Phytoplankton response to nutrient runoff in a large lagoon system in the Gulf of California

Respuesta del fitoplancton al aporte de nutrientes en un sistema lagunar del Golfo de California

Aída Martínez-López¹, Diana Escobedo-Urías², Amada Reyes-Salinas¹ and Ma. Teresa Hernández-Real²

¹ Laboratorio de Fitoplancton, Centro Interdisciplinario de Ciencias Marinas-Instituto Politécnico Nacional, Av. Instituto Politécnico Nacional s/n, Colonia Playa Palo de Santa Rita, La Paz, B.C.S. 23096, México. Email: amartin@ipn.mx Fax: +52-612-122-5322

Recibido: 2 de enero de 2006
Aceptado: 13 de diciembre de 2006

Abstract

To evaluate changes in abundance and composition of phytoplankton in the San Ignacio-Navachiste-Macapule Lagoon Complex in the Gulf of California during the wet-dry transition months, 18 sampling sites were established. Samples were analyzed for abundance, chemical water composition, temperature, and Secchi disk measurements in September, October, and November 1998. The combined effects of rainfall, municipal wastewater, and agricultural drainage yielded runoff that generate low salinity, high concentration of nutrients, low pH, and high biochemical oxygen demand conditions. Temporal and spatial patterns of phytoplankton related to these drainage waters were mapped. The highest concentrations of chlorophyll (15 mg/m³), maximum phytoplankton abundance (3.7 × 10⁶ cells/L), and dominance by microphytoplankton (cells > 20 µm) occurred with the high runoff contribution of September. Phytoplankton concentrations (cells/L) decreased in October (1.6 × 10⁶) and November (2.3 × 10⁶), and the community was dominated by nannoplankton (cells < 20 µm). Cluster analysis showed the influence of runoff in the distribution of species, as well as abundance of cyanobacteria (5.5 × 10⁵ cells/L), higher in the inner lagoon in September and October. The study clearly showed a relationship between the development of phytoplankton blooms and the input of nutrients.

Key words: Wastewater, phytoplankton, Gulf of California, Navachiste, nutrients.

Resumen

Palabras clave: Aguas residuales, fitoplancton, Golfo de California, Navachiste, nutrientes.

Introduction

Coastal ecosystems in the Gulf of California support diverse and important fisheries, and are reservoirs of great biological diversity. In northern Sinaloa, population growth and development, as well as increased use of these natural systems for recreation, has substantially increased the pressure placed upon marine resources. Discharge of untreated wastewaters generated by diverse human activities has been notably altered its health and integrity, principally along the lagoon's eastern shore (De la Lanza-Espino, 1991; Escobedo-Urías, 1997).

In the late 60s, agriculture moved into a dominant role in coastal northern Sinaloa. The coastal plain encompasses more than 200,000 hectares under cultivation that now introduces large amounts of organic material, pesticides, heavy metals, and fertilizers into the lagoon systems at drainage discharge points (Escobedo-Urías et al., 1999; Ayala-Baldenegro, 2004). The municipality of Guasave discharges approximately 709,660 m³/year of wastewater into the tripartite lagoon of San Ignacio-Navachiste-Macapule (HAMG, 1996).

Nutrient runoff into the lagoon system can stimulate episodes of rapid phytoplankton growth. Some of the episodes may benefit the lagoon as an important source of food for bottom living organisms. However, proliferation of some planktonic species represents a risk to public health because they produce toxins eaten by consumable fish and shellfish. Certainly, for public health, it is essential to develop an inventory of the species in the lagoon and their dynamics in the ecosystem.

In Sinaloa, studies of phytoplankton dynamics have focused on the coastal waters around Mazatlán, in the southern portion of the state (Caballasi-Flores, 1985; Cortés-Altamirano & Pastén-Miranda, 1982; Cortés-Altamirano & Nuñez- Pastén, 1992; Cruz & Calvario, 1994; Alonso-Rodriguez et al., 2000). In the northern coastal region, the few studies available have been of a descriptive nature, providing valuable information on phytoplankton composition (Gómez-Aguirre, 1969; Licea-Durán, 1971; Meraz-Del Angel, 1997). For the tripartite lagoon system of San Ignacio-Navachiste-Macapule, the studies (Vicencio, 1979; Páez-Osuna et al., 1991; Escobedo-Urías et al., 1999) do not include information about phytoplankton, even though this lagoon system is the second largest in the state and one of the most productive coastal habitats in terms of fish capture.

The impact of wastewater in the coastal zone on production and biomass varies among systems (NRC, 2000). However, to understand how the anthropogenic factors interact with the natural variations of phytoplankton biomass and, in turn, be able to assess their impact on coastal systems, it is necessary to document the seasonal variability of phytoplankton and their physical-chemical environment. This study discusses the changes in abundance and composition of phytoplankton in the San Ignacio-Navachiste-Macapule lagoon complex during late summer and early autumn. The annual rainfall maximum in this region coincides with the start of the fall/winter agricultural cycle, the period of heaviest application of fertilizers and subsequently the period of highest nutrient input to the system.

The San Ignacio-Navachiste-Macapule Lagoon Complex (25°15'-25°35' N, 108°30'-109°03' W) covers an area of 220 km² (HAMG, 1996; Magaña-Álvarez, 2004). The lagoon complex has three entrances: Ajoro, Vasiquilla, and Bocanita (Fig. 1). Mean depth of the three lagoons is 2.5 m, with a range from 0.5 m to 5 m and the greatest depth at the Vasiquilla entrance (11 m). Annual precipitation averages about 300 mm, with the rainy season occurring in late summer and early fall (Vicencio, 1979; Escobedo-Urías et al., 1999). The tides in this lagoon complex have a strong semi-diurnal component with two unequal flood and ebb cycles every 24.84 hours. Tidal amplitude is about 1.08 m, and maximum current speed during ebb tide is approximately 2.1 m/s at the Vasiquilla entrance (Escobedo-Urías et al., 2001). Circulation patterns indicate a major influence of continental shelf waters at the northern entrance (Ajoro) (Escobedo-Urías et al., 2001; Ulloa-Pérez, 2005). Seasonal condition defines two periods, one cold season (December to March) and a warm season (May to September) (Magaña-Álvarez, 2004; De Silva-Dávila et al., 2006). The system is anti-estuarine (annual mean = 36 psu) with higher average salinity during the wet season and lower average salinity during the dry season (30-45 psu) (Escobedo-Urías et al., 2001). Agricultural and municipal wastewater drains are the main source of freshwater, in addition to runoff during the wet season (De Silva-Dávila et al., 2006).

Data of pluvial precipitation, wind direction and speed were recorded every 15 minutes in the municipality of Guasave, about 20 km from the lagoon complex (Meteorological Station of the Comision Nacional del Agua; CNA). During September, October, and November 1998, field measurements at 18 sampling stations (Fig. 1) were taken over 5-6 h of survey during flood tides, with the exception of November, when sampling was performed under ebb tidal condition. Surface temperature and salinity was obtained (Beckman salinometer) and pH measured (Corning potentiometer model 3D). Transparency of the water was estimated with the Secchi disk. Simultaneously, water samples were taken with a van Dorn bottle, filtered and frozen to determine dissolved inorganic nitrogen and phosphorus (NO₃^-+N, NO₂^-+N, NH₄^-+N and PO₄^-3+P) according to Strickland and Parsons (1972). Dissolved oxygen (DO), biochemical oxygen demand (BOD5), and total suspended solids (TSS) were measured according to Eaton et al. (1995). The effect of salinity and temperature on dissolved oxygen was normalized by estimating the percentage of saturation, according to Riley & Chester (1971). N:P ratios were calculated from NO₂^-+ NO₃^-+ NH₄^- nitrogen and PO₄^3-phosphorus. Water samples for measuring chlorophyll were filtered through GF/F glass fiber filters (0.7 µm nominal pore size). These filters were frozen at -70°C and later analyzed spectrophotometrically after extraction in 90% acetone (Venrick & Hayward, 1984). Active chlorophyll a was calculated according to equations in Jeffrey & Humphrey (1975). Additionally, water samples were collected to determine abundance and composition of phytoplankton. The enumeration of nannoplankton (2-20 µm) and microphytoplankton (>20 µm) was made using 1% Lugol's solution fixed samples with the standard technique of Utermöhl (Hasle, 1978) under an inverted microscope (Olympus). Identification of microphytoplankton was performed at 400× by using several standard identification references (Tomas, 1997; Hustedt, 1959; Hustedt, 1961-66), between others.

To obtain information on the degree of variability of the system using the phytoplankton assemblages, the species diversity index of Shannon-Wiener was calculated (Pielou, 1966). A multivariate analysis was used to examine relationships in the microphytoplankton data set. Cyanobacteria (individuals are < 20 µm) were included in this category because they are organized in filaments. To reduce the number of variables included in the analysis, a selection of the most frequently observed species (occurring in at least 10% of the samples) was made. The matrices of sampling stations and species categories were used for a Q-mode cluster analysis after a log (x+1) transformation.

Results

Monthly precipitation in the wet season of 1998, which occurs between June and October ranged from 360 mm in September and declined to 54 mm in October (Fig. 2A). During this season, wind oscillates between its winter and summer/fall patterns. Southwest winds (average speed 6.1 m/s) prevail during September and oscillated during October and November between this direction and northwest (Figure 2B).

Physicochemical Variables. The physicochemical variables showed distinct differences among the sampled months. Temperature declined, but salinity increased. Minimum salinity occurred at stations 8-9 and the maximum was localized in the innermost part of the lagoon, farthest from the coast (station 6) (Fig. 3A, Table 1). The pH increased from September to November, and BOD₅ values showed similar in September, and November, but were higher (6.32) in October, with maximum values in the innermost part of the lagoon (Fig. 3B, Table 1). Transparency was inversely related to the concentration of total suspended solids, with higher suspended solids and lower transparency at sampling sites close to drains (Fig. 3C, Table 1). A regression analysis of Kd (1.6/Secchi disc depth) vs TSS and chlorophyll a concentration showed strong effects of solids suspended on water transparency, resulting in 45.4% (P + 0.05) of the variance attributable to this parameter occurring in September, and declining in October and November (Fig. 4). During the study period, approximately 25% (P + 0.05) of the variance is attributable to chlorophyll a (Fig. 4).

A marked influence of the input of residual wastewaters, such that the maximum values of all nutrients, occurred near the agricultural and municipal outlets in the three months (Fig. 5A). The lagoon complex was nutrient rich but the ratio of dissolved inorganic N to inorganic P was far below the Redfield ratio stechiometry of 16:1 (by atoms), with average values of 2.61, 0.99, and 2.77 for September, October, and November, respectively. This indicates N limitation condition for phytoplankton growth due to the fluctuations between N and P concentrations. The concentrations of all types of nitrogen were lowest in September and highest in November, while the average maximum concentration of orthophosphates occurred in October and was the case along the lagoon complex (Table 1, Fig. 5A). The major component of dissolved inorganic nitrogen was ammonium (average > 78%), but nitrate and nitrite concentrations increased in November (Fig. 5B).

During the highest precipitation in September, there was a higher positive correlation between oxygen saturation with the abundance of phytoplankton, resulting in 44.3% (P < 0.05) of the variance attributable to phytoplankton.

Spatial-temporal distribution of phytoplankton. Phytoplankton abundance was highest in September, with a maximum concentration (6 × 10⁶ cells/L) in front of the wastewater and agricultural discharge drains at Novobampo, and Batamote. The lowest phytoplankton concentrations in September (6 × 10⁵ cells/L) occurred near the Ajoro entrance of Laguna San Ignacio. The mayor contributors to the maximum concentrations of chlorophyll a (15 mg Chl a/m³) (Fig. 5D) were nannophytoplankton, diatoms, and cyanobacteria (Fig. 6). In October, phytoplankton declined (1.7 × 10⁶ cells/L), but there were larger numbers of nannophytoplankton. November showed similar abundances as September, maximum of 3 × 10⁶ cells/L and 5.73 mg Chl a/m³), but microphytoplankton was dominant.

A total of 376 species belonging to the microphytoplankton size were identified. The most common and abundant groups were diatoms, dinoflagellates, silicoflagellates, and cyanobacteria, in that order, with diatoms clearly more dominant than all other groups combined. The Shannon-Wiener Diversity Index increased slightly from September to November except at stations located near the wastewater discharge (stations 7-9) (Fig. 6).

Cluster analysis. During September (S) and October (O), a similar phytoplankton assemblage was observed close to the drain outlets (clusters S1, S2, O1, and O2) (Figs. 7 and 8). In these areas, small cells, such as Nitzschia longissima (Brébisson) Ralfs, 1861, Cyanobacteria sp 1, Cylindrotheca closterium (Ehrenberg) Reimer and Lewin 1964, and Skeletonema costatum (Greville) Cleve 1873, were dominant. In October, cluster group O3 was distinguished by the dominant species of Chaetoceros lasciniosus Schütt 1895, S. costatum, and Campylosira cymbelliformis (A. Schmidt) Grunow ex Van Heurck 1885 (Fig. 8). Cyanobacteria reached their highest concentrations (5 × 10⁵ filaments/L) in September, declining to one-fifth in October, when their distribution was more homogeneous in the lagoon complex. In November (N), there were three clusters (N1, N2, and N3) (Fig. 9). The separation of clusters N1 and N2 is based on the dominance of the diatom Rhizosolenia setigera Brightwell 1858. Noteworthy is that their density was one order of magnitude higher in N1 than in N2. A lesser component of these two clusters was N. longissima and S. costatum. Cluster N3 was dominated by S. costatum with lesser density of R. setigera. No cyanobacteria were present in this month.

Our observations of the lagoon complex of San Ignacio-Navachiste-Macapule provided ample evidence of anthropogenic effects on phytoplankton. Nitrite and ammonium were high in comparison with other impacted lagoons in the region (Paredes & López, 1988; DGO, 1990; Castro-Longoria & Grijalva-Chon, 1991; Escobedo-Urías, 1997; Escobedo-Urías et al., 1999). This condition, as well as the high biological oxygen demand (2-6.32 mg/L) located near the outlet drains indicate the role of domestic and agricultural wastes (De la Lanza-Espino, 1984, 1994; Contreras-Espinosa, 1993) passing into the lagoons, mainly in Navachiste Bay. Other indicators of anthropogenic influence include high levels of organic material and heavy metals with the highest concentrations near the drain outlets (Ayala-Baldenegro, 2004).

Abundance of phytoplankton was in the range of previous studies in impacted southern lagoons in the state (Gilmartin & Revelante, 1978; Alonso-Rodriguez et al., 2000), and for the Guaymas area (Gilbert & Allen, 1943). However, are higher than had been reported for the nearby area of Bahía Topolobampo and the central region of the Gulf of California (Gilbert & Allen, 1943; Álvarez-Borrego & Lara-Lara, 1991). The dominance of nannoflagellates (2-20 µm) and small microphytoplankton (diatoms and cyanobacteria) is a major feature found in this lagoon complex. This is contrary to the situation found in Mazatlan Bay, Sinaloa during the 80s (Caballasi-Flores, 1985) and for other nitrogenenriched coastal systems, such as the Bay of Brest (Del Amo et al., 1997), where phytoplankton is dominated by microphytoplankton. The dominance of small-sized phytoplankton does not seem to represent a response of the community structure to the nutrient loads of freshwater runoff because the phytoplankton are better adapted to low nutrient conditions (Riegman et al., 1993). Nutrients often have major regulatory effects on phytoplankton abundance and composition; however, proportions of elements are particularly important. With the high precipitation (360 mm) in September, nutrient concentrations were lower than what is usually expected at the discharge sites, probably from phytoplankton growth (the highest concentration found, 6 × 10⁶ cells/L, and oxygen saturation). These concentrations were six times higher than near the Ajoro entrance where water exchange with the gulf is most intense. In October, with only 54 mm of rainfall, runoff greatly declined and the concentration of phytoplankton, particularly diatoms, diminished approximately by 50%.

The ratio of dissolved inorganic nitrogen to phosphorus in surface water was lower than 16:1, indicating a nitrogen limitation on microphytoplankton growth, particularly in September and October, except in the areas close to the drain outlets, where the ratio fluctuated between 2 and 6 to1. Phosphorus as a limiting factor for growth was not observed. Phosphate concentrations were slightly higher in October, compared to the previous and following months. Higher values of DBO₅ indicated that high remineralization was occurring in this month. This condition as well a lower phytoplankton growth could explain phosphate concentrations, circumstance reported in other studies (Mee, 1977; Liss, 1976; Valiela, 1995; Magaña-Álvarez, 2004).

Under nitrogen-limiting conditions, nannophytoplankton and the diatoms N. longissima, Cylindrotheca closterium, and S. costatum, can grow rapidly (Furnas, 1990). These species are apparently able to respond rapidly to reduction of limiting nutrient conditions (Harrison et al., 1977). S. costatum in particular, has a preference for high ammonium and phosphorus environments (Sakshaug & Andersen, 1986) with lower nitrogen to phosphorus ratios (Moisander et al., 2003), as were the prevailing conditions in this lagoon complex.

In November, an increase of ammonium occurred, but the lack of significant correlation between phytoplankton density and oxygen saturation, as well as an increase in nitrate concentration, indicates high oxygen demand in the remineralization process. This process, in addition to the runoff of fertilizers at the beginning of the fall/winter agriculture cycle (Escobedo-Urías, 1997; Escobedo-Urías et al., 1999; Magaña-Álvarez, 2004), promoted an increase in the dissolved inorganic nitrogen to phosphorus ratio, which occurred at the time of a bloom of larger-sized diatoms dominated by R. setigera. The diatom bloom was most abundant where agricultural wastewater discharged into the lagoons and the nitrogen to phosphorus ratio was close to 6 to 1, indicating a minor nitrogen limitation.

Other elements besides N and P can have a major influence on the structure of the phytoplankton community and can affect the nature of their response to nutrient inputs. The availability of silica has little or no influence on the overall rate of algal growth in an aquatic system, but when silica is abundant, diatoms are one of the major components of the phytoplankton. Although silica analysis was not performed, concentrations of this nutrient in another study of Laguna de Macapule showed abundant silica, ranging from 24.4 to 37.4 µM (Magaña-Álvarez, 2004). The relative availability of nitrogen and silica may influence the abundance of diatom species (Gilpin et al., 2004), explaining why there was a diatom bloom in November.

Other indicators of wastewater influence were a low diversity index and a great concentration of cyanobacteria mainly during the rainy season (September/October). Particularly, cyanobacteria have been associated with these conditions at other sites around the world (Jones, 2000), as well as lagoons and estuaries along the eastern coast of the Gulf of California (Gómez-Aguirre, 1969; Santoyo, 1972; Gómez-Aguirre et al., 1974).

For many years, there has been speculation that discharges from agricultural areas can stimulate the development of phytoplankton blooms from the considerable quantities of fertilizers used in agriculture in the state of Sinaloa (= 14 tons nitrogen/ month and 3 tons phosphorus/month incorporated into coastal lagoons, Calvario-Martínez et al., 2006). This study clearly shows a relationship between phytoplankton bloom development and the input of nutrients. However, comprehension of the dynamics will require long-term time-series biological and physical-chemical studies, as well as physiological bioassays.

The Dirección de Estudios de Posgrado e Investigación, Instituto Politécnico Nacional provided financial support for the project "Variabilidad espacio-temporal de la calidad del agua del Sistema Lagunar San Ignacio-Navachiste, Sinaloa" (CGPI 980071). AML, DEU, and MaTHR were supported by the Comisión de Operación y Fomento de Actividades Académicas (COFAA-IPN) and Estímulos al Desempeño en Investigación (EDI) fellowships, from the Instituto Politécnico Nacional.

References

ALONSO-RODRÍGUEZ, R., F. PÁEZ-OSUNA & R. CORTÉS-ALTAMIRANO. 2000. Trophics conditions and stechiometry nutrient balance in subtropical waters influenced by municipal sewage effluents in Mazatlán Bay (SE Gulf of California). Marine Pollution Bulletin 40 (4): 331-339.         [ Links ]

ÁLVAREZ-BORREGO, S. & J. R. LARA-LARA. 1991. The physical environmental and primary productivity of the Gulf of California. In: Simonett, B.R.T. & Dauphim, J.P. (Eds.). The Gulf and Peninsular Province of the Californias. American Association of Petroleum Geologists Memoir. pp. 555-567.         [ Links ]

AYALA-BALDENEGRO, L. 2004. Distribución de la concentración de metales pesados en sedimentos y su relación con organismos indicadores (Crassostrea sp. y Mytella sp.) en el Sistema Lagunar del Municipio de Guasave, Sinaloa. Tesis de Maestría en Recursos Naturales y Medio Ambiente. IPN-CIIDIR Sinaloa México. 73 p.         [ Links ]

CABALLASI-FLORES, P. 1985. Comparación fitoplanctónica de la bahía de Mazatlán y estero de Urías, Sinaloa, México. 1981. Tesis Profesional. UNAM-ENEP-Iztacala. México 50 p.         [ Links ]

CALVARIO-MARTÍNEZ, O., P. DOMÍNGUEZ-JIMÉNEZ, D. ESCOBEDO-URÍAS, A. ULLOA-PÉREZ, N. HERRERA-MORENO, C. LECHUGA-DEVÉZE, M. ZARAIN-HERZBERG & M. PACHECO-MARGES, 2006. Estudio para determinar la capacidad de carga de los sistemas lagunares del norte y centro del Estado de Sinaloa para los proyectos de camarón y peces en jaulas. CONAPESCA. 100 p.         [ Links ]

CASTRO-LONGORIA, R. & J. M. GRIJALVA-CHON. 1991. Variabilidad espacio-temporal de nutrientes y seston en la laguna costera de La Cruz, Sonora. Ciencias Marinas 17 (2): 83-97.         [ Links ]

CONTRERAS-ESPINOSA, F. 1993. Ecosistemas Costeros Mexicanos. 1ª. Edición. CONABIO-UAM. México. 415 p.         [ Links ]

CORTÉS-ALTAMIRANO, R. & N. PASTÉN-MIRANDA. 1982. Composición, abundancia y distribución del fitoplancton del Estero Urías, Sin., México. I. Período primavera (1980). Revista Latinoamericana de Microbiología. 24: 103-114.         [ Links ]

CORTÉS-ALTAMIRANO, R. & P. A. NUÑEZ- PASTÉN. 1992. Doce años (1979-1990) de registros de mareas rojas en la bahía de Mazatlán, Sinaloa, México. Anales del Instituto de Ciencias del Mar y Limnología. UNAM 19 (1): 113-121.         [ Links ]

CRUZ M. A. & M. O. CALVARIO. 1994. Productividad acuática en la costa noroccidental del Pacífico Mexicano. Determinación, análisis y predicción. Resúmenes de X Simposium Internacional de Biología Marina. pp 63.         [ Links ]

DE LA LANZA-ESPINO, G. 1984. Calidad ambiental de la Laguna de Mezcaltitán, Nayarit, México, durante el estiaje. Nota Científica. Anales del Instituto de Ciencias del Mar y Limnología. UNAM. 18 p.         [ Links ]

DE LA LANZA-ESPINO, G. 1991. Oceanografía de Mares Mexicanos. AGT Editor. México, D. F. 569 p.         [ Links ]

DE LA LANZA-ESPINO, G. 1994. Química de las Lagunas Costeras y el Litoral Mexicano. In: De la Lanza y Cáceres (Eds.). Lagunas Costeras y el Litoral Mexicano. UABCS. pp. 27-198.         [ Links ]

DEL AMO, Y., B. QUÉGUINER, P. TRÉGUER, H. BRETON & L. LAMPERT. 1997. Impacts of high-nitrate freshwater inputs on macrotidal ecosystems. II. Specific role of the silicate pump in the year-round dominance of diatoms in the Bay of Brest (France). Marine Ecology Progress Series 161: 225-237.         [ Links ]

DE SILVA-DÁVILA, R., R. PALOMARES-GARCÍA, A. ZAVALA-NORZAGARAY, & D. C. ESCOBEDO-URÍAS. 2006. Ciclo anual de los grupos dominantes del zooplancton en Navachiste, Sinaloa. In: Hendrickx M.E. (Ed.). Contributions to the Study of East Pacific Crustaceans 4 (1). Instituto de Ciencias del Mar y Limnología, México. UNAM, pp. 25-39.         [ Links ]

DIRECCIÓN GENERAL DE OCEANOGRAFÍA NAVAL (DGO). 1990. Estudio de calidad del agua del Puerto de Guaymas, Sonora y proximidades.. Dirección de Prevención de la Contaminación Marina. DGO/DPCM/ GUAY/87.Secretaría de Marina, México. Folio variado.         [ Links ]

EATON, A.D., L.S. CLESCERI & A.E. GREENBERG (EDS.). 1995. Standard methods for the examination of water and wastewater. 19th Ed. American Public Health Associaton (APHA). Maryland. Folio variado.         [ Links ]

ESCOBEDO-URÍAS, D. 1997. Hidrología, nutrientes e influencia de las aguas residuales en la Laguna de Santa María, Sinaloa. Tesis de Maestría. CICIMAR-IPN. B: C. S., México. 87 p.         [ Links ]

ESCOBEDO-URÍAS, D., M. T. HERNÁNDEZ-REAL, N. HERRERA-MORENO, A. ULLOA-PÉREZ & A. CHIQUETE-OZONO. 1999. Calidad bacteriológica del sistema lagunar de San Ignacio-Navachiste, Sinaloa. Ciencia y Mar. UMAR. Oaxaca, México. pp. 17-27.         [ Links ]

ESCOBEDO-URÍAS, D., A. JIMÉNEZ-ILLESCAS, A. MARTÍNEZ-LÓPEZ, A. REYES-SALINAS, T. HERNÁNDEZ-REAL, N. HERRERA-MORENO, A. E. ULLOA-PÉREZ, A. ZAVALA-NORZAGARAY, & P. ÁLVAREZ-RUIZ. 2001. Oceanografía de la Bahía de Navachiste, Guasave, Sinaloa. Informe Técnico IPN-CIIDIR.Sinaloa. México. 37 pp.         [ Links ]

FURNAS, M. J. 1990. In situ growth rates of marine phytoplankton: approaches to measurement, community and species growth rates. Journal of Plankton Research 12: 1117- 1157.         [ Links ]

GILBERT, J. Y. & W. E. ALLEN. 1943. The phytoplankton of the Gulf of California, obtained by the E. W. Scripps in 1939 and 1940. Journal of Marine Research 5: 89-110.         [ Links ]

GILMARTIN, M. & N. REVELANTE. 1978. The phytoplankton characteristics of the barrier island lagoons of the Gulf of California. Estuarine and Coastal Marine Science 7 (1): 29-47.         [ Links ]

GILPIN, L. C., K. DAVIDSON & E. ROBERTS. 2004. The influence of changes in nitrogen: silicon rates on diatom growth dynamics. Journal of Sea Research 51: 21-35.         [ Links ]

GÓMEZ-AGUIRRE, S. 1969. Estudios del plancton de la laguna de Agiabampo, Son./Sin., México (Resultados preliminares). Resumenes IV Congreso Nacional de Oceanografía. p. 84.         [ Links ]

GÓMEZ-AGUIRRE, S., H. SANTOYO & A. MARTÍNEZ. 1974. Plancton de lagunas costeras II. Ciclo anual en la laguna de Yavaros (1969-1970). Anales del Instituto de Biología. UNAM. Serie Zoología 45 (1): 1-30.         [ Links ]

HONORABLE AYUNTAMIENTO DEL MUNICIPIO DE GUASAVE (HAMG). 1996. Plan municipal de desarrollo de Guasave (1996-1998). H. Ayuntamiento del Municipio de Guasave.187 p.         [ Links ]

HARRISON, P.J., H. L. CONWAY, R. W. HOLMES, & C. O. DAVIS. 1977. Marine diatoms grown in chemostats under silicate or ammonium limitation. III. Cellular chemical composition and morphology of Chaetoceros debilis, Skeletonema costatum and Thalassiosira gravida. Marine Biology 43: 19-31.         [ Links ]

HASLE, G.R. 1978. Using the inverted microscope. In: Sournia, A. (Eds.). Phytoplankton Manual. UNESCO. Paris. 91-196 pp.         [ Links ]

HUSTEDT, F. 1959. Die Kieselalgen Deutschland, Osterreichs und der Schweiz. In: L. Rabenhorst (Ed.), Kryptogamen-Flora von Deutschland, Osterreich un Schweiz, VII Band, II Teil. Koetz Scientific Books (Rep. 1991), Germany. 845 p.         [ Links ]

HUSTEDT, F. 1961-66. Die Kieselalgen Deutschland, Osterreichs und der Schweiz. In: L. Rabenhorst (Eds.), Kryptogamen-Flora von Deutschland, Osterreich un Schweiz, VII Band, III Teil. Koeltz Scientific Books (Rep. 1991), Germany. 816 p.         [ Links ]

JEFFREY, S. W. & G. F. HUMPHREY. 1975. New spectrophotometric equations for the determining chlorophylls a, b, c₁ and c₂ in higher plants, algae and natural phytoplankton. Biochemie und Physiologie der Pflanzen. 167: 191-194.         [ Links ]

JONES, R. I. 2000. Mixotrophy in planktonic proteists: an overview. Freshwater Biology. 45: 219-226.         [ Links ]

LICEA-DURÁN, S. 1971. Sistemática, distribución y variación de diatomeas de la laguna de Agiabampo, Sonora/Sinaloa, México. Tesis Profesional. Facultad de Ciencias. UNAM, México. 31 p.         [ Links ]

LISS, P. S. 1976. Conservative and non-conservative behavior of dissolved constituents during estuarine mixing. In: Burton J. D. & P. S. Liss (Eds.). Estuarine Chemistry. Academic Press. London, pp. 93-130.         [ Links ]

MAGAÑA-ÁLVAREZ, M. E. 2004. Distribución de nutrientes y su efecto en el nivel trófico de la laguna Macapule, Sinaloa. Tesis de Maestría. IPN-CIIDIR, Sinaloa. México. 105 p.         [ Links ]

MEE, L. D. 1977. Coastal Lagoons. In: Riley & Chester (Eds.). Chemical Oceanography. United States of America. 7: 441-490.         [ Links ]

MERAZ-DEL ANGEL, J. C. 1997. Análisis cualitativo del microfitoplancton en época de invierno de las Bahías de Ohuira, Topolobampo y Santa María, Sinaloa, México. Informe Técnico. Secretaría de Marina. Dirección General de Oceanografía Naval. Estación de Investigación Oceanográfica del Pacífico Centro. Topolobampo, Sinaloa. 13 p.         [ Links ]

MOISANDER, P. H., T. F. STEPPE, N. S. HALL, J. KUPARINEN & H. W. PAERL. 2003. Variability in nitrogen and phosphorous limitation for Baltic Sea phytoplankton during nitrogen-fixing cyanobacterial blooms. Marine Ecology Progress Series 262: 81-95.         [ Links ]

NATIONAL RESEARCH COUNCIL (NRC) (EDS.). 2000. Clean Coastal Waters. Understanding and Reducing the Effects of Nutrient Pollution. National Academy Press. pp 163-175.         [ Links ]

PÁEZ-OSUNA, F., P. H. ZAZUETA & F. G. IZAGUIRRE. 1991. Trace metals in bivalves from Navachiste Lagoon, México. Marine Pollution Bulletin 22 (6): 305-307.         [ Links ]

PAREDES R. & M. A. LÓPEZ. 1988. Comportamiento de parámetros hidrográficos y de productividad orgánica en un sistema lagunar del Estado de Sonora. Tesis Profesional. Universidad de Sonora, Sonora. 165 p.         [ Links ]

PIELOU, E. C. 1966. The measurement of diversity in different types of biological collections. Journal Theoretical Biology. 13: 131-144.         [ Links ]

RIEGMAN, R., B. R., KUIPERS, A. A. M.,NOORDELOOS & H.J., WITTE. 1993. Size-differential control of phytoplankton and the structure of plankton communities. Netherlands. Journal of Sea Research 31 (3): 255-265.         [ Links ]

RILEY, J. P. & R. CHESTER. 1971. Introduction to Marine Chemistry. Academic Press. Nueva York. 465 p.         [ Links ]

SANTOYO, H. 1972. Variación estacional del fitoplancton y la hidrología de la Laguna de Yavaros, Sonora. Tesis Profesional. Facultad de Ciencias. UNAM, México. 71 p.         [ Links ]

SAKSHAUG, E. & K. ANDERSEN. 1986. Effect of light regime upon growth rate and chemical composition of a clone of Skeletonema costatum from the Trondheimsfjord, Norway. Journal of Plankton Research 8: 619-637.         [ Links ]

STRICKLAND, J.D. & T. R. PARSONS. 1972. A practical handbook for the sea water analysis. Fisheries Research Board of Canada. Bulletin 167. Second Edition.         [ Links ]

TOMAS, R. C.1997. Identifying marine phytoplankton. 2da ed. Academic Press Inc. London, U.K. 858 p.         [ Links ]

ULLOA-PÉREZ. A. E., 2005. Influencia de la disponibilidad de nutrientes sobre los cambios espacio-temporales de la comunidad de fitoplancton en el litoral del Municipio de Guasave, Sinaloa. Tesis de Maestría. CIIDIR-IPN. 89 p.         [ Links ]

VALIELA, I., 1995. Marine Ecology Processes. Second Edition. Springer. New York, USA. 686 p.         [ Links ]

VENRICK, E. & T. HAYWARD. 1984. Determining chlorophyll on the 1984 CALCOFI surveys. California Cooperative Oceanic Fisheries Investigations Report 25: 74-79.         [ Links ]

VICENCIO, A. 1979. Estudio ictiológico de dos lagunas costeras de la zona norte de Sinaloa, México. Tesis Profesional. Fac. Cienc. UNAM, México. 116 p.         [ Links ]