimulatory effect on primary productivity in a series of a runoff addition series from a fringe mangrove forest in water from Terminos Lagoon, Mexico.

3The response of phytoplankton growth has been tested using specific humic compounds such as humic acid, fulvic acid and tannins on different microalgae species. These studies show that the stimulatory effect of humic substances results from their capacity to chelate damaging metallic ions such as copper (Toledo et al., 1980, 1982), possible cell sensitization, chelation of essential ions that penetrate the cell (Prakash et al., 1973), and by supplying nitrogen as a nutrient (Granéli et al., 1985). The inhibitory effect is due mainly to humic substances that decrease the availability of trace minerals such as iron (Jackson & Henry, 1980; Imai et al., 1999).

4Tropical coastal lagoons and estuaries are characterized by a high input of terrestrial organic materials from surrounding mangrove communities (Flores-Verdugo et al., 1987; Tam et al., 1990). Mangrove leaves have a high concentration of tannins which are liberated rapidly in the early stages of decomposition (Cundell et al., 1979); in coastal systems, the concentration of these substances can be high (Kalesh et al., 2001). Sontecomapan is a coastal lagoon bordered by a mangrove forest where Rhizophora mangle L. is the dominant species. The concentration of folin phenol active substances in this lagoon varies seasonally from 0 to 0.236 mg l-1 (Aké-Castillo & Vázquez, 2008), with the highest values in the dry season. These concentrations are indicative of the high input of plant organic matter. The phytoplankton dynamics in the lagoon is characterized by blooms of diatoms and dinoflagellates, which dominate the species’ composition seasonally (Aké-Castillo & Vázquez, 2008).

5Due to the different effects that organic matter can have on phytoplankton function, we experimented with the effects of mangrove leaf litter extracts on primary productivity and phytoplankton growth in different seasons. Our aim was to determine if the mangrove leaf litter was a source of nutrients throughout the decomposition process. To test the effect of substances from mangrove leachate, products from different days of decomposition were used to test the effect on the primary productivity and phytoplankton growth from a Sontecomapan Lagoon natural community.

Materials and methods

Site description

6Sontecomapan Lagoon is a shallow coastal lagoon permanently connected to the Gulf of Mexico. It is located in Los Tuxtlas Biosphere Reserve between 18º 30’-18º 34’ N and 94º 59’-95º 04’ W (Fig. 1). This region is has three climatic seasons: dry from March to May, rainy from June to September, and “Nortes” from October to February. The latter is determined by strong winds coming from the North and sporadic rainfalls. The lagoon is bordered by a mangrove forest where Rhizophora mangle is the dominant species (Aké-Castillo et al., 2006): it is a brackish water system where salinity varies spatially and temporally from 0 to 35 %. Variation in the phytoplankton community is reflected by a dominant species in each season: in the “Nortes” season, the community is dominated by the diatoms Skeletonema subsalsum, S. pseudocostaum and S. costatum; during the dry season, the dinoflagellates Peridinium quinquecorne, Prorocentrum cordatum, Ceratium furca var hircus, Scrippsiella sp., and the diatom Thalassiosira cedarkeyensis are the dominating species; and during the rainy season the lagoon is again dominated by diatoms: Cyclotella cryptica, C. meneghiniana, C. striata, Chaetoceros holsaticus and C. simplex (Aké-Castillo & Vázquez, 2008). Phytoplankton production is higher in the rainy season and it is correlated significantly to different groups of the zooplankton community (Benítez-Díaz Mirón et al., 2014).

Figure 1. Sontecomapan Lagoon’s location indicating primary productivity experiments sites.

Figure 1. Sontecomapan Lagoon’s location indicating primary productivity experiments sites.

Extract obtained from decomposing Rhizophora mangle leaves

7Senescent leaves of Rhizophora mangle were collected by hand from different sites of the water edge at Sontecomapan Lagoon in February 2003, and transported in a cooler with ice to the laboratory. Over there, leaves from the sites were mixed up and gently washed to eliminate mud. Substances from the decomposing leaves were obtained by incubating 10 g of the wet fresh leaves into 3 l of distilled water in 3 plastics bottles previously washed with a HCI solution at 5 %. The chosen concentration (10 g/ 3 l) is an intermediate value of experimental designs of leaf decomposition used in different previous works (Ashton et al., 1999; Aké-Castillo et al., 2006). Three bottles without leaves were used as controls, all bottles were maintained at room/laboratory temperature (26 °C) under natural daylight-darkness conditions and were aerated with low pressure using aquarium pumps. At day 2 of the experiment, water level was maintained by adding distilled water when necessary (without replenish the water from analyses).

8As wet fresh leaves were used for the incubations, initial dry weight was estimated by weighing 3 samples of the fresh leaves and then drying them to constant weight at 60 ºC in a muffle furnace (Davis III et al., 2003).

9Considering classical negative exponential model of mangrove leaf litter decay (Flores-Verdugo et al., 1987; Aké-Castillo et al., 2006), on days 0, 2, 5, 10, 25 and 45 a sample of 160 ml of water was taken from each bottle for chemical analyses. Ammonium (N-NH4+), nitrate (N-NO3-), orthophosphate (P-PO43-) and folin phenol active substances (tannins and lignins) (FPAS) were determined using colorimetric techniques following the Strickland and Parsons methods (1977), Horwitz (1980), and APHA (1998). Each day a 20 ml sample was stored in ambar jars at 4 °C for later use in the primary productivity and phytoplankton growth experiments. We assumed not evolution of inorganic concentration occurred in refrigeration (APHA, 1998).

Effect on primary productivity

10Experimental design. The effect of mangrove leaf extracts on primary productivity (PP) was evaluated during 2003, close to the time when senescent leaves were collected, in three different months representing the three climatic seasons: dry season (May), rainy season (August) and “Nortes” season (October). There were five treatments including controls and three extracts from mangrove leaves in different stages of decomposition. One control consisted in no addition of any extract, and the other one with addition of the freshwater media used for incubating leaf litter. The extracts tested were those obtained on days 2, 10, and 45, which represent times in early, late and inflexion point of leaf litter decay model.. The treatments for the experimental design and characteristics of the extracts are shown in Table 1. Each treatment was triple-tested.

11Treatments were tested in water samples from two sites with different marine influence: one in the interior of the lagoon and the other close to the channel connection with the sea (Fig. 1).

Table 1. Characteristics of extracts obtained from decomposing mangrove leaf litter and used in experiments on primary productivity and phytoplankton growth.

Table 1. Characteristics of extracts obtained from decomposing mangrove leaf litter and used in experiments on primary productivity and phytoplankton growth.

WL: water lagoon from each month of experiment (standard deviation)

12Primary productivity experiment. Each month, primary production was determined using the light-dark DBO bottle method, and oxygen concentration was evaluated using the Winkler method (Vollenweider, 1974). DBO bottles (300 ml) were filled with water collected from both sites. Except for treatment 1, DBO bottles were inoculated with 1 ml of each extract (0.3 % of DBO volume) and were hung 20 cm deep into the lagoon to incubate for 4 hours. The results are expressed as gross primary productivity (GPP) transformed to mg C L-1hr-1with a conversion factor of 0.375 mol carbon production with a photosynthetic coefficient of 1.2 (Wetzel & Likens, 2000).

The effect on phytoplankton growth

13Experimental design. The effect of mangrove leaf extract on phytoplankton growth was evaluated in phytoplankton cultures from water samples taken in May, August and October 2003 at site 1 in Sontecomapan Lagoon (Fig.1). The phytoplankton cultures represented the three climatic seasons: dry, rainy and “Nortes”. The same treatments as in the PP experiment were tested on phytoplankton growth (Table 1). Each treatment was tested in 5 replicates.

14Phytoplankton cultures. We used natural water from the lagoon as culture medium. This was prepared by collecting 3 l of water from the Sontecomapan Lagoon at site 1 a month before May, August and October when the phytoplankton inoculations were done (Fig. 1). The collected water was taken to the laboratory and then filtered using a 1.2 μm Millipore membrane and sterilized in an autoclave at 120 ºC for 15 minutes. 25 ml Pyrex culture tubes were filled with 20 ml of the medium.

15Each month, culture tubes were transported to the field for in situ phytoplankton inoculations. Lagoon water with phytoplankton was collected and a 1 ml sample was inoculated in the tubes (cell density in the lagoon is above 1000 cells per milliliter in previous observations). The tubes for each treatment were inoculated with 0.2 ml of the mangrove extracts with the exception of treatment 1 (1 % of the total volume of cultures representing final concentrations of humic substances within the range detected in the lagoon). A 125 ml water sample from the lagoon was fixed with acetate-lugol (Throndsen, 1978) to determine the phytoplankton abundance and the species composition at the beginning of the experiment (Table 2).

Table 2. Species composition and cell density (cell ml-1) at the beginning of experiments of phytoplankton growth.

Species

May

August

October

Chaetoceros muelleri var subsalsum*

174

0

0

Thalassiosira cedarkeyensis

166

0

0

Scrippsiella sp.

6

0

0

Chaetoceros simplex

863

964

0

Cylindroteca closterium

2

2

0

Scenedesmus armatus

0

19

0

Chaetoceros subtilis var abnomis f. simplex

0

2

0

Cyclotella spp.*

0

2540

225

Skeletonema pseudocostatum

0

0

9938

Skeletonema subsalsum*

0

0

3403

Skeletonema costatum

0

0

0

Fragilaria ulna

16

8

23

Total

1227

3534

13589

* Species that dominated at the end of the experiment

16The tubes were taken to the laboratory and placed in a culture chamber (LAB-LINE) at 26 ºC with a 12/12 light-dark cycle and 9.9 µmol m-2 s-1 irradiance. All tubes were gently shaken daily and every 2 or 3 days, a drop was extracted from one tube of each treatment to monitor phytoplankton growth. We wanted to test the effect on cell density as a result of growth, so we established weekly samplings. On days 7, 14, 21, 28, 35, 42, and 49 a 1 ml sample from each tube was fixed with acetate-lugol for cell counting and species identification. This was done in a Neubauer chamber (Semina, 1978) under a light microscope (LEICA).

Statistical analysis

17A two-way repeated analysis of variance (ANOVA) was executed to test the differences between the incubating leaves and the controls (treatments), and other one to determine differences in phytoplankton growth. Differences obtained in GPP between treatments were analyzed with a nested factorial ANOVA. Factors were treatments, months, and site nested by month. All data were log10 (x+1) transformed for normalization (Zar, 1999). The Statistica ver 7.0 software was used for the analysis (StatSoft, 2004).

Results

Extract obtained from Decomposing Rhizophora Mangle Leaves

18The differences between incubated bottles with leaf litter and controls show that leaf litter decomposition produced N-NH4+ (ANOVA: F = 459.81, P < 0.001), N-NO3- (ANOVA: F = 55.47, P < 0.001), and FPAS (ANOVA: F = 459.81, P < 0.001). P-PO43- concentration in the extract was not significantly different from the control (ANOVA: F = 4.8, P = 0.09).

19During the first two days of decomposition there was a rapid increase in N-NH4+, N-NO3-, and FPAS concentrations (Figs. 2a, 2b, and 2d). After the 5th day there were changes in the nitrogen compounds concentration, but tendency in bottles with leaf litter was to decrease (Figs. 2a, 2b). Variation in P-PO43- concentration did not differ over time (Fig. 2c). Also, after the 5th day, FPAS concentration increased slowly in the bottles with leaf litter until the end of the experiment (Fig. 2d).

Figure 2. Mean concentration of a) N-NH4+, b) N-NO3-, c) P-PO43- and d) FPAS released from 1 g of leaf litter decomposition in 1 l of water over time. Dotted line represents the leaf litter treatment; continuous line represents the control without litter. Whiskers are 95 % confidence intervals

Figure 2. Mean concentration of a) N-NH4+, b) N-NO3-, c) P-PO43- and d) FPAS released from 1 g of leaf litter decomposition in 1 l of water over time. Dotted line represents the leaf litter treatment; continuous line represents the control without litter. Whiskers are 95 % confidence intervals

The effect on primary productivity

20The different treatments had an effect on GPP (ANOVA: F = 12.52, P < 0.001). However significant differences in the effect of treatments were only detected in the experiments carried out in May and August.

21In May, treatment 5 (extract from day 45) inhibited PP compared to controls and to the extracts of leaf litter from days 2 and 10 (P-values < 0.001) at site 1 (Fig. 3). At site 2 no significant differences were detected. In August, although no significant effect was detected at site 1, treatment 3 (extract from day 2) stimulated PP. At site 2, the effect of treatment 3 differed significantly from treatment 5 (P = 0.01). These differences resulted from treatment 3 stimulating PP while treatment 5 inhibited it (Fig. 3). In October there were no differences among treatments within the sites, but treatment 3 showed stimulation in GPP at site 2 (Fig. 3).

Figure 3. Mean gross primary productivity for two sites on Sontecomapan Lagoon for three different months in 2003. Treatments tested are given in table 1. Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.

Figure 3. Mean gross primary productivity for two sites on Sontecomapan Lagoon for three different months in 2003. Treatments tested are given in table 1. Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.

The effect on phytoplankton growth

Figure 4. Mean cell density during phytoplankton growth: a) Chaetoceros muelleri var subsalsum, b) Cyclotella spp., and c) Skeletonema subsalsum subjected to different treatments (see Table 1). Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.

Figure 4. Mean cell density during phytoplankton growth: a) Chaetoceros muelleri var subsalsum, b) Cyclotella spp., and c) Skeletonema subsalsum subjected to different treatments (see Table 1). Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.

22All phytoplankton cultures began with at least 4 species in each month evaluated (Table 2), but at the end of the experiments all cultures were dominated by only one species (or genus). In May, Chaetoceros muelleri var subsalsum (Lemmermann) J.R.Johansen & Rushforth accounted for more than 80 % of total cell density, in August, a complex of two Cyclotella species (C. cryptica and C. meneghiniana) accounted for more than 95 % and in October, Skeletonema subsalsum accounted for more than 92 %. The rest of the species did not survive or did not increase cell density significantly, so we only present the treatments effect on the dominant species growth.

23On the experiment conducted in May, treatments had effects on the cell density of Chaetoceros muelleri var subsalsum (ANOVA: F= 4.46, P = 0.01) and cell density was different among days (ANOVA: F= 57.24, P < 0.001). However, differences among treatments did not depend on the day of cell evaluation (ANOVA: F= 0.69, P = 0.84). Treatment 5 (extract of leaf litter obtained on day 45) inhibited growth compared to treatments 1 (control), 2 and 4 (P < 0.05). Cell density under this treatment was always lower than the numbers recorded through the rest of treatments (Fig. 4a). Although the cell density in treatment 3 was maintained below the treatments growth 1, 2 and 4, the difference was not significant (P values > 0.05).

24In the August experiment, the effect of the treatments on the cell density of Cyclotella spp. depended on the day on which the effect was evaluated (ANOVA: treatments: F= 3.11, P = 0.05; day: F= 47.1, P < 0.001; treatment x day: F= 3.10, P < 0.001). Differences in cell density were detected on day 14, when treatment 5 inhibited the growth compared to treatments 1, 2, and 4 (P values < 0.02). Even though no significant differences were detected on the following days, the treatments with leaf litter extract had lower cell densities than the controls (treatment 1 and 2) after day 35 (Fig 4b).

25In October, treatments did not significantly affect the Skeletonema subsalsum cell density (ANOVA: F= 2.59, P = 0.09) and this did not depend on the day (ANOVA: F= 0.36, P = 0.99). In spite of this, on day 42 cell density in treatment 3 (extract from day 2) was higher than in treatments 1 and 2 (controls). On day 49, cell density in treatments 3 and 4 was also higher (Fig. 4c). Cell density in treatment 5 (extract from day 45) was always lower than that the rest.

Discussion

26Extract obtained from decomposing Rhizophora mangle leaves, showed that leaching is a very important process during the first phase of degradation. Leaching has been identified as the main way nutrients are released during the early stages of decomposition (Davis III et al., 2003). The high concentration of N compounds rapidly recorded during this experiment (on day 2) show that a quick mineralization occurred, therefore microbial action was important during the decomposition process (Cundell et al., 1979). The concentration of FPAS was the result of leaching, which went on during the entire decomposition process. Although FPAS comprise different phenolic compounds (APHA, 1998), it is indicative of high tannins concentrations in the leaf mangrove released into the water. The P-PO43- dynamics could not be attributed to the decomposing litter as our control had similar concentrations however, varying P-PO43 concentrations suggested that this nutrient-was used by microbial activity through accumulation in litter or rapid recycling (Davis III et al., 2003; Gürel et al., 2005).

27Effects on primary productivity resulted in both stimulatory and inhibitory effects depending on the concentrations of extracts, thus indicating that mangrove leachate is a mixture of stimulatory and inhibitory substances as well. A stimulatory effect in PP using runoff from mangrove forest has been observed at Términos Lagoon (Rivera-Monroy et al., 1998), but in high quantities the PP is inhibited. Similar responses have been found in experiments on dinoflagellates and diatoms photosynthetic activity (Prakash & Rashid 1968; Prakash et al., 1973), the stimulatory effect may be associated to moderate concentration of humic substances, whereas the inhibitory effect of humic substances contained in water with a high concentration of organic matter can be attributed to their ability to chelate trace metals and phosphate (Jackson & Hecky 1980), or by increasing toxicity through stimulating absorption of heavy metals such as lead, as demonstrated experimentally by Sánchez-Marín & Beiras (2014).

28In addition, the stimulatory-inhibitory effect detected in PP experiments suggests that the metabolism of the phytoplankton species present during the months when the experiments were carried out did affect the responses (Table 2). Each species has a different threshold for carrying out biological functions such as photosynthetic activity and growth (Bonilla et al., 1998). The results of the PP experiments indicate that in May the phytoplankton community was composed of species sensitive to high concentrations of FPAS, which inhibited PP. In August, species were more sensitive to the addition of the nutrients that stimulated PP and depressed it when high concentration of FPAS occurred. In October species were tolerant to high concentrations of FPAS.

29The effect on phytoplankton growth showed that the species composition was important in the response; the only significant effect (growth suppression) was detected for the extract with a high FPAS concentration. The species responses indicated that Chaetoceros muelleri var subsalsum is more sensitive to high FPAS concentrations than Cyclotella spp (complex with C. cryptica, C. meneghiniana) or Skeletonema subsalsum. Cyclotella spp. was sensitive to high FPAS concentrations in its early growth stage, but later it was able to tolerate them. The S.subsalsum growth was not affected significantly by any treatment, but its positive response in treatments 3 and 4 indicate that this species might be able to tolerate moderate concentrations of FPAS. These responses support the idea that tolerance to organic compounds in natural systems can determine the dynamics of phytoplankton communities (Herrera-Silveira & Ramírez-Ramírez, 1996; Aké-Castillo & Vázquez, 2008).

30The results of this study demonstrate the effects of mangrove extracts on two different metabolic functions acting at two different time scales: photosynthetic rate in the short term, and growth in the mid term. Photosynthetic activity is a basic function that determines growth, so the stimulatory and inhibitory effects on this process are reflected in the species’ growth. Extracts of leaf litter can enhance PP by supplying nutrients, but if the FPAS concentration is too high there is no stimulatory effect and growth can be stopped. The negative effect of the extract on PP in May decreased the growth of Chaetoceros. The antagonistic stimulatory and inhibitory effect on PP may be reflected in the adjustment of Cyclotella’s metabolism observed during its growth in August. The lack of a significant effect on PP in October may reflect the lack of significant effect on the S. subsalsum growth. Although all the responses were observed in the diatom group, other microalgae are known to respond in a similar way (Prakash & Rashid, 1968; Heil, 2005; Sánchez-Marín & Beiras, 2014).

31These results support the observations made during a one-year study of phytoplankton dynamics in Sontecomapan Lagoon, where C.cryptica and C. meneghiniana were associated with a low FPAS concentrations gradient, whereas S.subsalsum was associated with moderate FPAS concentrations (Aké-Castillo & Vázquez, 2008). Although C.muelleri var subsalsum did not account for more than 3 % of the total cell density in that study, this species can potentially grow in moderate FPAS concentrations.

Acknowledgements

32Instituto de Ecología, A. C. (projects 902-17 and 902-11-280) and CONACYT (32732- Tand scholarship 90031) for providing financial support. Ariadna Martínez Virués, Olivia Hernández and Ricardo Madrigal helped with the experiment in the field.

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Table des illustrations

Titre Figure 1. Sontecomapan Lagoon’s location indicating primary productivity experiments sites.
URL http://books.openedition.org/irdeditions/docannexe/image/35489/img-1.jpg
Fichier image/jpeg, 19k
Titre Table 1. Characteristics of extracts obtained from decomposing mangrove leaf litter and used in experiments on primary productivity and phytoplankton growth.
Légende WL: water lagoon from each month of experiment (standard deviation)
URL http://books.openedition.org/irdeditions/docannexe/image/35489/img-2.jpg
Fichier image/jpeg, 32k
Titre Figure 2. Mean concentration of a) N-NH4+, b) N-NO3-, c) P-PO43- and d) FPAS released from 1 g of leaf litter decomposition in 1 l of water over time. Dotted line represents the leaf litter treatment; continuous line represents the control without litter. Whiskers are 95 % confidence intervals
URL http://books.openedition.org/irdeditions/docannexe/image/35489/img-3.jpg
Fichier image/jpeg, 28k
Titre Figure 3. Mean gross primary productivity for two sites on Sontecomapan Lagoon for three different months in 2003. Treatments tested are given in table 1. Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.
URL http://books.openedition.org/irdeditions/docannexe/image/35489/img-4.jpg
Fichier image/jpeg, 18k
Titre Figure 4. Mean cell density during phytoplankton growth: a) Chaetoceros muelleri var subsalsum, b) Cyclotella spp., and c) Skeletonema subsalsum subjected to different treatments (see Table 1). Whiskers are 95 % confidence intervals. Empty circles are treatment 1 (control), squares are treatment 2 (control), the rhombus treatment 3, triangles are treatment 4, and the filled circles treatment 5.
URL http://books.openedition.org/irdeditions/docannexe/image/35489/img-5.jpg
Fichier image/jpeg, 40k

Auteurs

Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana. Calle Hidalgo 617 Col. Río Jamapa, C. P. 94290, Boca del Río, Veracruz, México. Phone and Fax: +52 229 956 70 70,

Ecología Funcional, Instituto de Ecología, A. C., Carretera Antigua a Coatepec No. 351, Congregación el Haya, 91070, Xalapa, Veracruz, México.

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