Trophic Conditions and Stoichiometric Nutrient ...

PII: S0025-326X(99)00225-8

Marine Pollution Bulletin Vol. 40, No. 4, pp. 331±339, 2000 Ó 2000 Elsevier Science Ltd. All rights reserved Printed in Great Britain 0025-326X/00 $ - see front matter

Trophic Conditions and Stoichiometric Nutrient Balance in Subtropical Waters In¯uenced by Municipal Sewage Euents in Mazatl an Bay (SE Gulf of California) ROSALBA ALONSO-RODRIGUEZ , FEDERICO PAEZ-OSUNAà* and ROBERTO CORTES-ALTAMIRANOà Programa de Posgrado en Ciencias del Mar y Limnologõa, Estaci on Mazatl an, Universidad Nacional Aut onoma de M exico, Mazatl an Sinaloa, Mexico àEstaci on Mazatl an, Instituto de Ciencias del Mar y Limnologõa, Universidad Nacional Aut onoma de M exico, Apdo. Postal 811, 82000 Mazatl an Sinaloa, Mexico

This work presents results of a study carried out between February 1995 and August 1996, on the trophic state of coastal waters in¯uenced by a sewage outfall in Mazatlan Bay. Dissolved nutrients (ammonia, nitrate, nitrite, total inorganic nitrogen, reactive silicate and inorganic phosphate) and phytoplankton were used as parameters. The relative abundance by phytoplanktonic group changed in the dierent sites, in some sites (monthly sampled) bacillariophyte was the best-represented group with abundance ca. 70%. In additional sites around outfall and where red tides blooms occurred, this group was lower representation on the phytoplanktonic community. The application of two trophic indices based on nutrient concentrations corroborated along with the Shannon± Wiener diversity index indicates that Mazatl an Bay can be regarded as a predominantly eutrophic system. Additionally, the stoichiometric balance criterion in all selected sites con®rmed that the mean ratio for the nutrients calculated does not reach the Red®eld ratio Si:N:P of 16:16:1. Ó 2000 Elsevier Science Ltd. All rights reserved. Keywords: red tides; phytoplankton; nutrients; trophic state; Mazatlan Bay; Gulf of California. Mazatlan Bay is an open subtropical coastal embayment located at the south-east of the Gulf of California (Fig. 1). Mazatlan Bay is in¯uenced in summer by tropical water from the south and in winter by sporadic windinduced upwelling (Mee et al., 1984). The Bay receives *Corresponding author. Tel.: +69-852-845; fax: +69-826-133. E-mail address: [email protected]

untreated sewage and eventually primary treated sewage (Table 1) mainly from the south portion and from the port. Depending on the season about 380±450 000 residents in Mazatlan city generate ca. 1700 l sÿ1 of raw sewage (Anonymous, 1997). Although the development rate in Mazatlan Bay has been relatively moderate, the domestic and industrial euents as in other countries have brought concerns about the possible eects on the coastal ecosystems. Continuous studies during the last twenty years in Mazatlan Bay (Cortes-Altamirano et al., 1999) have shown that the frequency of the red tides exhibit a tendency to increase in the time, in the last decade, close to 60% of the blooms have been recorded. Similarly, cases of Paralytic Shell®sh Poisoning (PSP) by bivalve mollusks consumption have been recorded eventually in the Mazatlan population (Mee et al., 1986). Eutrophication is considered the manifestation of nutrient-enhanced primary productivity, all trophic state classi®cations are based on arbitrary divisions of continuum. For marine ecosystems, no speci®c criteria have yet become established (Jingzhong et al., 1985). State eutrophic is enrichment of nutrients or organic matter associated to presence of noxious phytoplankton, while state oligotrophic is the absence of measurable concentrations of a nutrient. State mesotrophic in marine ecosystem is attributable to a intermediate state related to nutrient concentration and phytoplanktonic growth (Ignatiades et al., 1992). This work aims to assess the trophic state in a coastal environment in¯uenced predominantly by domestic sewage applying four dierent approaches, i.e., two conventional nutrient scales, a stoichiometric balance and the Shannon±Wiener diversity index. 331

Marine Pollution Bulletin

Fig. 1 Location of the study area and collection sites. Filled circles corresponds to sites 1, 2 and 3; ®lled stars at stations in site around sewage outfall: A1, B1, C1, D1, E1 and F1, close to shoreline; stations A2, B2, C2, D2, E2, and F2 are located at 1 km distance. TABLE 1 Sewage outfall characteristics in Mazatl an Bay. Euent treatment Lengtha (m) Diuser lengtha (m) Capacityb (l sÿ1 ) Discharge receivedc (l sÿ1 ) Operation timea (y) a b c

Primary 700 150 650 1500±2000 14

Mendez and Rivas (1995). Anonymous (1997). Estimated in this study.

Materials and Methods The study area covers the south portion of Mazatlan Bay, and includes four selected sites (Fig. 1): Site 1 that represents a point close (0.5 km) to the shoreline and apparently more in¯uenced by the sewage outfall than site 2, which represents a point away (2.3 km) from the shoreline. Site 3 was selected simply to sample red tide 332

blooms present during the study period (February 1995± August 1996). Additionally one site with a group of six transects (A, B, C, D, E and F) and 12 stations around the municipal sewage outfall was selected. Adjacent to transect A, the mouth of Urõas Estuary is located, which includes Mazatlan harbor; it is a vertically mixed water body (salinity range 25.8±38.4) with an average mixed tidal amplitude of 1.5 m and water velocities of 0±0.5 msÿ1 (Paez-Osuna et al., 1990). Water samples were collected monthly in sites 1 and 2 (Fig. 1) from February 1995 to August 1996. Sampling at the stations around the municipal outfall was carried out only at dry (11 March 1996) and rainy (16 August 1996) season. Additionally, three group of samples during red tide events were collected in site 3 on 22 February, 5 March and 19 August of 1996. All samples were collected in the morning (9.00±11.00 h). A 3-l Van Dorn horizontal bottle was used to collect water samples in the surface (0.5 m of depth) and in the

Volume 40/Number 4/April 2000

bottom (10 m). Each sample was divided into clean containers as follows: (1) water ®ltered through Whatmann GF/C ®lters to determine dissolved nutrients and salinity; (2) four aliquots to analyse ammonia by the method of standard addition, were ®xed in situ; (3) a BOD bottle for dissolved oxygen measurements; (4) two pre-ashed and weighed GF/C glass ®lters to measure suspended solids and suspended organic matter; and (5) 300 ml of un®ltered water for the phytoplankton analysis. Excepting temperature, which was measured in the ®eld, all samples were carried immediately in coolers to the laboratory for analysis. Water samples for nutrients were stored refrigerated (4°C) until analysis after an addition of 20 lg mlÿ1 HgCl2 0.4%. Analyses were done with the methods described by Grassho et al. (1983), more details on the methodology are given in AlonsoRodrõguez (1998). The qualitative and quantitative phytoplankton analyses were based in techniques described by Uterm ol (1958). The identi®cation of species was done considering general manuals (Balech, 1974, 1988; Tomas, 1993; Licea et al. 1995; Moreno et al., 1996), previous studies in the Gulf of California (Cupp, 1943; Hern andez-Becerril, 1987, 1988a,b) and annual studies in the area (Rojas-Trejo, 1984; Priego, 1985; Caballasi-Flores, 1985). The speci®c diversity estimated by Shannon± Wiener index was evaluated considering random samples drawn from a large community in which the number of species is known (Pielou, 1966). The general equation is: H0 ÿ

k X pi log2 pi ; i1

where k is the number of species in the sample and pi is the proportion of total sample belonging to the ith species (Krebs, 1989). The data processing was made with software for personal computers (Microsoft Excel 97, Statistica 5.0). To determine the trophic state in the area, a concentration scale proposed by Ignatiades et al. (1992) data for scaling was adopted in Mazatl an Bay into oligotrophic ( 1:68 lg at lÿ1 DIN) water types. The procedure followed was the application of the frequency distribution analysis to transformed data and development of nutrient concentration scales on the basis of probabilistic parameters. Due to its universal validity to identify and classify mass waters rich in variable nutrient concentrations, this scale has ranges at 90%, 95% and 99% of con®dence limit. Data were separated considering the stations of each one of the sites selected and using the 95% con®dence limit (Table 2). A third approach employed to determine the trophic state in the study area consisted in the nutrient or

trophic index proposed by Karydis et al. (1983). This index is speci®c for each nutrient and sensitive to pressure by eutrophication, it is given by I

C log A; C ÿ log x

where I is the trophic index, C the logarithm of the total nutrient load, x the nutrient total concentration in certain station and A is the number of stations. The scale is: I > 5 an eutrophic environment, 3 < I < 5 is a mesotrophic state and I < 3 an oligotrophic state. It was applied during the sampling period (9 February 1995±14 August 1996) in sites 1 and 2 (Table 3); in winter and summer monitoring (5±11 March, 14±19 August 1996) in all of the collection sites (Table 4). In addition, standard deviation (SD) of temperature over the water column from 0 to 10 m was used as simple index of thermal strati®cation (Valdes and Moral, 1988). One unit of SD is equivalent to 2.0°C of thermal dierence in the water column. Finally, in a fourth approach the nutrient balances were elaborated considering the Red®eld ratio criterion Si:N:P (16:16:1) (Justic et al., 1995). It was carried out separating the red tide data (site 3) by each sampling period, and the rest were presented by site and strategy of sampling (Table 5).

Results and Discussion Seasonal variations of thermal strati®cation in the sites 1 and 2 were observed, showed higher in the beginning of spring to reach minimum in winter when the column of water is mixed due to the presence of NW predominant winds. In each station were determined the concentrations of total suspended solids (TSS > 0.45 lm) found to vary between 1.0 and 50.6 mg lÿ1 , and more often 8±15 mg lÿ1 (Alonso-Rodrõguez, 1998). Considering readings of Secchi disk, obtained during 1990±1991 (Flores-Verdugo et al., 1991), it is estimated that the mean light extinction coecient (k0 ) ranges from 0.14 to 1.1 mÿ1 . Under such conditions, is dicult that in Mazatlan Bay waters, light-limitation could be an important regulator of phytoplankton production. In all the samplings, the totality of nutrients, except nitrite, corresponded to an eutrophic state according to the nutrient concentration scale of Ignatiades et al. (1992) (Table 2). The nitrite levels showed mesotrophic water for sites 1 and 2, an oligotrophic water type for site 3 and the samples collected around the sewage outfall during the rainy season. Mazatlan Bay receives the nutrient inputs associated to tropical water from the south during summer and in spring and winter from wind-induced upwelling (Roden, 1964; Badan-Dang on et al., 1985). Additionally, the Bay receives the nutrient inputs associated to discharges of untreated and primary treated sewage. Considering the population equivalent representative of the region 6 g nitrogen and 1.4 g phosphorus per day for the municipal 333

Marine Pollution Bulletin TABLE 2 Nutrient mean concentrations (lg at lÿ1 ) in the study sites and their classi®cation in according to con®dence limit 95% (l to l 2r) of the nutrient scale (Ignatiades et al., 1992) for dierent water types. P±PO4 (lg at P lÿ1 ), N±NO3 , N±NO2 , N±NH3 and total inorganic N (lg at N lÿ1 ), S±SiO4 (lg at Si lÿ1 ). Collection site

Number of data

Nutrient

Mean (range ) S.D.

Site 1 Site 1 Site 1 Site 1 Site 1 Site 1 Site 2 Site 2 Site 2 Site 2 Site 2 Site 2 Site 3 Site 3 Site 3 Site 3 Site 3 Site 3 Dry season Dry season Dry season Dry season Dry season Dry season Rainy season Rainy season Rainy season Rainy season Rainy season Rainy season

57 57 57 57 57 57 56 56 56 56 56 56 9 9 9 9 9 9 24 24 24 24 24 24 24 24 24 24 24 24

P±PO4 N±NO3 N±NO2 N±NH3 N(N±NH3 +N±NO3 +N±NO2 ) S±SiO4 P±PO4 N±NO3 N±NO2 N±NH3 N(N±NH3 +N±NO3 +N±NO2 ) S±SiO4 P±PO4 N±NO3 N±NO2 N±NH3 N(N±NH3 +N±NO3 +N±NO2 ) S±SiO4 P±PO4 N±NO3 N±NO2 N±NH3 N(N±NH3 +N±NO3 +N±NO2 ) S±SiO4 P±PO4 N±NO3 N±NO2 N±NH3 N(N±NH3 +N±NO3 +N±NO2 ) S±SiO4

0.89(0.14±2.34) 0.49 2.99(0.30±35.74) 6.31 0.20(0.05±1.76) 0.30 4.65(0.50±18.71) 5.18 7.84(0.85±39.17) 7.86 5.11(0.50±19.41) 4.58 0.87(0.09±2.94) 0.56 2.32(0.30±29.52) 5.24 0.18(0.05±1.58) 0.28 5.26(0.50±28.62) 6.70 7.76(0.85±34.45) 7.94 4.85(0.50±18.50) 4.52 0.94(0.13±3.58) 0.98 0.93(0.30±3.16) 1.02 0.12(0.05±0.40) 0.10 3.75(0.50±8.79) 3.30 4.80(1.14±11.13) 3.57 7.49(3.61±11.84) 3.28 1.88(0.69±10.97) 2.18 4.58(0.30±11.86) 3.64 0.41(0.05±0.94) 0.28 10.16(0.50±119.84) 28.19 15.15(0.85±124.27) 28.30 4.99(0.50±16.62) 3.66 0.65(0.20±2.50) 0.46 0.75(0.30±3.80) 0.74 0.06(0.05±0.20) 0.03 4.58(0.50±57.40) 11.65 5.39(0.85±61.30) 12.32 11.40(0.50±20.20) 3.84

Classi®cation Eutrophic Eutrophic Mesotrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Mesotrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Oligotrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Eutrophic Oligotrophic Eutrophic Eutrophic Eutrophic

TABLE 3 Trophic Index I, sites 1 and 2 (9th February 1995±16th August 1996). Nutrients

Sites

1 2

Ammonia

Nitrate

Nitrite

Total Inorg. N

Silicate

Phosphate

Eutrophic Eutrophic

Eutrophic Mesotrophic

Mesotrophic Mesotrophic

Eutrophic Eutrophic

Eutrophic Oligotrophic

Oligotrophic Oligotrophic

sewage (Paez-Osuna et al., 1999), the nutrient load gives an N:P ratio of 9.5. Therefore, if the municipal load is more signi®cant, in accordance to the population growth, it is not surprising that the mean ratio for nutrients calculated in the bay waters does not reach the Red®eld ratio Si:N:P of 16:16:1. The thermal strati®cation index (TSI), results lower for site 3 in red tide events and rainy season when tropical storms are present, medium for sites 1 and 2 for complete period study. This index was higher for dry season, in the winter, due to major temperature on super®cial layer than discharged in this zone. Coincidentally in the winter is presented the maximum concentrations of nitrate and phosphate, therefore Si:N and Si P ratios are lowest (Table 5). Except for the red tide bloom of August 1996, stoichiometric balance criterion in all cases con®rmed that the mean ratio calcu334

lated did not reach the Red®eld ratio Si:N:P 16:16:1. Considering 1 P atom, the proportion Si:N is low for most of the sites, except in the waters present during the red tide event of 19 August 1996, when ®gures of Si:N were higher than Red®eld ratio. The ratio of nutrients N:P based on 16 Si atoms was also low in all cases. Distance between Red®eld ratio and nutrient proportion in the waters of Mazatlan Bay is shown in Fig. 2. Red®eld ratio deviations could de®ne eutrophic conditions as a biolimiting factor for diatoms and other phytoplankton groups, generating harmful phytoplankton blooms (Ryther and Dustan, 1971; Ocer and Ryther, 1980; Smayda, 1990). Changes in the proportions of Si, N and P in nutrient loads may aect coastal phytoplankton communities (Justic et al., 1995). The atomic Si:N:P ratio of marine diatoms is about 16:16:1, these organisms are the main

Volume 40/Number 4/April 2000 TABLE 4 Trophic Index I, sites 1, 2, 3 and site around sewage monitoring on dry (5±11 March) and rainy (14±19 August) seasons in stations A, B, C, D, E, F. Site/station 1 2 3 A1 A2 B1 B2 C1 C2 D1 D2 E1 E2 F1 F2 *

Ammonia

Nitrate

Nitrite

Total Inor. N

Silicate

Phosphate

Mesotrophic Mesotrophic Mesotrophic Mesotrophic Oligotrophic Oligotrophic Oligotrophic Mesotrophic Oligotrophic Eutrophic Oligotrophic Eutrophic Mesotrophic Mesotrophic Oligotrophic

Mesotrophic Oligotrophic Oligotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Oligotrophic Mesotrophic Mesotrophic Oligotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic

Oligotrophic Oligotrophic Oligotrophic Mesotrophic Mesotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic Oligotrophic

Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Eutrophic Oligotrophic Eutrophic Mesotrophic Mesotrophic Mesotrophic

Mesotrophic Oligotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic

Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic Oligotrophic Mesotrophic Mesotrophic Eutrophic Oligotrophic Mesotrophic Mesotrophic Mesotrophic Mesotrophic

Odd stations or odd sub-index are close to the shoreline, the even stations are at 1 km of distance of shoreline. TABLE 5

Index of thermal strati®cation (ITS) and stoichiometric nutrient balance for the dierent sites in Mazatl an Bay. Dissolved nutrient concentrations (lM), total inorganic nitrogen (N), reactive phosphorus (P) and reactive silica (Si).a

TSI N P Si

x SD x SD x SD x S

Ratio

R

Si:N N:P Si:P

1 16 16

Nutrient

R

N P

16 1

Nutrient

R

Si N

16 16

Site 1

Site 2

Site 3

Dry season

Rainy season

9-2-95

12-8-96

22-2-96

5-3-96

19-8-96

22-3-96

19-8-99

n 57

n 56

n3

n3

n3

n 24

n 24

0.74 0.65 7.84 7.86 0.89 0.49 5.11 4.58

0.79 0.68 7.76 7.94 0.87 0.56 4.85 4.52

0.56 ± 4.56 5.69 1.75 1.59 6.41 1.56

0.15 ± 5.91 1.55 0.83 0.08 4.07 0.51

0.06 ± 4.04 4.43 0.21 0.09 10.54 1.84

1.29 0.54 15.15 28.30 1.88 2.18 4.99 3.66

0.12 0.07 5.39 12.32 0.65 0.46 11.40 3.84

2.61 19.24 50.19

0.33 8.06 2.65

2.12 8.29 17.54

3 0

0 0

3 8

18 8

Average atomic ratio 0.65 8.81 5.74

0.63 8.92 5.57

1.41 2.61 3.66

0.69 7.12 4.90

Nutrient atom number on base 16 silica atom 2 0

2 0

1 0

1 0

0 0

Nutrient atom number on base one phosphate atom 6 9

6 9

constituents of phytoplankton in Mazatl an Bay, when available nutrient levels are sucient (Brzezinski, 1985). Ocer and Ryther (1980) hypothesized that decreasing Si:N ratio may exacerbate eutrophication by reducing the potential for diatom growth, in favour of noxious ¯agellates. Several studies have clearly shown that nutrient ratio can be the most important regulator of the phytoplanktonic communities, particularly, in terms of species selection (Hodgkiss and Ho, 1997). Hodgkiss and Chan (1987) and Chan and Hodgkiss (1987) found a decline in N:P ratio in Tolo Harbour, Hong Kong, accordingly with a change in the phytoplankton commu-

4 3

5 7

50 19

nity, with a substitution of diatoms by red tide organisms. Smayda (1990) indicated how long-term declines in the Si:N and Si:P ratios in the Baltic, North and Black Seas in response to nitri®cation, are accompanied by increased blooms of non-siliceous phytoplanktonic communities. This same author not only evidenced to have blooms of non-silica requiring groups increased during this same period, but they have even replaced the diatoms as the dominant biomass group in some areas. The results obtained from the application of Shannon±Wiener diversity index using frequency values, for 335


Fig. 2 Mean atomic ratios of dissolved inorganic nitrogen (N), phosphorus (P) and silica (Si) in the dierent sites of study with reference to Red®eld ratio 16:16:1; sites 1, 2 and 3 (February, March and August); dry season and rainy season.

Mazatlan Bay are shown in Fig. 3. Frequency percentage in site 1 (Fig. 3(a)) for 2.7±4.5 was 79%. In site 2 (Fig. 3(b)) for 2.7±4.5 was 83%. In site 3 (Fig. 3(c)) for 0±2.7, was 88%. Site 3 corresponds to low diversity index, and few dominant species, characteristic of red tide events. The percentage for the waters around the sewage outfall in the dry season (Fig. 3(d)) for 2.5±3.3 was 58%. During the rainy season (Fig. 3(e)) in these same waters, 87% of diversity index was 2.1±2.7. Shannon±Wiener diversity index analyses in the waters at sites 1 and 2, are close to upper empiric boundary of 5, as a possible consequence of a relationship between phytoplankton and turbulence in the water column (Margalef, 1978): diatoms are dominant in turbulent water, rich in nutrients, and dino¯agellates constitute the bulk of the population in strati®ed waters, poor in nutrients (Gaxiola-Castro et al., 1995). Gilmartin and Revelante (1978) studied 15 dierent coastal areas in the Gulf of California, in the summer of 1972, they found that the Shannon±Wiener diversity index was high for the Bays in the west portion. Los Angeles and Conception Bays showed oligotrophic waters with H 0 of 3.4±3.8, and the rest of the lagoons were H 0 values of 0.4±4.2. The 0.4 corresponded to Urõas Estuary, where a bloom of Trichodesmium hildebrantii and Skeletonema costatum was present and the phosphate level was relatively elevated (0.93 lM). In other studies H 0 values from 1.9 to 4.8 have been reported (Hernandez-Becerril, 1985) and from 3.6 to 4.9 (Atilano, 1987) for the central and south part of the Gulf. Gonzalez-L opez (1987) found H 0 from 3.8 to 4.6 in the south region of the Gulf for the spring and summer of 1984. Garate-Lizarraga et al. (1990) during spring 1986 studied the phytoplanktonic communities in the centre of the Gulf of California and found that H 0 was relatively high in most of the stations (5.0±5.9), except the value found in a station of 0.85 due to a Stephanopyxis palmeriana bloom. 336

Fig. 3 Frequency (%) of Shannon±Wiener diversity index in: (a) site 1, (b) site 2, (c) site 3, (d) dry season, (e) rainy season.

The Shannon±Wiener diversity index has been used as pollution index in diatom communities and the next scale has been proposed (Hendley, 1977): of 0±1 for high pollution, of 1±2 for moderate pollution, of 2±3 for small pollution, and of 3±4 for incipient pollution. Wu (1984) using phytoplankton as bioindicator for water quality in Taipei, Taiwan indicated that the diversity index of phytoplanktonic community was correlated in some cases with the degree of pollution. In general, the author established that the value of diversity index of a community in less polluted waters would be higher. Wu (1984), also argued that the diversity index of community is not linearly correlated with the water quality and that the N:P ratio decreases with increased eutrophication and hence decreased species diversity of community. This last explanation is congruent with the results obtained here in Mazatlan Bay, where clearly the low diversity index corresponds to sites in which red tide blooms were present. Considering the nutrient index proposed by Karydis et al. (1983) the eutrophic state was evident for ammonia and total nitrogen in sites 1 and 2, and for nitrate and silicate for site 1 near to the sewage outfall (0.5 km). The mesotrophic and oligotrophic state was evidenced with the nitrate and phosphate, respectively, in sites 1 and 2 (Table 3). In order to identify eutrophic manifestations

Volume 40/Number 4/April 2000

on the area around the municipal discharge, the odd stations that were closer stations to the sewage outfall were separated from the pair stations that were located at a distance of 1 km from the sewage outfall (Fig. 1, Table 4). From the above analysis, stations D1 and E1, constitute a `Hot Spot' regarding the level of eutrophication. This evidence that the sewage material has a major in¯uence close to the shoreline and to the outfall, which is probably due to ruptures in the outfall that discharges sewage. The relative dominance by the phytoplanktonic group changed in the dierent stations, in sites 1 and 2 bacillariophyte was sampled monthly with a relative abundance ca. 70%. In the other stations, the diatoms were of minor relevance, e.g., in site 3 where red tide blooms were present; the abundance was represented by the phototrophic ciliate Mesodinium rubrum (99.7%) during February 22, 1996; the dino¯agellata group during March 5, 1996 (99.4%, Scrippsiella trochoidea) and August 19, 1996 (41.0±58.6%, S. trochoidea and Pyramimonas sp.). In the 12 stations around the sewage outfall, the cyanophyta (43.1%) and small ¯agellate (31.0%) groups were dominant during the dry season, while in the rainy season, the abundance was mainly determined by small ¯agellates (49.9%) and cyanophyta (26.0%). The predominance of certain members of cyanophyta group may be promoted by the presence of sewage in the Mazatl an Bay waters, in this context, Shilo (1980) related to such organisms with eutrophic conditions where the dissolved organic matter is high, and dissolved oxygen is low or zero. The annual mean abundance of phytoplankton in this study was lower in comparison with previous studies (Cortes-Altamirano and Rojas-Trejo, 1981; CaballasiFlores, 1985) in Mazatl an Bay. The group most important were the diatoms with a relative abundance of ca. 70%, followed by dino¯agellate (12%) and phyto-

¯agellate (12%) groups. The rest of the groups have relative abundance lower than 3% and include the silico¯agellate, cyanophyta and euglenophyta groups. The relative abundance of the diatoms is similar between the present work and studies referred previously but in the rest of the groups it was variable. The present study constitutes the ®rst record of annual abundance of the ciliate M. rubrum (Lohmann, 1908) with an annual relative abundance of 2.5%. Systematic studies on the water quality and the nutrient load in Mazatlan Bay are not available. However, the increase of the population during the past years in Mazatlan City should be re¯ected in a higher load of nutrients to the Mazatlan Bay, which also might account for the water quality of the Bay. The trend of the water quality in terms of nutrient concentrations in Mazatlan Bay in some available data in the last twenty years is shown in Table 6. However, there is not a clear increase of the levels in most of the nutrients from such data sets, particularly, this is valid for phosphorus and nitrite. The eastern tropical Paci®c can be divided (Thomas, 1970) into nutrient-rich and nutrient-poor areas. In the nutrient-poor areas, nitrate is typically undetectable in near-surface water. In open oceanic areas in front of Mazatlan Bay, Lambourn and Devol (1995) reported data for the site 22°3000 , and 106°5000 and found nutrient mean values for the 5 and 10 m depth: ammonia 0.03 and 0.04 lM, nitrate 0.23 and 0.01 lM, nitrite 0.01 and 0.01 lM, silicate 6.95 and 10.91 lM, and phosphate 0.22 and 0.21 lM, respectively. These levels correspond more closely to nitrogen-poor waters, with exception of silicates these levels and the N:P ratio are low in comparison with the nutrient contents of Mazatlan Bay waters (Table 6). Considering an average municipal discharge of 63 m3 ÿ1 y per capita, a total nitrogen concentration of 16 mg

TABLE 6 Trends in nutrient concentrations and N:P ratios in surface waters (0±1 m depth) from Mazatl an Bay.a Year

1980±1982

1983±1984

1995±1996

a

Nutrient (lM)

Period NO2

NO3

NH4

PO4

N:P

Reference

Winter Summer Surface annual Annual 1±10 m depth

0.16 0.15 0.16 0.20

0.30 0.40 0.40 0.70

± ± ± 3.2

0.83 0.74 0.79 0.87

±(0.6) ±(0.8) ±(0.7) 4.7(1.0)

Mee et al. (1984)


0.09 0.11 0.10 ±

0.34 0.09 0.20 ±

± ± ± ±

0.19 0.32 0.26 ±

±(2.3) ±(0.6) ±(0.2) ±(±)

Garcõa-de-la-Parra (1992)


0.18 0.08 0.13 0.19

3.93 0.91 2.42 3.16

4.88 5.57 5.22 5.00

0.84 0.68 0.76 0.89

15.2(4.9) 25.9(1.5) 20.6(3.4) 17.3(3.1)

This study

±Not available; (±) Red®eld ratio calculated without ammonia.

337


lÿ1 and ammonia 5 mg N-ammonia lÿ1 (Mendez and Rivas, 1995), then the discharge estimated per capita is of 2.8 g N dayÿ1 and 0.86 g N±NH4 dayÿ1 . This ®rst ®gure is comparable to 3 g N inorganic dayÿ1 estimated through data from Mee et al. (1984) in 1982. These values are 46% lower than the average estimated for the aez-Osuna et al., 1999), which is region of 6 g N dayÿ1 (P probably because N-organic was not included in the second case or peculiar dierences among locations in the region. Other studies have reported highest wastewater concentrations from dierent coastal areas, 16±30 mg N inorganic lÿ1 (Ocer and Ryther, 1980) and 15±35 mg N-ammonia lÿ1 (Manahan, 1979; Jingzhong et al., 1985). Red tides are common in the Gulf of California, and especially frequent in some coastal localities, including Mazatlan Bay (Cortes-Altamirano and Nu~ nez-Pasten, 1992). The study of red tides has been incomplete in Mazatlan Bay with respect to a detailed identi®cation of the mechanism causing blooms. However red tides in the coastal waters of Mazatl an Bay can be examined as a consequence of the upwelling events frequently common in the region, and the cultural eutrophication. The evaluation of the trophic state based on conventional nutrient scales applied here and one diversity index, showed similar results and it is possible to conclude that Mazatlan Bay as other coastal areas subject to cultural eutrophication, has a regime predominantly of eutrophic waters. This study provides a ®rst approach to assess the load and eect of the nutrients discharged in the south portion of Mazatl an Bay on the phytoplankton communities. In practical terms is necessary (a) a knowledge of the total nutrient load, (b) a knowledge of the critical factor or factors of the assimilation capacity of the Mazatlan Bay waters. These considerations are relevant in the context of the selection of coastal management options. Finally, it is evident the need to evaluate damages to other animal communities as soon as economic loss for discharge of wastewaters in the Mazatlan Bay through long-term and systematic studies with the local or regional strategies for red tide management and eventually mitigate the problems involved. The authors thank to J. Ruelas-Inzunza for the revision of the manuscript. In the same way to A. Nu~ nez-Pasten, H. Boj orquezLeyva, G. Ramõrez-Resendiz, C. Ramõrez-J auregui, and A. Castro-delRõo for their assistance in the ®eld, laboratory, ®gures, bibliography and help in the preparation of the ®rst manuscript, respectively. Alonso-Rodrõguez, R. (1998) Ocurrencia de mareas rojas y calidad del agua en la zona sur de la bahõa de Mazatl an, Sinaloa, Mexico. Tesis de Maestrõa ICMyL. UNAM, Mexico. 165 pp., in Spanish. Anonymous (1997) Anuario Estadõstico del Estado de Sinaloa. Instituto Nacional de Estadõstica, Geografõa e Inform atica. Gobierno del Estado de Sinaloa Mexico, 402 pp., in Spanish. Atilano, M. H. M. (1987) Composici on y estructura de la comunidad del ®toplancton silõceo en el Golfo de California en Marzo de 1983. Tesis Profesional CICESE, 161 pp., in Spanish. Badan-Dang on, A., Koblinsky, C.J. and Baumgartner, T. (1985) Spring and summer in the Gulf of California: observations of surface thermal patterns. Oceanologica Acta 8, 13±22.

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Balech, E. (1974) El genero Protoperidinium Berg, 1881 (Peridinium Ehrenberg, 1831, Partim) Revisi on del Museo Argentino de Ciencias Naturales B. Rivaldavia Hidrobiologõa 1 (6), 77±126. Balech, E. (1988) Los dino¯agelados del Atl antico sudoccidental. Publicaci on. Especial Instituto Espa~ nol de Oceanografõa, Ministerio de Agricultura Pesca y Alimentaci on, Madrid, 310 pp., in Spanish. Brzezinski, M. A. (1985) The Si:C:N ratio of marine diatoms: interspeci®c variability and the eect of some environmental variables. Journal of Phycology 21, 347±357. Caballasi-Flores, P. (1985) Comparaci on ®toplanct onica de la Bahõa de Mazatl an y Estero de Urõas, Sinaloa, Mexico, 1981. Tesis Profesional. ENEP Iztacala. UNAM, 50 pp., in Spanish. Cortes-Altamirano, R. and Nu~ nez-Pasten, A. (1992) Doce a~ nos (1979± 1990) de registros de mareas rojas en la Bahõa de Mazatl an, Sin., Mexico. Anales del Instituto de Ciencias del Mar y Limnologõa 19, pp. 113±121, in Spanish. Cortes-Altamirano, R. and Rojas-Trejo, S. (1981) Variaci on estacional de las comunidades ®toplanct onicas de la bahõa de Mazatl an, Sin. Mexico. In VII Simposio Latinoamericano sobre Oceanografõa Biol ogica, 15±19 noviembre de 1981, pp. 219±239. Acapulco, Guerrero, Mexico, in Spanish. Cortes-Altamirano, R., Licea-Dur an, S. and G omez-Aguirre, S. (1999) Evidencias del aumento de microalgas nocivas en la bahõa de Mazatl an, Sin., Mexico. Memorias del VIII Congreso Latinoamericano sobre Ciencias del Mar. 17±21 Octubre 1999, Trujillo, Per u., in Spanish. Cupp, E. E. (1943) Marine plankton diatoms of the West Coast of North America. Bulletin of the Scripps Institution of Oceanography of the University of California 5(1), 1±237. Chan, B. S. S. and Hodgkiss, I. J. (1987) Phytoplankton productivity in Tolo Harbour. Asian Marine Biology 4, 79±90. Flores-Verdugo, F., Rodrõguez-Garcõa, J. and Gonz alez-Farõas, F. (1991) Variaci on espacio-temporal de la productividad primaria acu atica en la bahõa de Mazatl an, Sin. 9: 350 pp. In V. ArenasFuentes, y F. Flores-Verdugo (Coord.). Ecologõa de los manglares, productividad Acu atica y Per®l de las comunidades en ecosistemas lagunares-estuarinos de la costa noroccidental de Mexico. Parte I Ensenada del Pabell on, bahõa de Altata y bahõa de Mazatl an. Informe Tecnico DGPA (IN202389), in Spanish. G arate-Liz arraga,. I, Siqueiros-Beltrones, D. A. and Lechuga-Deveze C. H. (1990) Structure of the microphytoplankton associations of the central region of the Gulf of California in autumn 1986. Ciencias Marinas 16 (3), 131±153. Garcõa-de-la-Parra, M. L. (1992) Estimaci on de las tasas de ®jaci on de nitr ogeno atmosferico en la bahõa de Mazatl an, Sinaloa, Mexico. Tesis de Maestrõa, ICMyL. UNAM, Mexico, 166. Gaxiola-Castro, G., Garcõa-C ordova, J., Valdez-Holguin J. E. and Botello-Ruvalcaba, M. (1995) Spatial distribution of chlorophyll a and primary productivity in relation to winter physical structure in the Gulf of California. Continental Shelf Research 15 (9), 1043± 1059. Gilmartin, M. and Revelante, N. (1978) The phytoplankton characteristics of the barrier island lagoons of the Gulf of California. Estuarine, Coastal and Shelf Science 17, 599±612. Gonzalez-L opez, I. (1987) Composici on especõ®ca, diversidad, distribuci on y abundancia relativa de las diatomeas y dino¯agelados micro®toplanct onicos de aguas super®ciales de la regi on sur del Golfo de California, Mexico, durante la primavera y verano de 1984. Tesis Profesional, UABCS, 107 pp. Grassho, K., Ehrhardt, M. and Kremling, K. (1983) Methods of Seawater Analysis. Verlag Chemie 2a . Ed. 419 pp. Hendley, N. I. (1977) The species diversity index of some in-shore diatoms communities and its use in assessing the degree of pollution insult on parts of the North Coast of Cornwall. In Fourth Symposium on recent and fossil marine diatoms, ed. J. Cramme, pp. 355±378. Hern andez-Becerril, D. U. (1985) Phytoplankton structure in the Gulf of California. Ciencias Marinas 11 (2) 23±38. Hern andez-Becerril, D. U. (1987) Especies de ®toplancton tropical del Pacõ®co Mexicano. I. Diatomeas y Silico¯agelados. Revista Latinoamericana de Microbiologõa 29, 413±426, in Spanish. Hern andez-Becerril, D. U. (1988a) Especies del ®toplancton tropical del Pacõ®co Mexicano. II. Dino¯agelados y cianobacterias. Revista Latinoamericana de Microbiologõa 30, 187±196, in Spanish. Hern andez-Becerril, D. U. (1988b) Planktonic dino¯agellates (except Ceratium and Protoperidinium) from the Gulf of California and coast of Baja California. Botanica Marina 31, 423±435.

Volume 40/Number 4/April 2000 Hodgkiss, I. J. and Ho, K. C. (1997) Are changes N:P ratios in coastal waters the key to increased red tide blooms? Hydrobiologia 352, 141±147. Hodgkiss, I. J. and Chan, B. S. S. (1987) Phytoplankton dynamics in Tolo Harbour. Asian Marine Biology 4, 103±112. Ignatiades, L., Karydis, M. and Vonatsou, P. (1992) A possible method for evaluating oligotrophy and eutrophication based on nutrient concentration scales. Marine Pollution Bulletin 24, 238±243. Jingzhong, Z., Liping, D. and Baoping, Q. (1985) Preliminary studies on eutrophication and red tide problems in Bohai Bay. Hydrobiologia 127, 27±30. Justic, D., Rabalais, N. and Turner, E. (1995) Stoichiometric nutrient balance and origin of coastal eutrophication. Marine Pollution Bulletin 30 (1), 41±46. Karydis, M., Ignatiades L. and Moshopoulou, N. (1983) An index associated with nutrient eutrophication in the marine environment. Estuarine, Coastal and Shelf Science 16, 339±344. Krebs, C. J. (1989) Species diversity measures. In Ecological Methodology, ed. Harper y Row, pp. 329±370. New York. Lambourn, D. L. and Devol, H. A. (1995) Special report N° 12 Water column and porewater data from the mexican shelf and slope: cruise TTAN of the R/V New Horizon. School of Oceanography. College of Ocean and Fishery Sciences University of Washington 98195, 31 pp. Licea, S., Moreno, J. L., Santoyo, H. and Figueroa, G. (1995) Dino¯ageladas del Golfo de California. Universidad Aut onoma de Baja California Sur, SEP-FOMES PROMARCO. Mexico, 155 pp., in Spanish. Lohmann, H. (1908) Untersuchungen zur festsellung des vollst andingen Gehaltes des Meeres an Plankton. Wiss Meeesuntersuch 10, 129±370. Manahan, S. E. (1979) Environmental Chemistry, 490 pp. Willard Grant Press, Boston, Massachusetts. Margalef, R. (1978) Life-forms of phytoplankton as survival alternatives in an unstable environment. Oceanologica Acta 1, 493±509. Mee, L. D., Cortes-Altamirano, R. and Garcõa-de-la-Parra, L. M. (1984) Di-nitrogen ®xation in a eutrophic tropical Bay. Estuarine, Coastal and Shelf Science 19, 477±483. Mee, L. D., Espinosa, M. and Dõaz, G. (1986) Paralytic shell®sh poisoning with a Gymnodinium catenatum red tide on the Paci®c coast of Mexico. Marine Environmental Research 19, 77±92. Mendez, G. E. and Rivas, M. A. M. (1995) Programa de prevenci on, control y mejoramiento del medio ambiente acu atico. Planta de tratamiento del Crest on. Informe Tecnico. Instituto Tecnol ogico de Mar. Mazatlan, Sinaloa, in Spanish. Moreno, J. L., Licea, S. and Santoyo, H. (1996) Diatomeas. Universidad Aut onoma de Baja California Sur, SEP-FOMES PROMARCO. Mexico, 272 pp, in Spanish.

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