Influence of agriculture and aquaculture activities on the response of autotrophic picoplankton in Laguna Macapule, Gulf of California (Mexico)

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 170:45–53 Agawin NSR, Duarte CM, Agusti S (2000) Nutrient and temperature control of the contribution of picoplankton to phytoplankton biomass and production. Limnol Oceanogr 45:591–600 Álvarez-Borrego S, Rivera JA, Gaxiola-Castro G, Acosta-Ruiz MD, Schwartzlose RA (1978) Nutrientes en el Golfo de California. Cienc Mar 5:53–71 Ayala-Rodríguez GA (2008) Grupos funcionales del fitoplancton y estado trófico del sistema lagunar Topolobampo-Ohuira-Santa María MSc Dissertation. CICIMAR, La Paz, BCS México 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 26:1229–1247 Barber RT (2007) Oceans. Picoplankton do some heavy lifting. Science 315:838–40 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 27:595–617 Berns DS, Holohan P, Scott E (1966) Urease activity in blue-green algae. Science 152:1077–1078 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 69:7009–7018 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 111:265–273 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 70:431–442 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 31:1500–1514 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 49:282–298 Calvo-Díaz A, Morán XAG (2006) Seasonal dynamics of picoplankton in shelf waters of the southern Bay of Biscay. Aquat Microb Ecol 42:159–174 Caron DA (1983) Technique for enumeration of heterotrophic and phototrophic nanoplankton, using epifluorescence microscopy, and comparison with other procedures. Appl Environ Microbiol 46:491–498 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 46:191–201 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 26:561–583 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 50:1265–1278 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 22:3–13 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 334:340–343 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 43:458–464 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 145:447–459 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 99:197–203 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 26:441–461 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. Dissertation 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 3:17–27 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 171–186 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 90:45–54 Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea—a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463 Glover HE, Prézelin B, Campbell L, Wyman M, Garside C (1988) A nitrate dependent Synechococcus bloom in surface Sargasso Sea water. Nature 331:161–163 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 12:55–73 Gutiérrez-Mendieta F, Torres-Mejía H, Torres-Alvarado R (1998) Importancia de la determinación de la urea en ecosistemas costeros. Hidrobiológica 8:155–164 Hakspiel-Segura C (2009) Variación estacional de la trama trófica microbiana en la Laguna de Macapule. CICIMAR, La Paz, BCS México, Sinaloa MSc Dissertation 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 41:16–32 Hoppe HG (2003) Phosphatase activity in the sea. Hydrobiologia 493:187–200 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 Johnson PW, Sieburth JMN (1979) Chroococcoid cyanobacteria in the sea: a ubiquitous and diverse phototrophic biomass. Limnol Oceanogr 24:928–935 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 18:318–327 Kobori H, Taga N (1979) Phosphatase activity and its role in the mineralization of organic phosphorus in coastal seawater. J Exp Mar Biol Ecol 36:23–39 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 27:263–270 Lai DYF, Lam KC (2008) Phosphorus retention and release by sediments in the eutrophic Mai Po Marshes, Hong Kong. Mar Pollut Bull 57:349–356 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 31:1–19 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 11:143–170 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 35:135–146 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 187–197 Magaña-Álvarez ME (2004) Distribución de nutrientes y su efecto en el nivel trófico de la laguna Macapule. CIIDIR, Guasave, Sinaloa, México, Sinaloa MSc Dissertation Marshall HG (2002) Autotrophic picoplankton: their presence and significance in marine and freshwater ecosystems. Va J Sci 53:13–33 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 17:101–112 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 28:1693–1701 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 99:21–30 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 12:205–216 Mulvenna PF, Savidge G (1992) A modified manual method for the determination of urea in seawater using diacetylmonoxime reagent. Estuar Coast Shelf Sci 34:429–438 Murrell MC, Caffrey JM (2005) High cyanobacterial abundance in three northeastern Gulf of Mexico estuaries. Gulf Caribb Res 17:95–106 Murrell MC, Lores EM (2004) Phytoplankton and zooplankton seasonal dynamics in subtropical estuary: Importance of cyanobacteria. Journal of Plankton Research 26:371–382 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 46:806–815 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, México 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 67:369–381 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 103:13555–13559 Pant HK, Reddy KR (2001) Phosphorus sorption characteristics of estuarine sediments under different redox. J Environ Qual 30:1474–1480 Phlips EJ, Badylak S, Lynch TC (1999) Blooms of the picoplanktonic cyanobacterium Synechococcus in Florida Bay, a subtropical inner-shelf lagoon. Limnol Oceanogr 44:1166–1175 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 Dissertation Rassoulzadegan F, Laval-Peuto M, Sheldon RW (1988) Partitioning of the food ration of marine ciliates between pico- and nanoplankton. Hydrobiologia 159:75–88 Raven JA (1998) The twelfth Tansley lecture. Small is beautiful: the picophytoplankton. Funct Ecol 12:503–513 Sakamoto T, Bryant DA (1998) Growth at low temperature causes nitrogen limitation in the cyanobacterium Synechococcus sp PCC 7002. Arch Microbiol 169:10–19 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 151:767–783 Sanders RW (1987) Tintinnids and other microzooplankton—seasonal distributions and relationships to resources and hydrography in a Maine estuary. J Plankton Res 9:65–77 Satpathy KK, Nair KVK (1996) Occurrence of phytoplankton bloom and its effect on coastal water quality. Indian J Mar Sci 25:145–147 Šilović T, Bosak S, Jakši Ž, Fuks D (2012) Seasonal dynamics of the autotrophic community in the Lim Bay (NE Adriatic Sea). Acta Adriat 53:41–56 Smith SV (1984) Phosphorus versus nitrogen limitation in the marine environment. Limnol Oceanogr 29:1149–1160 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 3:421–429 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 57:69–88 Solórzano L (1969) Determination of ammonia in natural water by the phenolhypochlorite method. Limnol Oceanogr 14:799–801 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 67:743–753 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 310 Sutherland TF, Leonard C, Taylor FJR (1992) A segmented pipe sampler for integrated profiling of the upper water column. J Plankton Res 14:915–923 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 34:778–789 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 53:109–120 Toshikazu S, Chieko M (2007) Ecological balance between ciliate plankton and its prey candidates, pico- and nanoplankton, in the East China Sea. Hydrobiologia 586:403–410 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 57:1169–1182 van der Zee C, Chou L (2004) Seasonal cycling of phosphorus in the Southern Bight of the North Sea. Biogeosci Discuss 1:681–707 Verdugo-Díaz G, Martínez-López A, Gárate-Lizárraga I (2010) Ecological indicators of the phytoplankton community structure in Bahía Concepción México. Oceánides 25:95–102 Waterbury JB, Watson SW, Guillard RL, Brand LE (1979) Widespread occurrence of a unicellular, marine, planktonic cyanobacterium. Nature 277:293–294 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 29:118–127 Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Upper Saddle River, N.J, p 929 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 69:1299–1304 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 10:147–161