Revista Ciencias Marinas y Costeras ISSN: 1659-455X [email protected] Universidad Nacional

García-Rojas, Andrea; Vega Bolaños, Hannia Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya, Costa Rica Revista Ciencias Marinas y Costeras, vol. 8, núm. 2, julio-diciembre, 2016, pp. 29-45 Universidad Nacional Heredia, Costa Rica

Available in: http://www.redalyc.org/articulo.oa?id=633766725002

How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya, Costa Rica

Cambios estacionales del fitoplancton en el área marina de pesca responsable de Paquera-Tambor, Golfo de Nicoya, Costa Rica

Andrea García-Rojas1* & Hannia Vega Bolaños1

ABSTRACT The implementation of Marine Areas for Responsible Fishing (MARF) is a tool for fisheries management; therefore, baseline studies play an important role in understanding the ecological dynamics from the bases of the food web in the MARF. The aim of this study was to identify the abundance of the phytoplankton communities associated with the MARF to determine the seasonal changes between abiotic variables and phytoplankton in the Paquera-Tambor MARF, Gulf of Nicoya, Costa Rica. Monthly sampling (September 2013 to August 2014) was performed for physical-chemical factors and phytoplankton. The data showed a temporal variation of both environmental factors and the phytoplankton community. The most representative microalgae were diatoms and dinoflagellates with a richness of 51 and 32 species, respectively, where the presence of some algal bloom forming species such as Cochlodinium catenatum was highlighted, with a concentration of 5.85x104 cells L-1. Regarding diatoms and parameters such as Secchi disk depth (r = -0.558) and the percentage of oxygen saturation (r = -0.490), a negative correlation was found due to climate variability in the area. Zooplanktonic tintinnids were identified and showed a positive correlation with diatoms (r = 0.433). A fundamental ecosystem dynamic was evident for the trophic development of the Tambor-Paquera-MARF, which underpins the importance of the fishing zone and reflects the relevance of continued biotic and abiotic monitoring for the area.

Keywords: Microalgae, seasonal changes, Marine Areas for Responsible Fishing, Gulf of Nicoya, Costa Rica.

RESUMEN La implementación de Áreas Marinas de Pesca Responsable (AMPR) es una herramienta para el ordenamiento pesquero, por ello, los estudios de línea base juegan un rol importante para comprender la dinámica ecológica desde las bases de la red trófica en las AMPR. El objetivo de este trabajo fue caracterizar la abundancia de los grupos taxonómicos del fitoplancton en el AMPR-Paquera-Tambor, para la determinación de cambios estacionales entre variables abióticas y el fitoplancton. Se realizó un muestreo mensual (de septiembre-2013 a agosto-2014) para la toma de muestras de factores fisicoquímicos, así como de microalgas planctónicas. Los datos evidenciaron una variación temporal tanto de los factores ambientales como del fitoplancton. Las microalgas más representativas fueron las diatomeas y los dinoflagelados con una riqueza de 51

1 Juan Bertoglia Richards Marine Biology Station, School of Biological Sciences, Universidad Nacional, Costa Rica. [email protected]*; hannia.vega.bolañ[email protected]

Recibido: 27 de julio de 2015 Corregido: 3 de junio de 2016 Aceptado: 15 de junio de 2016

Licencia Creative Commons DOI: http://dx.doi.org/10.15359/revmar.8-2.2 Atribución No Comercial Compartir Igual 4.0 Internacional Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 29 García-Rojas & Vega Bolaños y 32 especies, respectivamente, donde se resalta la presencia de algunas especies productoras de florecimientos algales comoCochlodinium catenatum con una concentración de 5.85x104cél L-1. Con respecto a las diatomeas y los parámetros, como la profundidad del disco Secchi (r = -0.558) y el porcentaje de saturación de oxígeno (r = -0.490), se reflejó una correlación negativa debido a la variabilidad climática de la zona. Se identificaron organismos del grupo zooplanctónico de los tintínidos, los cuales presentaron una correlación positiva con las diatomeas (r = 0.433). Se evidenció una dinámica ecosistémica fundamental para el desarrollo trófico del AMPR-Paquera- Tambor, que fundamenta la importancia pesquera de la zona y refleja la relevancia de continuar con un monitoreo biótico y abiótico para la zona.

Palabras claves: Microalgas, cambios estacionales, áreas marinas de pesca responsable, Golfo de Nicoya, Costa Rica.

INTRODUCTION designate an area as a MARF, includ- In Costa Rica, overfishing and the ing baseline studies, which represent lack of planning in the use of coastal a fundamental tool to learn about the resources has promoted the implemen- biodiversity and environmental state tation of Marine Areas for Responsible of the ecosystem to be managed. As a Fishing (MARF), which are marine result, the analysis of the phytoplank- areas demarcated and managed by ton community is important, since this coastal communities together with the group of organisms represents the plant relevant authorities in order to regu- material of marine plankton, and they late fishing activities with a better use are the primary producers of the aquat- of resources in the long term (MAG, ic ecosystems, which bears ecological 2009). MARFs provide some advan- importance since this is the basis of the tages for fisheries management. For marine food chain (Valiela, 1995; Ro- instance, they reduce conflict in the use chelle-Newall et al. 2011). This group of fishing gear harmful to marine bio- is made up of a wide variety of taxa, diversity that affect the abundance of including the Cyanophyta, Prochlo- organisms. Fishing efforts are reduced rophyta, Chlorophyta, Euglenophyta, in recruitment areas, which leads to Dinophyta, Haptophyta, Cryptophyta, conservation of sites and resources. and Chromophyta (Bacillariophyceae, There is a better collection of fisher- Chrysophyceae, Raphidophyte, and ies data which helps improve policies Prymnesiophyceae), with diatoms and that directly affect the sector. Mainly, dinoflagellates being the most diverse products are guaranteed to come from groups (Dawes, 1991; Valiela, 1995; a sustainably exploited area that com- Jeffreyet al. 1997; Knox, 2000; Mann, bines the human development of the 2000; MacIntery et al. 2000; Nybak- social groups involved (OCEANA, ken, 2001; Throndsen et al. 2007; 2013; Hoff et al. 2015). Hoppenrath et al. 2009; Simon et al. Given the advantages provided by 2009; Widdicombe et al. 2010). this fishery regulation, there are a num- Phytoplankton, due to their ber of provisions that must be met to short life cycles, respond quickly

30 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya to environmental changes, and MATERIALS AND METHODS their qualitative and quantitative composition allows an estimation Study area of water quality. The development This study was conducted on the of these organisms is controlled by outer part of the Gulf of Nicoya (GN), biological, physical and chemical Costa Rica, specifically in the Paquera- processes (Hu et al. 2011); therefore, Tambor Marine Area for Responsible the information that they may give as Fishing (Paquera-Tambor-MARF). This bioindicators should be interpreted area is characterized for having the great- est depths within the GN (25 to 100 m) with other physical and chemical and a strong influence by oceanic water data. In addition, the rapid response masses (Brenes & León, 1995). of the phytoplankton community to Four sampling stations were located changes induced by human activity in the Paquera-Tambor MARF, taking (introduction of nutrients, organic into account bathymetric, geographic matter, or pollutants) currently and biological characteristics of the makes them a key element in the area. Stations 1 and 2 were located in the evaluation of the quality of seawater outermost zone in the Paquera-Tambor (Domingues et al. 2008; Spatharis & MARF, the first station in front of the Tsirtsis, 2010). Tambor Beach area, with depths close Similarly, interspecific relation- to 45 m, and the second station between ships in communities affect the sta- Tortuga Island and the Negritos Islands, bility of food webs, which have been since the latter constitute a natural barrier evaluated in order to analyze their dividing the MARF. Sampling station 3 effects on ecosystems and their- rela was located in front the sanitary landfill tionship with trophic chains (Li et al. (El Relleno) in Paquera, since it is an 2009); for instance, the relationship important area for the reproduction and between phytoplankton and cod pro- growth of the spotted snapper Lutjanus duction has been studied, which shows guttatus (Steindachner, 1869), a fish that primary productivity determines species important for the area (Araya et the load capacity of systems (Stein- al. 2007). Station 4 was located between and Naranjo Beach, in grund & Gaard, 2005; Hansen et al. the shallowest and innermost part of the 2005) and, therefore, the production of sampling area (Fig. 1). commercial species. The aim of this study was to Collecting data and water characterize the abundance of the samples: taxa of the phytoplankton in the Monthly water and environmen- Paquera-Tambor Marine Area for tal data samples were taken from Responsible Fishing to determine September 2013 to August 2014 for seasonal changes of microalgae, phytoplankton analysis. Temperature, influenced by abiotic variables. salinity, total dissolved solids concen-

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 31 García-Rojas & Vega Bolaños

Fig. 1. Study area and sampling points in the Paquera-Tambor MARF Fig. 1. Localización del área de estudio y los puntos de muestreo en el AMPR-Paquera-Tambor tration, and percentage of dissolved counting chambers and a Nikon’s Eclipse oxygen saturation were measured E600 light microscope, for which a 1 with a YSI 556 MPS multiparameter ml aliquot of the sample was placed in-situ at each of the sampling sta- directly on the cell count (the sample tions, as well as the Secchi disk depth. was not concentrated). Phytoplankton In order to determine phytoplankton were counted and identified observing abundance, water samples were the entire bottom of the counting collected with a 6L Niskin bottle at a chamber with 10x and 20x objectives, 2m depth. Water samples were stored depending on the dimensions of the in 500 ml plastic bottles (previously organisms. Organisms were identified washed with water from the site), and up to the lowest possible taxonomic a 5 ml Lugol solution was added to level and counts were done making preserve the microalgae. groups of cells according to the main phytoplankton groups identified. Identification and counts of The studies by Cupp (1937), phytoplankton: Sournia (1986), Ricard (1987), Phytoplankton organisms were Chrétiennot-Dinet (1990), Round et al. studied using 1 ml Sedgewick Rafter (1990), Tomas (1997), Horner (2002),

32 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya and Ojeda (2006) were used for the used, and, in cases where data did identification of microalgae. not follow a normal curve, data was transformed using the log(x+1) function. Data analysis: In order to determine significant In order to determine the normality temporal differences between of data obtained, a Levene’s test was biological and abiotic parameters, a

Fig. 2. Temporal variation of the 2013-2014 physical and chemical variables in the Paquera-Tambor MARF (lines correspond to average values per month with their respective standard error) Fig. 2. Comportamiento temporal de las variables físicas y químicas determinadas en el AMPR-Paquera-Tambor en el 2013-2014 (las líneas corresponden a valores promedio por mes con su respectivo error estándar)

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 33 García-Rojas & Vega Bolaños

Fig. 3. Temporal variation of the abundance of phytoplankton groups in the Paquera- Tambor MARF in 2013-2014 (lines correspond to average values per month with their respective standard error) Fig. 3. Comportamiento temporal de la concentración de los grupos fitoplanctónicos determinados en el AMPR-Paquera-Tambor en el 2013-2014 (las líneas corresponden a valores promedio por mes con su respectivo error estándar)

34 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya one-way ANOVA test was used, and Table 1. Results of one-way ANOVA the significance of each variable was assessing temporal variations for the confirmed with a multiple comparison physical and chemical variables and Student-Newman-Keuls (S-N-K) post- taxonomic phytoplankton groups in the hoc test. The relationship of the different Paquera-Tambor MARF (*: significant phytoplankton groups identified with differences with p-value <0.05) respect to the physical and chemical Cuadro 1. Resultados de ANOVA de factors was determined using the un factor evaluando las diferencias Pearson correlation. The ANOVA, temporales para las variables físicas y correlation, and normality analyses químicas y los grupos fitoplanctónicos en el AMPR-Paquera-Tambor (*: diferencias were conducted using the SPSS 17.0 significativas con p-valor <0.05) statistical program (SPSS, 2008). P RESULTS Temperature 0.001* Determining the temporal varia- Salinity 0.001* tion between the sampling months for Total solids 0.001* the physical-chemical variables and the % of O2 Saturation 0.001* phytoplankton groups showed significant Secchi Disk 0.949 differences (P <0.05) for parameters such Diatoms 0.016* as temperature (P <0.001), salinity (P Dinoflagellates 0.048* <0.001), total solids (P <0.001) and per- Prasinophytes 0.465 Cyanophytes 0.705 centage of oxygen saturation (P <0.001), Silicoflagellates 0.261 as well as for dinoflagellates (P <0.048) Chromophytes 0.070 and diatoms (P <0.016) (Table 1). Since Tintinnids 0.443 sampling began in the rainy season, tem- perature tended to increase throughout the study period, with a minimum value of by the silicoflagellates, with values of 27°C in October and a maximum value of 1.3x104 ± 2.3x103 cells L-1, 5.9x104 ± 30°C in April. For variables such as salin- 9.1x103 cells L-1 and 2.9x102 ± 84 cells ity, total solids concentration and percent L-1, respectively. It is worth highlighting of dissolved oxygen saturation, the period that dinoflagellates showed algal blooms with the highest values was mainly the dry associated with the harmful species, season, with values equal to 33.57PSU, Cochlodinium catenatum, which exhibited 33.36 mg L-1 and 126.7%, respectively. a concentration of 5.85x104 ± 3x104 cells L-1 The Secchi disk depth ranged between during October 2013. Other phytoplankton 0.7m and 14.6m, with a strong variability groups such as the prasinophytes (125 ± during the sampling period (Figs. 2 and 3). 125 cells L-1), cyanophytes (84 ± 40 cells Regarding the micro-algae L-1) and chromophytes (94 ± 60 cells L-1) community, diatoms and dinoflagellates had a sporadic presence and relatively were the most representative groups low concentrations in comparison with throughout the sampling period, followed the dominant groups. In addition, the

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 35 García-Rojas & Vega Bolaños zooplanktonic group tintinnids was present 1916), Pyrodinium bahamense var. throughout the study period, although compressum (Böhm, Steidinger, in low concentrations (ranging between Tester & Taylor, 1980), Alexandrium 1x103 and 2.5x103 cells L-1) (Fig. 3). monilatum (Balech, 1995), and The same trend seen in the abundance diatoms Pseudo-nitzschia spp. was observed in species richness, with However, during the study period, diatoms and dinoflagellates showing only the dinoflagellates A. monilatum 51 and 32 species, respectively. For and C. catenatum generated an algal the remaining phytoplankton groups bloom with water discoloration and identified, abundance of species ranged production of mucous substances. between one and four specimens, The most dominant phytoplankton while eight species were observed for species were the diatoms Cyclothella tintinnids (Table 2). spp., Guinardia striata (Hasle, 1996), Within the dinoflagellates, Leptocylindrus danicus (Cleve, 1889), the presence of the following Navicula spp., Nitzschia spp., and algal bloom forming organisms Thalassiosira spp., with frequency was highlighted: dinoflagellates percentages in the samples greater Cochlodinium catenatum (Okamura, than 50%. Within the same frequency

Table 2. Phytoplanktonic richness in the Paquera-Tambor MARF for the sampling period Cuadro 2. Riqueza fitoplanctónica en el AMPR-Paquera-Tambor durante el periodo de muestreo Sampling period 2013 2014 S O N D J F M A M J J A DINOFLAGELLATES Alexandrium catenella - - x - x - - - x - - - Alexandrium monilatum - x - x - x x x x - - - Ceratium candelabrum ------x - Ceratium furca x x x - x - x - x x x - Ceratium fusus x x - - - - x - - x - x Ceratium horridum - - - - - x ------Ceratium macroceros - - - - x - - - - - x - Cochlodinium catenatum x x x x - x x x x x x - Corythodinium tesselatum ------x - - - - - Dinophysis caudata - - - - x - x - x - - - Gonyualax cf. polygramma - - - x x ------Gymnodinium catenatum - - x x - x ------Gyrodinium cf. spirale x x x x - x x - x x - x Noctiluca scintillans x ------Oxyphyxis cf. - - - - x x ------Phalacroma rotundatum ------x - - - - Prorocentrum gracile x x - - x x - x x - x x Prorocentrum cf. mexicanum - - - - x - - x - - - - Prorocentrum micans - x - x - x - x x x x x Prorocentrum rostratum - - x x - - x - - - - - Prorocentrum cf. scutellum - - - x ------Protoperidinium conicum - x x - x x - - x x - - Protoperidinium pellucidum x x x x - x x - x x - - Protoperidinium pentagonum x - - - - x - - x - - - Protoperidinium steinii x - x - x ------Protoperidium claudicans - x ------Pyrocistys cf. lunata x - x ------Pyrodinium bahamense var. compressum x - x x - - - - x - x - Pyrophacus cf. steinii - - - x x x ------Scripsiella trochoidea x x x x - x x x x x x x Torodinium cf. - - x ------Warnowia cf. - - - - - x ------

36 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya

DIATOMS Amphiprora cf. - - - - x - - - - x - - Bacteriastrum delicatum x - x - x - - - x - - - Bacteriastrum hyalinum - - x x - - - - x x - x Cerataulina bergonii - - - - - x x - - - - - Chaetoceros aequatorialis x ------Chaetoceros affinis - x ------Chaetoceros cf. atlanticus - - x - - - - - x - - - Chaetoceros coarctatus - - x ------Chaetoceros cf. debilis - - x - x ------Chaetoceros decipiens x x x x ------Chaetoceros lorenzianus - x x - x ------Chetoceros cf. laevis - - - x ------Cocconeis cf. ------Corethron criophylum x - x - x ------x Coscinodiscus sp x - - - x x x x x x x x Cyclotella x x x x x x - - x x x x Cylindrotheca closterium - - x - - - x - - x - - Diploneis bombus - - - - x - - x - - x - Ditylum brightwelli x - - x - - x - x x x x Eucampia cornuta - - x ------Fragilaria cf. ------x Guinardia cylindrus x - x ------Guinardia delicatula x - - x ------Guinardia flaccida - - - x x ------Guinardia striata x x x x - - x x x - x x Gyrosigma cf. ------x - - x x Haslea cf. - x x - x ------Hemiaulus hauckii x - x x - - - - x - - x Hemiaulus sinensis x x x x x x ------Leptocylindrus danicus x x x x x x x x x x x x Lithodesmium undulatum x - x x - x x - x x x x Navicula cf. granii x - - - x ------Navicula sp x x x x x x x - x x x x Nitzschia cf. - x - x - x x - x x x x Odontella aurita x - - x - - x - - - - x Odontella mobiliensis - - - - x - - x x - - x Odontella sinensis x - x x x - x x x - x x Paralia sulcata x x x x x x x x - x x x Pleurosigma cf. - - - - x x x - x x x - Prosbocia alata x - x - - x x - - - - - Pseudo-nitzschia cf. x x x x ------Rhizosolenia cf. - - x - x ------Rhizosolenia cf. setigera - - - x x - x - - x - x Rhizosolenia striata - - - - x - x x - - - - Skeletonema costatum x x x x x ------x Stephanopyxis turris - - x x x x x - x x - x Striatella unipucntata - - x x ------x Surirella fastuosa - - - - - x x - - x - - Thalassionema nitzschiodes x x x x x - x - - x x x Thalassiosira sp x x x x - x x x x x x x Triceratium ------x - - - PRASINOPHYTES Pyramimonas cf. - x ------CYANOPHYTES Merismopedia cf. (colonies) - - x - - - - x - - - - Oscillatoria cf. - - - - x x - x - - - x Spurulina cf. - - x ------SILICOFLAGELLATES Dictyoca fibula - - x x - x x x x x x x CHROMOPHYTES Hermesium adriaticum cf. x - x ------TINTINNIDS Codonellopsis gaussi cf. coxliella - - x ------Eutintinnus fracknoi x ------Salpingella cf. - x - - - - - x - - - - Tintinnopsis fimbriata x - x - x ------Tintinnopsis lobiancoi x ------Tintinnopsis parva - x x x - - x - x - - x Tintinnopsis radix - - x ------Undella claparedei - - x ------

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 37 García-Rojas & Vega Bolaños range, the dinoflagellates Gyrodinium hand, a dry season marked by increased spirale (Kofoid and Swezy, 1921), temperatures and the influence of Scripsiella trochoidea (Loeblich III, the wind mixing the waters, which 1976) and Cochlodinium catenatum generates greater turbulence in the were observed. water column and resuspension of When determining the correlation sediments, and, on the other hand, a between environmental variables and rainy season characterized by a high phytoplankton, negative relationships input of fresh water and sediment into were observed between diatoms the sea (Lizano & Vargas, 1994; Brenes and some variables such as depth (r et al. 2001). According to Voorhis = -0.448), percentage of dissolved et al. (1983) and Brenes (2001), the oxygen saturation (r = -0.490) and influence of the discharge of rivers Secchi disk depth (r = -0.558), as well such as the Tempisque, Barranca, and as between dinoflagellates and water Grande de Tárcoles is a determining temperature (r = -0.429). In addition, factor in the Gulf of Nicoya, since it diatoms were also positively correlated increases the variability of physical with the abundance of the tintinnids (r and chemical factors of the water, due = 0.443) (Table 3). to the constant input of fresh water in the estuary, which fluctuates depending DISCUSSION on the weather period. This study showed a temporal The variation in the percentage variability in most of the data obtained, of oxygen saturation also reflected both physically and chemically as constant changes experienced by well as biologically. From the abiotic the estuary of the Gulf of Nicoya perspective, results reflected a clear throughout an annual cycle. The trend related to the climatic variability values obtained from the percentages that characterizes Costa Rica: on one of oxygen saturation during the rainy

Table 3. Significant values of Pearson correlation between physical and chemical variables and phytoplankton in the Paquera-Tambor MARF (*: significant correlation with P <0.05) Cuadro 3. Valores significativos de la correlación de Pearson entre las variables físicas y químicas y los organismos fitoplanctónicos del AMPR-Paquera-Tambor (*: Correlación significativa aP -valor <0.05)

Correlation r-Pearson Value Dinoflagellates / Temperature -0.429* Diatoms / Depth -0.448* Diatoms / % of Dissolved Oxygen Saturation -0.490* Diatoms / Secchi Disk Depth -0.558* Tintinnids / Diatoms 0.433*

38 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya season agree with those obtained by of present species. This has already Kress et al. (2001) and Epifanio et al. been noted for other coastal estuarine (1983), who determined that the Gulf environments and is also evidenced of Nicoya is an unsaturated estuary by the fact that the most common when there is an increase in rainfall in species in this study belonged to these the area, caused by the consumption phytoplankton groups. Rochelle- of oxygen by the organic matter that Newall et al. (2011) evaluated enters through the runoff. the distribution and diversity of The Secchi disk depth was phytoplankton in northern Viet Nam closely related to the behavior of estuarine environments and found that the phytoplankton community, between 43% and 99% of the samples presenting the highest values when the were diatoms. In addition, Cabrita microalgae concentration was lower, (2014) determined the richness of and vice versa. This is confirmed the phytoplankton community as with the negative correlation between an indicator of changes related to the concentration of diatoms and the drainage in the Tagus estuary in the Secchi disk depth. In addition, Portugal, determining that groups such according to Medina (1995), Litchman as the diatoms, dinoflagellates, and & Klausmeier (2008) and Aktan cryptophytes represent a total of 92- (2011), the extinction of light in water 99% of the phytoplankton community. is proportional to the abundance of On the other hand, several authors phytoplankton. This condition is have determined that the dominant reflected only in the diatoms since numbers of diatoms species is strongly this is the dominant group as far related to increased concentrations as concentration, unlike the other of nutrients (Ishizaka et al. 1986; phytoplankton organisms. Day et al. 2012), which could be The richness of the phytoplankton associated to the characteristics of the in the Paquera-Tambor MARF reflects Gulf of Nicoya, where the dynamics an important group of organisms, of the estuary with constant inputs mainly belonging to diatoms and of freshwater, mangrove ecosystems dinoflagellates. This research, as near shore and the processes of mixing well as others in other coastal areas waters (Brenes & León, 1995) favor a (Eker & Kideyş, 2000; Peña & Pinilla, constant flow of nutrients (Magnoneet 2002; Varela & Prego, 2003; Álvarez- al. 2015; Sin et al. 2015). Góngora & Herrera-Silveira, 2006; The low numbers of Simon et al. 2009; Haraguchi et al. prasinophytes, cyanophytes and 2015) reported higher concentrations chromophytes can be related to the of diatoms with respect to the other fact that they are phytoplankton phytoplankton groups identified, with groups common in coastal ecosystems the dinoflagellates being the next of oligotrophic nature. According to highest group in terms of the number several authors, these phytoplanton

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 39 García-Rojas & Vega Bolaños groups represent some of the most catenatum, Pyrodinium bahamense important nanoplankton groups in the var. compressum, Alexandrium oligotrophic systems (Puigserver et monilatum, and diatoms Pseudo- al. 2002; Resende et al. 2007; Aktan, nitzschia spp. has been reported from 2011; Huete-Ortega et al. 2010; the inside to the outside area of the Gulf Schlüter et al. 2011). of Nicoya (García, 2005; Calvo et al. The presence of tintinnids in the 2014). In the case of dinoflagellates, waters of the Paquera-Tambor MARF these species are common in the waters is related to the adaptation of this of the Gulf of Nicoya; C. catenatum is group of organisms to areas where a recurring species in the production of freshwater and saltwater converge red tides in the Gulf (García, 2005) as (Zhang et al. 2015). However, few well as P. bahamense var. compressum studies of tintinnids have been reported (Víquez & Hargraves, 1995). In the in tropical areas, as subtropical to case of A. monilatum, it was not until temperate areas are considered to 2005 that the first red tide caused by be the comfort zone of this group of this species was reported for this area ciliates (Quevedo et al. 2003; Safi et (Calvo et al. 2005). al. 2007; Santoferrara & Alder, 2009; In general, results reflect that Li et al. 2015). the Paquera-Tambor MARF is an The positive relationship between important ecological area, since the diatoms and tintinnids is due to a presence of different microalgae primary trophic relationship, since it groups and zooplankton organisms was observed that the increase in the (tintinnids) are the basis of the food concentration of diatom cells coincides chain in the area (Magnone et al. 2015; with the increase in the abundance of Feng et al. 2015; Rakshit et al. 2016), ciliates, suggesting a relevant grazing and, therefore, favor the following process in the Paquera-Tambor MARF levels of the food chain. In addition, (Stelfox-Widdicombe et al. 2004). given that this is an important area for This is consistent with what was aquaculture and fishery production, observed by Widdicombe et al. (2010), this study is of vital importance to who determined that the seasonal ensure an ecosystem assessment that pattern of abundance of the ciliates allows for the recognition of guidelines in the Western English Channel was for a comprehensive management of similar to the population dynamics of the marine area for responsible fishing. the diatoms and the phytoflagellates. This type of monitoring should The presence of algal bloom be maintained in Marine Areas for forming species in the waters of the Responsible Fishing, since they are Paquera-Tambor MARF proves the areas susceptible to harmful and toxic wide distribution of these organisms in algal blooms, and, consequently, can the Gulf of Nicoya, where the presence affect the economy of the communities of dinoflagellates Cochlodinium exploiting them.

40 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya

ACKNOWLEDGMENTS 39-47). San Salvador, El Salvador: We would like to thank the PRADEPESCA. fishermen and the managers of the Brenes, C. L., León, S. & Chávez, J. Marine Area for Responsible Fishing (2001). Variación de las propiedades for their willingness to conduct termohalinas en el Golfo de Nico- the study as a complement to their ya, Costa Rica. Rev. Biol. Trop., 49, management plan and the reviewers 145-152. for their valuable suggestions. Cabrita, M. T. (2014). Phytoplankton community indicators of changes asso- ciated with dredging in the Tagus es- BIBLIOGRAPHY tuary (Portugal). Environ. Pollut., 191, Aktan, Y. (2011). Large-scale patterns in 17-24. http://dx.doi.org/10.1016/j. summer surface water phytoplank- envpol.2014.04.001 ton (except picophytoplankton) in the Calvo, E., Víquez, R. & García, A. (2005). Eastern Mediterranean. Estuar. Coast. Alexandrium monilatum (Howell) Ba- Shelf Sci., 91, 551-558. http://dx.doi. lech bloom in the Gulf of Nicoya, Pun- org/10.1016/j.ecss.2010.12.010 tarenas. Harmful Algae News. IOC- Álvarez-Góngora, C. & Herrera-Silveira, J. A. (2006). Variations of phytoplank- UNESCO, 29, 1-2. ton community structure related to wa- Calvo, E., Boza, J. & Berrocal, K. (2014). ter quality trends in a tropical karstic Efectos de El Niño y La Niña sobre el coastal zone. Mar. Pollut. Bull., 52, comportamiento del microfitoplancton 48-60. http://dx.doi.org/10.1016/j. marino y las variables fisicoquímicas marpolbul.2005.08.006 durante el 2008 a 2010 en el Golfo Araya, H., Vásquez, A., Marín, B., Pala- de Nicoya, Costa Rica. Rev. Cienc. cios, J. A., Soto-Rojas, R., Mejía-Ara- Mar. Cost., 6, 115-133. http://dx.doi. na, F., Shimazu, Y. & Hiramatsu, K. org/10.15359/revmar.8-1.9 (2007). Reporte no.1/2007 del Comité Chrétiennot-Dinet, M. J. (1990). Chlo- de Evaluación de Poblaciones: Repor- rarachniophycées, Chlorophycées, te del Manejo de los Recursos Pesque- Chrysophycées, Cryptophycées, Eu- ros en el Golfo de Nicoya. , glénophycées, Eustigmatophycées, Costa Rica: UNA-JICA-INCOPESCA. Prasinophycées, Prymnésiophycées, Brenes, C. (2001). Fundamentos de Ocea- Rhodophycées et Tribophycées. In A. nografía Descriptiva: Aplicación al Sournia (Ed.), Atlas Du Phytoplancton Istmo Centroamericano. Bluefields, Marin. Volume II (pp. 1-261). Paris, Nicaragua: Proyecto para el Desarrollo : Éditions du Centre National de Integral de la Pesca Artesanal en la Re- la Recherche Scientifique. gión Autónoma Atlántico Sur (DIPAL). Cupp, E. (1937). Marine Plankton Dia- Brenes, C. & León, S. (1995). Hidrogra- toms of the West Coast of North Amer- fía del Golfo de Nicoya. In J. Zarnorro ica. , USA: University of (Ed.), Actas del Simposium Ecosiste- California Press. ma de Manglares en el Pacífico Cen- Dawes, C. (1991). Botánica Marina. troamericano y sus Recursos de Post- Distrito Federal, México: Editorial larvas de Camarones Peneidos (pp. Limusa, S.A.

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 41 García-Rojas & Vega Bolaños

Day, J. G., Slocombe, S. P. & Stanley, M. Haraguchi, L., Carstensen, J., Abreu, P. S. (2012). Overcoming biological con- C. & Odebrecht, C. (2015). Long-term straints to enable the exploitation of changes of the phytoplankton com- microalgae for biofuels. Bioresource munity and biomass in the subtropi- Technol., 109, 245-251. http://dx.doi. cal shallow Patos Lagoon Estuary, org/10.1016/j.biortech.2011.05.033 Brazil. Estuar. Coast. Shelf Sci., 162, Domingues, R., Barbosa, A. & Galvão, H. 76-87. http://dx.doi.org/10.1016/j. (2008). Constraints on the use of phyto- ecss.2015.03.007 plankton as a biological quality element Hoff, N. T., Figueira, R. C. L. &Abes- within the Water Framework Directi- sa, D. M. S. (2015). Levels of metals, ve in Portuguese waters. Mar. Pollut. arsenic and phosphorus in sediments Bull., 56, 1389-1395. http://dx.doi. from two sectors of a Brazilian Marine org/10.1016/j.marpolbul.2008.05.006 Protected Area (Tupinambás Ecolo- Eker, E. & Kideyş, A. E. (2000). Weekly gical Station). Mar. Pollut. Bull., 91, variations in phytoplankton structure 403-409. http://dx.doi.org/10.1016/j. of a Harbour in Mersin Bay (north- marpolbul.2014.10.044 eastern Mediterranean). Turk. J. Bot., Hoppenrath, M., Elbrächter, M. & Dre- 24, 13-24. bes, G. (2009). Marine phytoplankton: Epifanio, C. E., Maurer, D. & Dittel, A. I. Selected microphytoplankton species (1983). Seasonal changes in nutrients from the North Sea around Helgoland and dissolved oxygen in the Gulf of and Sylt. Stuttgart, Germany: Kleine Nicoya, a tropical estuary on the Pa- Senckenberg-Reihe 49. cific coast of Central America. Hydro- Horner, R. (2002). A Taxonomic Guide to biologia, 101, 231-238. http://dx.doi. Some Common Marine Phytoplankton. org/10.1007/BF00009879 Briston, England: Biopress Ltd. Feng, M., Zhang, W., Wang, W., Zhang, Hu, H., Zhang, J. & Chen, W. (2011). G., Xiao, T. & Xu, H. (2015). Can Competition of bloom-forming ma- tintinnids be used for discriminating rine phytoplankton at low nutrient water quality status in marine ecosys- concentrations. J. Environ. Sci., 23, tems? Mar. Pollut. Bull., 101(2), 656-663. http://dx.doi.org/10.1016/ 549-555. http://dx.doi.org/10.1016/j. S1001-0742(10)60459-7 marpolbul.2015.10.059 Huete-Ortega, M., Marañón, E., Varela, M. García, A. (2005). Biomasa fitoplanctó- & Bode, A. (2010). General patterns in nica durante un florecimiento algal en the size scaling of phytoplankton abun- el Golfo de Nicoya, Costa Rica. Unpu- dance in coastal waters during a 10-year blished Licentiate Thesis, Universidad time series. J. Plankton Res., 32, 1-14. Nacional, Costa Rica. http://dx.doi.org/10.1093/plankt/fbp104 Hansen, B., Eliasen, S. K., Gaard, E. & Ishizaka, J., Takahashi, M. & Ishimura, Larsen, K. M. H. (2005). Climatic S. (1986). Changes in the growth rate effects on plankton and productivi- of phytoplankton in local upwelling ty on the Faroe Shelf. ICES J. Mar. around the Izu Peninsula, Japan. J. Sci., 62, 1224-1232. http://dx.doi. Plankton Res., 8(l), 169-181. http:// org/10.1016/j.icesjms.2005.04.014 dx.doi.org/10.1093/plankt/8.1.169

42 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya

Jeffrey, S. W., Montoura, R. F. C.& MAG. Ministerio de Agricultura y Gana- Wright, S. W. (1997). Phytoplankton dería. (2009). Reglamento para el Es- pigments in oceanography guidelines tablecimiento de las Áreas Marinas de to modern methods. Paris, France: Pesca Responsable y Declaratoria de UNESCO. Interés Público Nacional de las Áreas Knox, G. (2000). The ecology of seasho- Marinas de Pesca Responsable. De- res. Florida, USA: CRC Press. http:// creto Nº 35502-MAG. (Published in dx.doi.org/10.1201/9781420042634 the Gazette N° 191, October 01). San Kress, N., León, S., Brenes, C., Brenner, José, Costa Rica: Imprenta Nacional. S. & Arroyo, G. (2001). Horizontal Magnone, L., Bessonart, M., Gadea, J. & transport and seasonal distribution of Salhi, M. (2015). Trophic relationships nutrients, dissolved oxygen and chlo- in an estuarine environment: A quanti- rophyll-a in the Gulf of Nicoya, Cos- tative fatty acid analysis signature ap- ta Rica: a tropical estuary. Cont. Shelf proach. Estuar. Coast. Shelf Sci., 166, Res., 0, 1-16. 24-33. http://dx.doi.org/10.1016/j. Li, Y., Chen, Y., Song, B., Olson, D., Yu, ecss.2014.12.033 N. & Chen, L. (2009). Ecosystem Mann, K. H. (2000). Ecology of Coas- structure and functioning of Lake Tai- tal Waters: Implications for Manage- hu (China) and the impacts of fishing. ment. Massachusetts, USA: Blackwell Fish. Res., 95, 309-324. http://dx.doi. Science, Inc. org/10.1016/j.fishres.2008.09.039 Medina, L. (1995). Análisis multidisci- Li, H., Zhao, Y., Chen, X., Zhang, W., plinar del ecosistema costero insular, Xu, J., Li, J. & Xiao, T. (2015). Inte- balance energético, capa de mezcla y raction between neritic and warm wa- modelo biológico. Unpublished Doc- ter tintinnids in surface waters of East toral Dissertation, Universidad de Las China Sea. Deep-Sea Research II, 124, Palmas de Gran Canaria, Spain. 84-92. http://dx.doi.org/10.1016/j. Nybakken, J. W. (2001). Marine Ecology: dsr2.2015.06.008 An ecological approach. New York, Litchman, E. & Klausmeier, C. A. USA: Benjamin Cummings, Addison (2008). Trait-Based Community Wesley Longman. Ecology of Phytoplankton. Annu. OCEANA. (2013). Áreas marinas prote- Rev. Ecol. Evol. Syst., 39, 615-639. gidas: una herramienta para combatir http://dx.doi.org/10.1146/annurev. ecolsys.39.110707.173549 la sobrepesca y conservar los ecosiste- Lizano, O. & Vargas, J. (1994). Distribución mas marinos. Oceana, 4, 1-15. espacio-temporal de la salinidad y la Ojeda, A. (2006). Dinoflagelados de Ca- temperatura en la parte interna del Golfo narias: Estudio Taxonómico y Ecoló- de Nicoya. Tecnol. Mar., 12(2), 3-16. gico. Tenerife, Islas Canarias, Spain: MacIntery, H. L., Kana, T. M. & Geider, Litografía Romero, S.L. R. J. (2000). The effect of water motion Peña, V. & Pinilla, G. A. (2002). Compo- on short-term rates of photosynthe- sición, distribución y abundancia de la sis by marine phytoplankton. Trends comunidad fitoplanctónica de la ense- Plant. Sci. Rev., 5, 12-17. http://dx.doi. nada de Utría, Pacífico colombiano. org/10.1016/S1360-1385(99)01504-6 Rev. Biol. Mar. Oceano., 37, 67-81.

Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. 43 García-Rojas & Vega Bolaños

Puigserver, M., Ramon, G., Moya, G. & Round, F. E., Crawford, R. M. & Mann, Martínez-Taberner, A. (2002). Plank- D. G. (1990). The Diatoms: Biology & tonic chlorophyll a and eutrophication Morphology of the Genera. New York, in two Mediterranean littoral systems USA: Cambridge University Press. (Mallorca Island, Spain). Hydrobiolo- Safi, K., Griffiths, F. & Hall, J. A. (2007). gia, 475/476, 493-504. http://dx.doi. Microzooplankton composition, bio- org/10.1023/A:1020368215511 mass and grazing rates along the Quevedo, M., Viesca, L., Anadon, R. WOCE SR3 line between Tasma- & Fernández, E. (2003). The protis- nia and Antarctica. Deep-Sea Res. tan microzooplankton community in Pt. I, 54, 1025-1041. http://dx.doi. the oligotrophic north-eastern Atlan- org/10.1016/j.dsr.2007.05.003 tic: large- and mesoscale patterns. J. Santoferrara, L. & Alder, V. (2009). Abun- Plankton Res., 25, 551-563. http:// dance trends and ecology of planktonic dx.doi.org/10.1093/plankt/25.5.551 ciliates of the south-western Atlantic Rakshit, D., Ganeshb, P. S. & Sarkar, S. K. (35-63 o S): a comparison between (2016). Choreotrich ciliate tintinnid (Pro- neritic and oceanic environments. J. tozoa: Ciliophora) in a tropical meso- Plankton Res., 31, 837-851. http:// macrotidal estuary, eastern part of . dx.doi.org/10.1093/plankt/fbp033 Reg. Stud. Mar. Sci., 3, 89-100. http:// Schlüter, L., Henriksen, P., Nielsen, T. G. dx.doi.org/10.1016/j.rsma.2015.06.003 & Jakobsen, H. H. (2011). Phytoplank- Resende, P., Miranda, U., Gonçalves, F. ton composition and biomass across & Pereira, M. J. (2007). Distribution the southern Indian Ocean. Deep-Sea and ecological preferences of diatoms Res. Pt. I, 58, 546-556. http://dx.doi. and dinoflagellates in the west Iberian org/10.1016/j.dsr.2011.02.007 Coastal zone (North Portugal). Acta Simon, N., Cras, A. L., Foulon, E. & Le- Oecol., 32, 224-235. http://dx.doi. mée, R. (2009). Diversity and evolu- org/10.1016/j.actao.2007.05.004 tion of marine phytoplankton. C.R. Ricard, M. (1987). Diatomophycées. In A. Biol., 332, 159-170. http://dx.doi. Sournia (Ed.), Atlas du Phytoplancton org/10.1016/j.crvi.2008.09.009 Marin. Volume II (pp. 262-296). Paris, Sin, Y., Lee, E., Lee, Y. & Shin, K. H. France: Éditions du Centre National de (2015). The river-estuarine conti- la Recherche Scientifique. nuum of nutrients and phytoplankton Rochelle-Newall, E. J., Chu, T. V., Prin- communities in an estuary physically gault, O., Amouroux, D., Arfi, R., divided by a sea dike. Estuar. Coast. Bettarel, Y. T., Bouvier, C., Got, P., Shelf Sci., 163, 279-289. http://dx.doi. Nguyen, T. M. H., Mari, X., Navarro, org/10.1016/j.ecss.2014.12.028 P., Duong, T. N., Cao, T. T. T., Pham, T. Sournia, A. (1986). Atlas du Phytoplanc- T., Ouillon, S. & Torréton, J. P. (2011). ton Marin. Volume I: Introduction, Phytoplankton distribution and pro- Cyanophycées, Dictyochophycées, Di- ductivity in a highly turbid, tropical nophycées et Raphidophycées. Paris, coastal system (Bach Dang Estuary, France: Éditions du Centre National de Vietnam). Mar. Pollut. Bull., 62, 2317- la Recherche Scientifique. 2329. http://dx.doi.org/10.1016/j. Spatharis, S. & Tsirtsis, G. (2010). Ecologi- marpolbul.2011.08.044 cal quality scales based on phytoplankton

44 Rev. Mar. Cost. ISSN 1659-455X. Vol. 8 (2): 29-45, Julio-Diciembre 2016. Seasonal changes of phytoplankton in the Paquera-Tambor Marine Area for Responsible Fishing, Gulf of Nicoya

for implementation of Water Framework Varela, M. & Prego, R. (2003). Hydrogra- Directive in the Eastern Mediterranean. phy and phytoplankton in an isolated Ecol. Indic., 10, 840-847. http://dx.doi. and non-pristine ria area: the A Coruña org/10.1016/j.ecolind.2010.01.005 Harbour (NW Spain). Acta Oecol., 24, SPSS. (2008). SPSS Statistics for Windows, 113-124. http://dx.doi.org/10.1016/ Version 17.0. Chicago, USA: SPSS Inc. S1146-609X(03)00048-1 Steingrund, P. & Gaard, E. (2005). Re- Víquez, R. & Hargraves, P. (1995). Annual lationship between phytoplankton cycle of potentially harmful dinoflage- production and cod production on the llates in the Golfo de Nicoya, Costa Faroe Shelf. ICES J. Mar. Sci., 62(2), Rica. Bull. Mar. Sci., 57(2), 467-475. 163-176. http://dx.doi.org/10.1016/j. Voorhis, A., Epifanio, C., Maurer, D., Dit- icesjms.2004.08.019 tel, A. & Vargas, J. (1983). The estuarine Stelfox-Widdicombe, C. E., Archer, S. character of the Gulf of Nicoya, an em- D., Burkill, P. H. & Stefels, J. (2004). bayment on the Pacific coast of Central Microzooplankton grazing in Phaeo- America. Hydrobiologia, 99, 225-237. cystis and diatom-dominated waters http://dx.doi.org/10.1007/BF00008774 in the southern North Sea in spring. Widdicombe, C. E., Eloire, D., Harbour, D., J. Sea Res., 51, 37-51. http://dx.doi. Harris, R. P. & Somerfield, P. J. (2010). org/10.1016/j.seares.2003.04.004 Long-term phytoplankton community Throndsen, J., Hasle, G. R. & Tangen, K. (2007). dynamics in the Western English Chan- Phytoplankton of Norwegian Coastal Wa- nel. J. Plankton Res., 32, 643-655. http:// ters. Oslo, Norway: Almater Forlag As. dx.doi.org/10.1093/plankt/fbp127 Tomas, C. (1997). Identifying Marine Zhang, C., Zhang, W., Ni, X., Zhao, Y., Phytoplankton. San Diego, USA: Aca- Huang, L. & Xiao, T. (2015). Influence of demic Press. different water masses on planktonic cilia- Valiela, I. (1995). Marine ecological pro- te distribution on the East China Sea shelf. cess. New York, USA: Springer. http:// J. Mar. Syst., 141, 98-111. http://dx.doi. dx.doi.org/10.1007/978-1-4757-4125-4 org/10.1016/j.jmarsys.2014.09.003

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