Influence of agriculture and aquaculture activities on the response of autotrophic picoplankton in Laguna Macapule, Gulf of California (Mexico)
© The Author(s). 2017
Received: 10 October 2016
Accepted: 23 January 2017
Published: 27 February 2017
The lagoon is a component of coastal zones, whose populations of autotrophic picoplankton (APP) remain largely unstudied. These lagoons display high-nutrient productivity and additionally may also be subjected to anthropogenic activities. This study selected Laguna Macapule, located on the eastern shore in the mid-region of the Gulf of California, due to the fact that a drainage network servicing the surrounding agricultural region (>230,000 hectares under cultivation) directs irrigation runoff, shrimp farm effluents, and urban wastewater containing large quantities of nutrients to be discharged into this lagoon. We propose to identify the APP’s response to various types of environmental and anthropogenic influence in this highly impacted coastal lagoon.
Two sites (separated by 2.7 km) were monitored from December 2007 to December 2008. One, located at the entrance to Laguna Macapule (oceanic influence) and the other a discharge canal (eutrophic conditions) inside the lagoon at El Tortugón.
APP was the numerically dominant phytoplankton fraction (15 × 106 to 620 × 106 cells L−1) with coccoidal cyanobacteria as the dominant fraction throughout the year. Peak levels were reached in spring-early autumn and they were the second largest contributor to biomass. Abundance of APP cells corresponds to the lagoon’s eutrophic status. Maximum numbers and a higher average of APP were recorded at the El Tortugón channel during the warm season (months with SST higher than 24 °C). The general positive relationship of the APP’s annual cycle at both sites as well as a negative relationship with heterotrophic nanoflagellates (HNF) abundance, supports the idea that natural forcing, in particular sea surface temperature (SST) is the predominant influences on APP’s seasonal variability.
Distinguishable significant differences in APP abundances and nutrients were recognizable between the two sites. The interplay of these variables contributed to lower densities of APP in winter and high densities in spring-early autumn. N:P = ~4 suggests that spring-early autumn abundance of the APP autotrophic component was sustained by urea from shrimp farm discharge water. Thus, a total nutrient-based approach is likely the most suitable tool for establishing nitrogen limitation of biological production in Laguna Macapule and similarly impacted ecosystems around the world.
KeywordsAquaculture Autotrophic picoplankton Eutrophic conditions Heterotrophic ciliates Heterotrophic nanoflagellates Urea
Autotrophic picoplankton (APP) is recognized as a ubiquitous and abundant component of phytoplanktonic communities (Marshall 2002) represented primarily by prokaryotic coccoidal cyanobacteria (Flombaum et al. 2013) and prochlorophytes (Chisholm et al. 1988). There are also small eukaryotes with a potentially large representation (Johnson and Sieburth 1982; Jardillier et al. 2010). In the 1970s, high densities of APP were discovered in low-nutrient, temperate oceanic areas (Johnson and Sieburth 1979; Waterbury et al. 1979). Since then, most studies have focused on oligotrophic systems, which corroborated the contribution of APP to pelagic food webs and their role in carbon and mineral cycling (Barber and Hiscock 2006; Flombaum et al. 2013). Thus, the paradigm that APP was important primarily in oceanic waters was established. Subsequently, abundant evidence has shown that APP is a major component of the phytoplankton community in coastal and continental shelf areas (e.g., Calvo-Díaz and Morán 2006; Linacre-Rojas et al. 2010; Gunbua et al. 2012). Within coastal zones, there remains a specific subclass region where populations of APP, to a great extent, are unstudied. These are lagoons that display high-nutrient productivity, as well as those threatened by anthropogenic activities. Studies of ecosystems affected by eutrophication and imbalanced N:P ratios provide evidence of large abundances of APP (>100 × 106 cells L−1) (Badylak and Phlips 2004; Murrell and Caffrey 2005; Gaulke et al. 2010). In nitrogen-limited environments, APP displays a distinct competitive advantage (Raven 1998); however, the APP responses to seasonal changes in coastal systems remain unclear, mainly because there is limited documentation of the annual cycle.
In the Gulf of California, with numerous lagoons, the subtropical climate favors seasonal nutrient enrichment because rainfall is prevalent mainly in the summer, which leads to rapid nutrients runoff. Many lagoons receive nutrient inputs from fertilization of shrimp farms and crop fields, as well as the load derived from urban settlements that use streams as waste disposal channels. These sources of nutrient pollutants affect phytoplankton overall abundance and seasonal variability. Laguna Macapule is one of over 15 coastal water bodies along coast of Sinaloa. It was selected for this study because it is impacted by several nutrient sources of disparate origins. It receives large quantities of nutrients from irrigation runoff that are collected in a drainage network servicing the surrounding agricultural region (>230,000 ha under cultivation), shrimp farm effluents, and urban wastewater. These nutrient sources should favor microphytoplankton growth; instead, some studies indicate that smaller, coccoid cyanobacteria and flagellates are the dominant groups under conditions typified by high concentrations of ammonium and low inorganic N:P nutrient ratios of less than 16:1 (Poot-Delgado 2006). This suggested that APP could make an important contribution to the base of the trophic web structure. At present, there are no published annual data on the abundance of APP in Mexican coastal systems in the Gulf of California.
This study is the first compilation and will serve as a baseline for future surveys that document abundance and seasonal variability of APP in the Laguna Macapule, with the aim of understanding the small-size fraction of the planktonic food web in coastal systems affected by anthropogenic pressures.
Inside the lagoon, two sampling points were selected because of their contrasting characteristics. One site is located at the inlet of the lagoon, which exhibits open ocean water conditions year round. The other (El Tortugón) is located at the back of the lagoon in front of a discharge mouth, one of several drainage channels that enter the lagoon after passing through mangroves. This natural tidal channel receives discharge from a small settlement, two shrimp farms, and agricultural runoff from the backland. This site is strongly influenced by fresh water runoff during the rainy season, which carries agricultural effluents. Numerous others shrimp farms are located along the length of the inner shore of the lagoon.
Sampling procedures and analyses
Monthly samples were taken from December 2007 through December 2008 at the two sampling stations (2.7 km far away) at high tide. The tides in this lagoon have a strong semi-diurnal component with two unequal flood and ebb cycles every 24.84 h. Tidal amplitude is about 1.08 m (Martínez-López et al 2007). Sea surface temperature (SST) was measured with a multiparameter analyzer (Model U-10, Horiba, Kyoto, Japan). Water samples were taken with a segmented pipe sampler (Sutherland et al. 1992) for integrated profiling of the upper 3 m of the water column. The samples were filtered (Whatman GF/F, pore size 0.7 μm) and frozen for later assays of dissolved nutrients. Dissolved inorganic phosphorus (DIP) and urea were assayed according to Strickland and Parsons (1972) and Mulvenna and Savidge (1992), respectively. Ammonium (NH4 +) was assayed according to Solórzano (1969). Wind speed data were obtained from a meteorological station run by the federal agency Conagua located in the city of Guasave (25° 33′ 45″ N, 108° 27′ 40″ W), which is approximately 27 km from the lagoon.
Triplicate samples were collected in sterile glass bottles to quantify APP (phytoplankton <2 μm), autotrophic nanoplankton, and heterotrophic nanoplankton (2–20 μm). These samples were preserved with 1% phosphate-buffered glutaraldehyde. For APP, unstained subsamples (2–6 mL) were filtered through 0.2-μm polycarbonate membranes (MacIsaac and Stockner 1993). Autotrophic nanoplankton and heterotrophic nanoplankton subsamples (10–17 mL) were filtered through 0.8-μm polycarbonate filters and counted after primulin staining (Caron 1983). Both filters were mounted on microscope slides with non-fluorescent oil, and abundance was determined by epifluorescence microscopy equipped with a Hg 100-W lamp, blue-light excitation filter cube (exciter BP460 to 490 nm, dichroic mirror 505 nm, barrier 515 nm) and bright line multiband filter cube (exciter BP360 to 730 nm, dichroic mirror 400 nm, barrier 420 nm). At least 200 cells were counted from random fields at ×1000 magnifications in each of three replicate slides. In the case of blooms of autotrophic nanoplankton (>1 × 106 cells L−1), the organisms were identified to class level, with additional observations of water samples preserved with 1% lugol under an inverted microscope (Lund et al. 1958). Data on heterotrophic ciliates and microzooplanktonic organisms, such as microcrustaceans, were collected to assess their impact on the APP. Abundance was estimated with the Utermöhl technique (Lund et al. 1958). Samples preserved with 1% lugol (final concentration) were allowed to settle for at least 24 h in sedimentation chambers (10 cm3), followed by counts at ×200 and ×400 magnification under an inverted microscope (Olympus CKX41, Olympic America, Center Valley, PA).
The combined data from both sites and the data from each site were tested for normal distribution, using the Kolmogorov–Smirnov test (Smith et al. 1998). Distribution of many variables differed significantly (p < 0.05); therefore, relationships between biological data (abundance of autotrophic nanoplankton, heterotrophic nanoplankton, and microzooplankton) and various environmental variables (water temperature, temperature, NH4 +, DIP, and urea) were determined using Spearman’s rank correlations analysis (Zar 1999). Statistical differences between environmental variables and abundance of plankton at the two sites were tested with the Wilcoxon method for paired samples (Zar 1999). Monthly abundances of APP were compared, using the Kruskal–Wallis test. Significance was set at p < 0.05. Statistical analyses were performed with Statistica 8.0 computer software (StatSoft, Tulsa, OK, http://statistica.io/products/).
Abundance and biomass contribution of the three phytoplankton size classes at two sampling stations in Laguna Macapule during cold and warm months
Phytoplankton size fraction
Average abundance, ×106 cells L−1 (SD)
Relative biomass (%)
Average abundance, ×106 cells L−1 (SD)
Relative biomass (%)
Densities of heterotrophic nanoflagellates showed a distinctly different pattern from December through March than the other categories of microorganisms. Their abundance peaked at 7.9 × 106 cells L−1 in December, declining afterward through June and then remained low (1.44 × 106 cells L−1 and 0.34 × 106) until the end of the study (Fig. 3b). Significant statistical differences (Wilcoxon Z = 3.04; p = 0.002) in density occurred between sampling stations.
Microzooplankton included small crustacean nauplii, copepods, rotifers, and heterotrophic ciliates (HC). Heterotrophic ciliates, mainly composed of oligotrichs, were the main component of the microzooplankton community. There were no statistical differences between sites (Wilcoxon Z = 0.87; p = 0.38). Average abundance at both sites was 26.7 × 103 cells L−1. Abundance at the entrance spiked to 120 × 103 cells L−1 in March. By June, abundance was less than at El Tortugón and remained low for the rest of the year (Fig. 3c).
Spearman rank correlation coefficients between autotrophic picoplankton (APP), environmental components of temperature, ammonia, dissolved inorganic phosphorus (DIP), N:P ratio, and urea and heterotrophic components of nanoplankton (HNF), ciliates (HC), and microzooplankton (MZ), based on total data (two sampling locations) from Laguna Macapule (n = 26) and each sampling location (n = 13)
HNF (cells L−1)
HC (cells L−1)
MZ (ind L−1)
Laguna Macapule (combined data set)
Our results confirmed that APP was numerically the dominant fraction of phytoplankton in this subtropical lagoon, paralleling other studies that have detected this dominance in other subtropical and tropical coastal systems (e.g., Phlips et al. 1999; Agawin et al. 1998; Chang et al. 2003) and in eutrophic environments (Murrell and Caffrey 2005; Cai et al. 2007; Gaulke et al. 2010). Rough estimates of APP biomass in Laguna Macapule varied from 0.9 to 63% of the phytoplankton groups, with its highest contribution (>20%) occurring during March–July; this places AAP as the second largest contributor to the total phytoplankton biomass being surpassed only by the autotrophic microplankton contribution. Estimated abundances levels (15–620 × 106 cells L−1) are of the same order of magnitude as reported values for global abundances of marine cyanobacteria with the maximum value being two times greater than the maximum value reported for open waters (Flombaum et al. 2013) and four times greater than those values reported for open waters in Gulf of California’s northern region (Díaz-Hernández and Maske 2000). Considering the global quantitative distribution of Prochlorococcus and Synechococcus, the most probable scenario is that the latter would be dominant in Laguna Macapule (Flombaum et al. 2013) similar to results from other marine systems (e.g., Palenik et al. 2006; Zwirglmaier et al. 2008; Taylor et al. 2012). Noticeable differences in abundance and biomass among phytoplankton size classes suggest that APP has a competitive advantage over the nanoplankton, in the eutrophic Laguna Macapule, which is opposite to that which was observed in non-impacted lagoons of the Gulf of California (Verdugo-Díaz et al. 2010).
Various studies have proposed diverse mechanisms to account for the success of APP. Some have assigned temperature and grazing (Agawin et al. 1998; Chiang et al. 2002; Chang et al. 2003), while others have assigned nutrient inputs (Murrel and Lores 2004; Barber and Hiscock 2006; Barber 2007) as controlling factors. Our results show that all these mechanisms are important. We found a positive relationship of APP abundance to temperature, DIP (at Laguna Macapule) and urea (at Macapule entrance) and a negative relationship to heterotrophic nanoflagellates (HNF) abundance (Table 2), which suggests that grazing could be a potential regulator. However, the functional relationships are complex and are not readily explained (e.g., the differences between December/February 2007 and December 2008). Thus, a different experimental design is necessary in future studies to address these questions. Moreover, genetic analyses should be useful in discerning complex species compositions and ecological interactions in the communities.
The seasonality of APP, at both sites, presented a similarity in the general tendencies. The natural forcing of SST is the predominant factor in driving seasonal variability of APP in the lagoon. However, even if this dominant driver was discounted, clear differences remained in APP abundance and physicochemical variables between the two sampling stations utilizing a seasonal referential time frame. These differences likely are a consequence of a synergistic mixture of natural and anthropogenic forcing, manifesting in a complex mosaic that is difficult to reduce to independent variables (Bratbak et al. 2011).
Ecologically, many factors contribute to the growth of one species or functional group over another, including biologic interactions. Growth and uptake of nutrients by APP occurred when temperatures were >12 °C, which demonstrates the determinative pressure exerted by SST (Sakamoto and Bryant 1998, Chang et al. 2003; Gaulke et al. 2010). Winter densities of APP were relatively low, despite temperatures above 16 °C and high inorganic nutrient content. This suggests that other variables, such as grazing or nutrient competition with other photoautotrophs, also regulated the abundance of APP at Laguna Macapule. Grazing is consistent with the negative correlation between heterotrophic nanoplankton and abundance of APP. Heterotrophic nanoplankton are the main consumers of heterotrophic prokaryotes (bacteria and archaea) and APP (Rassoulzadegan et al. 1988; Caron et al. 1991; Detmer et al. 1993), but the latter likely are more susceptible to predation due to their larger size (Christaki et al. 1998).
In summer, microzooplankton exhibits a high growth rate in coastal environments (Urrutxurtu et al. 2003; Bojanic et al. 2006; Sakka-Hlaili et al. 2007). In Laguna Macapule, microzooplankton, including ciliates, and abundance of APP followed similar trends. These suggest that APP was not regulated by grazing pressure from this group, which is supported by the positive correlation between most zooplankton components and APP abundance. Thus, it is probable that this pressure influenced the heterotrophic nanoplankton, explaining reduction in their abundance from March until the end of the year. This is consistent with observations in other systems (Bojanic et al. 2006; Pagano et al. 2006; Toshikazu and Chieko 2007). Interestingly, dominance of heterotrophic ciliate grazers during this period suggests that they are the principal link that transfers microbial biomass to higher trophic levels. Their densities are comparable to maximum numbers found in other eutrophic coastal systems (e.g., Sanders 1987; Montagnes et al. 1988; Xu et al. 2011). However, specific studies on grazing are needed to assess this hypothesis.
Seasonal variability of concentrations of nutrient was multifaceted, with levels of NH4 +, DIP, and urea having similar patterns. The variety of possible natural and anthropogenic nutrient sources makes it unusually difficult to isolate and determine their independent contributions to water quality. Peak concentrations of NH4 + occur during autumn/winter, concurrent with fertilizer input from regional agricultural activity; this previously was reported in nearby coastal lagoons, such as the Topolobampo system (Ayala-Rodríguez 2008) and the San Ignacio–Navachiste–Macapule complex (Escobedo-Urías et al. 1999; Poot-Delgado 2006). These nutrients are transported to the lagoon by runoff drains (Magaña-Álvarez 2004; Poot-Delgado 2006; Martínez-López et al. 2007; Escobedo-Urías 2010) and by atmospheric transport (Escobedo-Urías 2010). Analysis results of NH4 + data revealed an unexpected lack of statistical correlation between APP and ammonia. Absence of correlation does not exclude the possibility of efficient use by APP that was not revealed due to data limitations imposed by a monthly sampling regime. Additionally, during autumn/winter, entrainment of enriched-nutrient water from coastal upwelling occurs (Escobedo-Urías et al. 2007). Thus, high concentrations of nitrate, concurrent with low concentrations of SiO4 and high abundance of diatoms (up to 1.4 × 106 cell L−1) were recorded at the inlet to Laguna Macapule (Hakspiel-Segura 2009), which suggests that upwelling events influenced conditions inside the lagoon. Year-to-year climate variability related to El Niño–La Niña events can affect this region. During the 2008 La Niña event, stronger northwest winds intensified coastal upwelling off Laguna Macapule, augmenting the potentially favorable situation for the incursion of nutrient-rich water into the lagoon system (Martínez-López et al. 2008). Under these conditions, diatoms may represent an efficient competitive vector for nutrients, acting (in concert with grazing) to limit the APP.
Abundances of APP began to increase in April at both sampling stations (temperatures >22 °C). At the El Tortugón site, APP was about three times higher than the highest abundances at the entrance, suggesting a response to maximum nutrient loading related to agricultural activity during this period (Escobedo-Urías 2010). During the summer rainy season, a twofold APP decline was noted simultaneously with a diatom increase (Hakspiel-Segura 2009). The decline of APP and an increase of diatoms observed at El Tortugón suggest that episodic nutrient input provides diatoms with a nutrient uptake advantage. This agrees with observations in similar ecosystems, where shifts from picoplankton to diatoms prevail in phytoplankton communities after an influx of nutrients (Šilović et al. 2012). Observation of the effects of heavy rainfall and subsequent runoff, with resultant nutrient input, utilized by fast-growing diatoms in domination over other phytoplankton groups (Martínez-López et al. 2007) support this concept.
Levels of DIP in the lagoon did not show the same seasonal trend reported in 2002 and 2005 (Magaña-Álvarez 2004; Poot-Delgado 2006), when the highest concentrations were recorded during the autumn/winter season or were associated with the summer rainy season. The peak of DIP at the entrance of Laguna Macapule preceded that at El Tortugón before the rainy season, suggesting that diatom blooms controlled phosphorus levels, subsequent input of organic matter derived from the diatoms, and fast regeneration of phosphorus compounds. A similar situation was observed during an intense bloom of the diatom Asterionella glacialis off the coast of Kalpakkam, Tamil Nadu, India, with decrease in nitrate and silicate and increase in phosphate (Satpathy and Nair 1996). Higher DIP during warming of the water column, related to a mineralization process, is common in estuaries and shallow coastal lagoons (Morris et al. 1981; Pant and Reddy 2001; van der Zee and Chou 2004).
Whether APP has a preference for a specific type of nitrogen is not clear. Harrison et al. (1996) found that picophytoplankton prefer NH4 +, whereas Glover et al. (1988) and Bird and Wyman (2003) demonstrated that they will consume nitrate and nitrite in the absence of other nitrogen sources. Other studies showed APP uptake of nitrogen and phosphorus from a variety of inorganic and organic compounds (Bjorkman and Karl 1994; Zubkov et al. 2003). Therefore, when NH4 + is insufficient to meet N demand, APP utilizes urea as an organic nitrogen source after internal biological hydrolyzation to NH4 + using urease (Berns et al. 1966; Collier et al. 1999). This is more readily accomplished than uptake of oxidized forms of nitrogen (Solomon et al. 2010 and references therein). In Laguna Macapule, urea was more prevalent than dissolved inorganic forms of nitrogen during spring-early autumn, suggesting that it served as a primary source of nitrogen when inorganic nitrogen was limited (Poot-Delgado 2006). It seems clear that urea may be an important player in primary production of this highly impacted lagoon, under limited inorganic nitrogen conditions.
Spatial differences in urea distribution defined that APP was positively correlated with urea only at the entrance to the lagoon (Spearman; p < 0.05). At this site during spring-early autumn, higher concentrations of urea also correlated with higher abundances of microzooplankton. This indicates that zooplankton excretion was the urea source (L’Helguen et al. 2005). However, urea generally is present in marine waters at levels below 1 μM-N (Solomon et al. 2010), which is substantially lower than observed (up to 35 μM-N), suggesting that this organic nitrogen derives from an external source and needs to be accounted for with seasonal variability of nutrient concentrations.
Urea concentrations at Laguna Macapule were comparable to other coastal systems where agricultural (Glibert et al. 2006) or other organic impacts are present (Gutiérrez-Mendieta et al. 1998). Higher values from March through October point to effluent discharge from shrimp farms. Urea is used as a nitrogen fertilizer (Lyle-Fritch et al. 2006) to stimulate plankton production in the ponds, as well as being produced by shrimp excretion. Water exchange is a dominant factor in shrimp production from March through October, when discharge from >5000 ha of ponds (Páez-Osuna et al. 2007) inputs large volumes of shrimp excretion and feed waste into the ecosystem (Páez-Osuna et al. 2003). Other sources could be municipal wastes from the city of Guasave (~80,000 inhabitants) or agriculture where urea-based herbicides or fertilizers are used. Shrimp farms occur along the margin of the lagoon, and the effluent enters the lagoon through several drains. However, the channel at El Tortugón contains only a limited discharge related to aquaculture activities. Thus, lagoon’s internal circulation predominantly concentrates and transports urea toward the lagoon inlet (Escobedo-Urías com. pers.) where lower abundances of APP are present in comparison to El Tortugón, explaining the strong presence of urea at the entrance of the lagoon. This situation is contrary to the original supposition that this site was less impacted.
The paradigm of inorganic N being the limiting nutrient in marine ecosystems apparently is not applicable in the Laguna Macapule ecosystem since significantly negative correlation was observed between APP and N:P (Spearman; p < 0.05). This could be explained by their relatively high affinity to low NID concentrations (Agawin et al. 2000) or more likely because it appears that the APP are using organic nitrogen to overcome limiting conditions (N:P = ~4) under dissolved inorganic nitrogen concentrations under 1.5 μM. Here, urea seems to be, at least for APP, a crucial nitrogen source. Urea is one of the regenerated forms of nitrogen, thus nutrient availability (internal biogeochemical rates), not concentration, is more relevant to limitations of net ecosystem production (Smith 1984). Further investigation is needed to assess the relative importance of biogeochemical rates and biological interactions in this impacted lagoon. From the perspective of this study, our results suggest, in agreement with other research teams (Souchu et al. 2010), that a total nutrient-based approach including dissolved organic nitrogen likely constitutes the most appropriate approach for future studies in this region and similar ones around the world.
Autotrophic picoplankton were described and quantified over a complete annual cycle for the first time in the Gulf of California. APP was the numerically dominant and the second greatest contributor to biomass of the phytoplankton fractions throughout the year, reaching peak levels in spring–early autumn (up to ~0.6 × 109 cells L−1). The interplay between natural (temperature and grazing) and anthropogenic forcing’s contributed to delineate the seasonality of APP, thereby promoting high densities in the spring–early autumn. The shift to low abundances of the APP may also result from zooplankton grazing or nutrient competition. Therefore, microphytoplankton blooms occur in winter when they outcompete APP for nutrient resources. Statistical relationships between APP and small-size zooplankton groups suggest that a considerable part of the pool of organic matter is retained in the microbial loop, instead of passing through to the productive herbivorous trophic web. Positive relationship with urea (bottom-up control) from aquaculture appears to contribute to maintaining high densities of APP in spring–early autumn. Increase in abundance of APP with a N:P = ~4 supports that urea is the sustaining nutrient source for this small size autotrophic component. Thus, a total nutrient-based approach likely constitutes the most suitable tool for establishing nitrogen limitation of biological production in this ecosystem as well as for improving criteria for management or restoration. Further investigation is needed to assess the relative importance of biogeochemical rates and biological interactions in this impacted lagoon.
This study was funded by the Dirección de Estudios de Posgrado e Investigación, Instituto Politécnico Nacional (SIP grant 20082265). A.M.L., D.E.U., and B.G.A. are COFAA-IPN and EDI-IPN fellows of the Instituto Politécnico Nacional of Mexico. C.H.S. received fellowships from PIFI-IPN and Consejo Nacional de Ciencia y Tecnología (CONACYT).
AML was involved in the framing hypotheses and experimental design, data interpretation, and manuscript preparation. CHS participated in the design of the study and carried out laboratory quantifications of microorganisms as well as data analysis and participated in the draft manuscript preparation. DEU carried out the fieldwork of the study and laboratory nutrients analysis, and BGA participated in the laboratory quantifications of microorganisms; both helped to draft the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
- Agawin NSR, Duarte CM, Agusti S (1998) Growth and abundance of Synechococcus sp in a Mediterranean Bay: seasonality and relationship with temperature. Mar Ecol Prog Ser 170:45–53View ArticleGoogle Scholar
- Agawin NSR, Duarte CM, Agusti S (2000) Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnol Oceanogr 45:591–600View ArticleGoogle Scholar
- Álvarez-Borrego S, Rivera JA, Gaxiola-Castro G, Acosta-Ruiz MD, Schwartzlose RA (1978) Nutrientes en el Golfo de California. Cienc Mar 5:53–71Google Scholar
- Ayala-Rodríguez GA (2008) Grupos funcionales del fitoplancton y estado trófico del sistema lagunar Topolobampo-Ohuira-Santa María MSc Dissertation. CICIMAR, La Paz, BCS MéxicoGoogle Scholar
- Badylak S, Phlips EJ (2004) Spatial and temporal patterns of phytoplankton composition in a subtropical coastal lagoon, the Indian River Lagoon, Florida, USA. J Plankton Res 26:1229–1247View ArticleGoogle Scholar
- Barber RT (2007) Oceans. Picoplankton do some heavy lifting. Science 315:838–40View ArticleGoogle Scholar
- Barber RT, Hiscock MR (2006) A rising tide lifts all phytoplankton: growth response of other phytoplankton taxa in diatom-dominated blooms. Global Biogeochem Cycles 20:GB4S03 doi:10.1029/2006GB002726.
- Bernal G, Ripa P, Herguera JC (2001) Oceanographic and climatic variability in the lower Gulf of California: links with the tropics and north Pacific. Cienc Mar 27:595–617Google Scholar
- Berns DS, Holohan P, Scott E (1966) Urease activity in blue-green algae. Science 152:1077–1078View ArticleGoogle Scholar
- Bird C, Wyman M (2003) Nitrate/nitrite assimilation system of the marine picoplanktonic cyanobacterium Synechococcus sp strain WH 8103: effect of nitrogen source and availability on gene expression. Appl Environ Microbiol 69:7009–7018View ArticleGoogle Scholar
- Bjorkman K, Karl DM (1994) Bioavailability of inorganic and organic phosphorus-compounds to natural assemblages of microorganisms in Hawaiian coastal waters. Mar Ecol Prog Ser 111:265–273View ArticleGoogle Scholar
- Bojanic N, Šolic M, Krstulovic N, Šestanovic S, Gladan Ž, Marasovic I, Brautovic I (2006) The role of ciliates within the microbial food web in the eutrophicated part of Kaštela Bay (middle Adriatic Sea). Sci Mar 70:431–442View ArticleGoogle Scholar
- Bratbak G, Jacquet S, Larsen A, Pettersson LH, Sazhin AF, Thyrhaug R (2011) The plankton community in Norwegian coastal waters - abundance, composition, spatial distribution and diel variation. Cont Shelf Res 31:1500–1514View ArticleGoogle Scholar
- Cai YM, Ning XN, Liu CG, Hao Q (2007) Distribution pattern of photosynthetic picoplankton and heterotrophic bacteria in the northern South China Sea. J Integr Plant Biol 49:282–298View ArticleGoogle Scholar
- Calvo-Díaz A, Morán XAG (2006) Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay. Aquat Microb Ecol 42:159–174View ArticleGoogle Scholar
- Caron DA (1983) Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures. Appl Environ Microbiol 46:491–498Google Scholar
- Caron DA, Lim EL, Miceli G, Waterbury J, Valois F (1991) Grazing and utilization of chroococcoid cyanobacteria and heterotrophic bacteria by protozoa in laboratory. Mar Ecol Prog Ser 46:191–201Google Scholar
- Castro R, Mascarenhas AS, Durazo R, Collins CA (2000) Seasonal variation of the temperature and salinity at the entrance to the Gulf of California, Mexico. Cienc Mar 26:561–583Google Scholar
- Chang J, Lin KH, Chen KM, Gong GC, Chiang KP (2003) Synechococcus growth and mortality rates in the East China Sea: range of variations and correlation with environmental factors. Deep Sea Res Part II 50:1265–1278View ArticleGoogle Scholar
- Chiang KP, Kuo MC, Chang J, Wang RH, Gong GC (2002) Spatial temporal variation of the Synechococcus population in the East China Sea its contribution to phytoplankton biomass. Cont Shelf Res 22:3–13View ArticleGoogle Scholar
- Chisholm SW, Olson RJ, Zettler ER, Waterbury J, Goericke R, Welschmeyer N (1988) A novel free-living prochlorophyte occurs at high cell concentrations in the oceanic euphotic zone. Nature 334:340–343View ArticleGoogle Scholar
- Christaki U, Dolan JR, Pelegri S, Rassoulzadegan F (1998) Consumption of picoplankton size particles by marine ciliates: effects of physiological state of the ciliate and particle quality. Limnol Oceanogr 43:458–464View ArticleGoogle Scholar
- Collier JL, Brahamsha B, Palenik B (1999) The marine cyanobacterium Synechococcus sp WH7805 requires urease (urea amidohydrolase, EC 3\5\1\5) to utilize urea as a nitrogen source: molecular-genetic and biochemical analysis of the enzyme. Microbiology 145:447–459View ArticleGoogle Scholar
- Detmer AE, Giesenhagen HC, Trenkel VM, dem Venne HA, Jochem FJ (1993) Phototrophic and heterotrophic pico- and nanoplankton in anoxic depths of the central Baltic Sea. Mar Ecol Prog Ser 99:197–203View ArticleGoogle Scholar
- Díaz-Hernández C, Maske H (2000) Abundance of coccoid cyanobacteria, hydrographic parameters and the possible underestimation of in situ chlorophyll a in the northern Gulf of California and Mexican California current. Ciencias Marinas 26:441–461Google Scholar
- Escobedo-Urías D (2010) Diagnóstico y descripción del proceso de eutrofización en lagunas costeras del norte de Sinaloa. IPN-CICIMAR La Paz, BCS México, Ph.D. DissertationGoogle Scholar
- Escobedo-Urías D, Hernández-Real MT, Herrera-Moreno N, Chiquete-Ozono AY (1999) Calidad bacteriológica del sistema lagunar de San Ignacio-Navachiste, Sinaloa. Cienc Mar 3:17–27Google Scholar
- Escobedo-Urías D, Martínez-López A, Jiménez-Illescas A, Ulloa-Pérez AE, Zavala-Norzagaray A (2007) Intercambio de carbono orgánico particulado del Sistema Lagunar San Ignacio-Navachiste, Sinaloa con el mar adyacente. In: Hernández de la Torre B, Gaxiola-Castro G (eds) Carbono en ecosistemas acuáticos mexicanos. INE-SEMARNAT, Mexico City, pp 171–186Google Scholar
- Flombaum P, Gallegos JL, Gordillo RA, Rincón J, Zabala LL, Jiao N, Karl DM, Li WKM, Lomas MW, Veneziano D, Vera CS, Vrugt JA, Martiny AC (2013) Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci USA 110:9824–9829
- Gaulke AK, Michael W, Paerl H (2010) Picophytoplankton: a major contributor to planktonic biomass and primary production in a eutrophic, river-dominated estuary. Estuar Coast Shelf Sci 90:45–54View ArticleGoogle Scholar
- Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463View ArticleGoogle Scholar
- Glover HE, Prézelin B, Campbell L, Wyman M, Garside C (1988) A nitrate dependent Synechococcus bloom in surface Sargasso Sea water. Nature 331:161–163View ArticleGoogle Scholar
- Gunbua V, Paphavasit N, Piumsomboon A (2012) Temporal and spatial variations of heterotrophic bacteria, pico- and nano-phytoplankton along the Bangpakong Estuary of Thailand. Trop Nat Hist 12:55–73Google Scholar
- Gutiérrez-Mendieta F, Torres-Mejía H, Torres-Alvarado R (1998) Importancia de la determinación de la urea en ecosistemas costeros. Hidrobiológica 8:155–164Google Scholar
- Hakspiel-Segura C (2009) Variación estacional de la trama trófica microbiana en la Laguna de Macapule. CICIMAR, La Paz, BCS México, Sinaloa MSc DissertationGoogle Scholar
- Harrison WG, Harris LR, Irwin BD (1996) The kinetics of nitrogen utilization in the oceanic mixed layer: nitrate and ammonium interactions at nanomolar concentrations. Limnol Oceanogr 41:16–32View ArticleGoogle Scholar
- Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200View ArticleGoogle Scholar
- Jardillier L, Zubkov MV, Pearman J, Scanlan DJ (2010) Significant CO2 fixation by small prymnesiophytes in the subtropical and tropical northeast Atlantic Ocean. ISME J 4:1180–1192. doi:10.1038/ismej.2010.36 View ArticleGoogle Scholar
- Johnson PW, Sieburth JMN (1979) Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol Oceanogr 24:928–935View ArticleGoogle Scholar
- Johnson PW, Sieburth JMN (1982) In-situ morphology and occurrence of eukaryotic phototrophs of bacterial size in the picoplankton of estuarine and oceanic waters. J Phycol 18:318–327View ArticleGoogle Scholar
- Kobori H, Taga N (1979) Phosphatase activity and its role in the mineralization of organic phosphorus in coastal seawater. J Exp Mar Biol Ecol 36:23–39View ArticleGoogle Scholar
- L’Helguen S, Slawyk G, Le Corre P (2005) Seasonal patterns of urea regeneration by size fractionated microheterotrophs in well-mixed temperate coastal waters. J Plankton Res 27:263–270View ArticleGoogle Scholar
- Lai DYF, Lam KC (2008) Phosphorus retention and release by sediments in the eutrophic Mai Po Marshes, Hong Kong. Mar Pollut Bull 57:349–356View ArticleGoogle Scholar
- Linacre-Rojas LP, Landry MR, Cajal-Medrano R, Lara-Lara JR, Hernández-Ayón JM, Mouriño-Pérez RR, García-Mendoza EM, Bazán-Guzmán DC (2010) Picoplankton dynamics during contrasting seasonal oceanographic conditions at a coastal upwelling station off Northern Baja California, México. J Plankton Res 31:1–19Google Scholar
- Lund J, Kipling C, Le Cren E (1958) The inverted microscope method of estimating algal numbers and the statistical basis of estimations by counting. Hydrobiologia 11:143–170View ArticleGoogle Scholar
- Lyle-Fritch LP, Romero-Beltran E, Páez-Osuna F (2006) A survey on use of the chemical and biological products for shrimp farming in Sinaloa (NW Mexico). Aquacult Eng 35:135–146View ArticleGoogle Scholar
- MacIsaac EA, Stockner JG (1993) Enumeration of phototrophic picoplancton by autofluorescence. In: Kemp P, Sherr B, Sherr E, Cole J (eds) Handbook of Methods in Aquatic Microbial Ecology. Lewis Publishers, Boca Raton, FL, pp 187–197Google Scholar
- Magaña-Álvarez ME (2004) Distribución de nutrientes y su efecto en el nivel trófico de la laguna Macapule. CIIDIR, Guasave, Sinaloa, México, Sinaloa MSc DissertationGoogle Scholar
- Marshall HG (2002) Autotrophic picoplankton: their presence and significance in marine and freshwater ecosystems. Va J Sci 53:13–33Google Scholar
- Martínez-López A, Escobedo-Urías D, Reyes-Salinas A, Hernández-Real MA (2007) Phytoplankton response to nutrients runoff in a lagoon system in the Gulf of California. Hidrobiología 17:101–112Google Scholar
- Martínez-López A, Escobedo-Urías DC, Ulloa-Pérez AE, Aguirre R (2008) Dynamics of a Prorocentrum minimum bloom along the northern coast of Sinaloa, Mexico. Cont Shelf Res 28:1693–1701View ArticleGoogle Scholar
- Montagnes DJS, Lynn DH, Roff JC, Taylor WD (1988) The annual cycle of heterotrophic planktonic ciliates in waters surrounding the Isles of Shoals Gulf of Maine: an assessment of their trophic role. Mar Biol 99:21–30View ArticleGoogle Scholar
- Morris AW, Bale AJ, Howlan RJM (1981) Nutrient distributions in an estuary: evidence of chemical precipitation of dissolved silicate and phosphate. Estuar Coast Shelf Sci 12:205–216View ArticleGoogle Scholar
- Mulvenna PF, Savidge G (1992) A modified manual method for the determination of urea in seawater using diacetylmonoxime reagent. Estuar Coast Shelf Sci 34:429–438View ArticleGoogle Scholar
- Murrell MC, Caffrey JM (2005) High cyanobacterial abundance in three northeastern Gulf of Mexico estuaries. Gulf Caribb Res 17:95–106View ArticleGoogle Scholar
- Murrell MC, Lores EM (2004) Phytoplankton and zooplankton seasonal dynamics in subtropical estuary: Importance of cyanobacteria. Journal of Plankton Research 26:371–382View ArticleGoogle Scholar
- Páez-Osuna F, Gracia A, Flores-Verdugo F, Lyle-Fritch LP, Alonso-Rodríguez R, Roque A, Ruiz-Fernández AC (2003) Shrimp aquaculture development and the environment in the Gulf of California ecoregion. Mar Pollut Bull 46:806–815View ArticleGoogle Scholar
- Páez-Osuna F, Ramírez-Reséndiz G, Ruiz-Fernández AC, Soto-Jiménez MF (2007) La contaminación por nitrógeno y fósforo en Sinaloa: Flujos, Fuentes, efectos y opciones de manejo Serie Lagunas Costeras de Sinaloa UNAM-ICMYL-Colegio de Sinaloa-SEMARNAT-CONACYT, MéxicoGoogle Scholar
- Pagano M, Champalbert G, Aka M, Kouassi E, Arfi R, Got P, Troussellier M, N’Doura EH, Corbin D, Bouvy M (2006) Herbivorous and microbial grazing pathways of metazooplankton in the Senegal River Estuary (West Africa). Estuar Coast Shelf Sci 67:369–381View ArticleGoogle Scholar
- Palenik B, Ren, Dupont Q, Myers CL, Heidelberg GS, Badger JF, Madupu J.H, Nelson R, Brinkac WC, Dodson LM, Durkin RJ, Daugherty AS, Sullivan SC, Khouri SA, Mohamoud H, Halpin Y, Paulsen R (2006) IT Genome sequence of Synechococcus CC9311: insights into adaptation to a coastal environment. Proceedings of the National Academy of Sciences of USA 103:13555–13559View ArticleGoogle Scholar
- Pant HK, Reddy KR (2001) Phosphorus sorption characteristics of estuarine sediments under different redox. J Environ Qual 30:1474–1480View ArticleGoogle Scholar
- Phlips EJ, Badylak S, Lynch TC (1999) Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon. Limnol Oceanogr 44:1166–1175View ArticleGoogle Scholar
- Poot-Delgado C (2006) Estructura de la comunidad fitoplanctónica con énfasis en las especies tóxicas y/o nocivas de laguna de Macapule. CICIMAR, La Paz, BCS, México, Sinaloa MSc DissertationGoogle Scholar
- Rassoulzadegan F, Laval-Peuto M, Sheldon RW (1988) Partitioning of the food ration of marine ciliates between pico- and nanoplankton. Hydrobiologia 159:75–88View ArticleGoogle Scholar
- Raven JA (1998) The twelfth Tansley lecture. Small is beautiful: the picophytoplankton. Funct Ecol 12:503–513View ArticleGoogle Scholar
- Sakamoto T, Bryant DA (1998) Growth at low temperature causes nitrogen limitation in the cyanobacterium Synechococcus sp PCC 7002. Arch Microbiol 169:10–19View ArticleGoogle Scholar
- Sakka-Hlaili A, Grami B, Mabrouk HH, Gosselin M, Hamel D (2007) Phytoplankton growth and microzooplankton grazing rates in a restricted Mediterranean lagoon (Bizerte Lagoon, Tunisia). Mar Biol 151:767–783View ArticleGoogle Scholar
- Sanders RW (1987) Tintinnids and other microzooplankton—seasonal distributions and relationships to resources and hydrography in a Maine estuary. J Plankton Res 9:65–77View ArticleGoogle Scholar
- Satpathy KK, Nair KVK (1996) Occurrence of phytoplankton bloom and its effect on coastal water quality. Indian J Mar Sci 25:145–147Google Scholar
- Šilović T, Bosak S, Jakši Ž, Fuks D (2012) Seasonal dynamics of the autotrophic community in the Lim Bay (NE Adriatic Sea). Acta Adriat 53:41–56Google Scholar
- Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnol Oceanogr 29:1149–1160View ArticleGoogle Scholar
- Smith W, Beet A, Solow AR (1998) Testing for shifts in the vertical distribution of plankton using a robust Kolmogorov-Smirnov like statistic. J Agric Biol Environ Stat 3:421–429View ArticleGoogle Scholar
- Solomon CM, Collier JL, Berg GM, Glibert PM (2010) Role of urea in microbial metabolism in aquatic systems: a biochemical and molecular review. Aquat Microb Ecol 57:69–88Google Scholar
- Solórzano L (1969) Determination of ammonia in natural water by the phenolhypochlorite method. Limnol Oceanogr 14:799–801View ArticleGoogle Scholar
- Souchu P, Bec B, Smith VH, Laugier T, Fiandrino A, Benau L, Orsoni V, Collos Y, Vaquer A (2010) Patterns in nutrient limitation and chlorophyll a along an anthropogenic eutrophication gradient in French Mediterranean coastal lagoons. Can J Fish Aquat Sci 67:743–753View ArticleGoogle Scholar
- Strickland JD, Parsons TR (1972) A practical handbook for the sea water analysis. In: Bulletin of the Fisheries Research Board of Canada, Ottawa, 2nd edn., p 310Google Scholar
- Sutherland TF, Leonard C, Taylor FJR (1992) A segmented pipe sampler for integrated profiling of the upper water column. J Plankton Res 14:915–923View ArticleGoogle Scholar
- Taylor AG, Goericke R, Landry MR, Selph KE, Wick DA, Roadman MJ (2012) Sharp gradients in phytoplankton community structure across a frontal zone in the California Current Ecosystem. Journal of Plankton Research 34:778–789View ArticleGoogle Scholar
- Timmermans KR, Van der Wagt B, Veldhuis MJW, Maatman A, de Baar HJW (2005) Physiological responses of three species of marine pico-phytoplankton to ammonium, phosphate, iron and light limitation. J Sea Res 53:109–120View ArticleGoogle Scholar
- Toshikazu S, Chieko M (2007) Ecological balance between ciliate plankton and its prey candidates, pico- and nanoplankton, in the East China Sea. Hydrobiologia 586:403–410View ArticleGoogle Scholar
- Urrutxurtu I, Orive E, Sota A (2003) Seasonal dynamics of ciliated protozoa and their potential food in a eutrophic estuary (Bay of Biscay). Estuar Coast Shelf Sci 57:1169–1182View ArticleGoogle Scholar
- van der Zee C, Chou L (2004) Seasonal cycling of phosphorus in the Southern Bight of the North Sea. Biogeosci Discuss 1:681–707View ArticleGoogle Scholar
- Verdugo-Díaz G, Martínez-López A, Gárate-Lizárraga I (2010) Ecological indicators of the phytoplankton community structure in Bahía Concepción México. Oceánides 25:95–102Google Scholar
- Waterbury JB, Watson SW, Guillard RL, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic cyanobacterium. Nature 277:293–294View ArticleGoogle Scholar
- Xu K, Choi JK, Lei Y, Yang EJ (2011) Marine ciliate community in relation to eutrophication of coastal waters in the Yellow Sea. Chin J Oceanol Limnol 29:118–127View ArticleGoogle Scholar
- Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, N.J, p 929Google Scholar
- Zubkov M, Fuchs B, Tarran G, Burkill P, Amann R (2003) High rate of uptake of organic nitrogen compounds by Prochlorococcus cyanobacteria as a key to their dominance in oligotrophic oceanic waters. Appl Environ Microbiol 69:1299–1304View ArticleGoogle Scholar
- Zwirglmaier K, Jardillier L, Ostrowski M, Mazard S, Garczarek L, Vaulot D, Not F, Massana R, Ulloa O, Scanlan DJ (2008). Global phylogeography of marine Synechococcus and Prochlorococcus reveals a distinct partitioning of lineages among oceanic biomes. Environ Microbiol 10:147–161Google Scholar