Acta125(4)

Planktonic algal blooms from 2000 to 2015 in Acapulco Bay, Guerrero, Mexico

Florecimientos de microalgas planctónicas de 2000 al 2015 en la Bahía de Acapulco, Guerrero, México

María Esther Meave del Castillo1,2 , María Eugenia Zamudio-Resendiz1

1 Universidad Autónoma Metropolitana, Unidad Iztapalapa, Departamento de Hidrobiología, Laboratorio de Fitoplancton Marino y Salobre, Av. San Rafael Atlixco 186, Col. Vicentina, Iztapalapa, 09340 Cd. Mx., México.

2 Author for correspondence:

mem@xanum.uam.mx

Received: November 21, 2017.

Reviewed: January 10, 2018.

Accepted: April 6, 2018.

Online first: August 2, 2018.

Published: October 3, 2018.

To cite as:

Meave del Castillo, M. E. y M. E. Zamudio-Resendiz. 2018. Planktonic algal blooms from 2000 to 2015 in Acapulco Bay, Guerrero, Mexico. Acta Botanica Mexicana 125: 61-93. DOI: 10.21829/abm125.2018.1316

DOI:

10.21829/abm125.2018.1316

Abstract:

Background and Aims: Harmful algal blooms (HABs) affect the marine ecosystem in multiple ways. The objective was to document the species that produced blooms in Acapulco Bay over a 15-year period (2000-2015) and analyze the presence of these events with El Niño-Southern Oscillation (ENSO).

Methods: Thirty-five collections, made during the years 2000, 2002-2004, 2006-2011, 2013-2015, were undertaken with phytoplankton nets and Van Dorn bottle, yielding 526 samples, of which 423 were quantified using the Utermöhl method. The relationship of HAB with ENSO was made with standardized values of Multivariate ENSO Index (MEI) and the significance was evaluated with the method quadrant sums of Olmstead-Tukey.

Key results: Using data of cell density and high relative abundance (>60%), 53 blooms were recorded, most of them occurring during the rainy season (June-October) and dry-cold season (November-March), plus 37 blooms reported by other authors. These 90 blooms were composed of 40 taxa: 21 diatoms and 19 dinoflagellates, the former mostly innocuous. Sixty-seven blooms had species reported as noxious, of which 11 species commonly produce toxic HAB. Toxic taxa are Pseudo-nitzschia spp. (four taxa), and seven dinoflagellates.

Conclusions: Abundance analyses of Pyrodinium bahamense var. compressum and Gymnodinium catenatum against values of MEI showed a clear tendency to produce HAB in La Niña conditions. Both taxa, producers of saxitoxins, cause paralytic shellfish poisoning (PSP) and coexist in Acapulco; therefore, they present a risk to human health. Another noxious 52 taxa found in Acapulco were currently considered potential HABs, because they have been recorded at low densities. Given the sharp differences in density values of bloom-forming species found in this work compared to those reported by other authors on similar dates, it is important to perform calibration tests to rule out possible errors in cell counts.

Key words: cell density, ENSO, HAB, harmful phytoplankton, Pyrodinium bahamense, relative abundance.

Resumen:

Antecedentes y Objetivos: Los florecimientos algales nocivos (FAN) afectan al ecosistema marino de varias maneras. El objetivo fue reconocer las especies productoras de dichos florecimientos en la Bahía de Acapulco, durante un periodo de 15 años (2000-2015) y relacionar su presencia con el fenómeno El Niño-Oscilación del Sur (ENSO).

Métodos: Analizamos 526 muestras de 35 colectas efectuadas durante los años 2000, 2002-2004, 2006-2011 y 2013-2015, realizadas con red y botella Van Dorn; éstas últimas (423) cuantificadas con el método de Utermöhl. La relación de FAN con ENSO se hizo con valores estandarizados del Índice Multivariado ENSO (MEI), y las significancia evaluada con el método de Asociación de Cuadrantes de Olmstead-Tukey.

Resultados clave: Con base en la densidad celular y abundancia relativa alta (>60%) se reconocieron 53 florecimientos, la mayoría durante la época de lluvias (junio-octubre) y secas-fría (noviembre-marzo), más otros 37 eventos reportados por distintos autores. Estos 90 eventos estuvieron conformados por 40 taxa (21 diatomeas y 19 dinoflagelados); los de diatomeas, en su mayoría, inocuos. Sesenta y siete florecimientos estuvieron conformados por especies reportadas como dañinas, de las cuales 11 comúnmente producen FAN tóxicos. Los taxa tóxicos fueron Pseudo-nitzschia spp. (cuatro taxa) y siete dinoflagelados.

Conclusiones: Los análisis de abundancia de Pyrodinium bahamense var. compressum y Gymnodinium catenatum, en relación con los valores MEI, mostraron una clara tendencia a producir FAN en condiciones La Niña. Ambos taxa, productores de saxitoxinas y causantes de envenenamiento paralítico por moluscos, incluso llegan a coexistir en Acapulco, representando un riesgo para la salud humana. Otros 52 taxa dañinos por encontrarse en bajas densidades, se consideraron por el momento potenciales formadores de FAN. Dadas las agudas diferencias encontradas en valores de densidad de especies formadoras de florecimientos respecto a las reportadas por otros autores en fechas similares, es importante realizar pruebas de calibración para descartar posibles errores en conteos celulares.

Palabras clave: abundancia relativa, densidad celular, ENSO, FAN, fitoplancton nocivo, Pyrodinium bahamense.

Introduction

Algal blooms are exponential growths of microalgae populations that occur spontaneously in aquatic environments. Generally, such blooms are harmful for several reasons, due to the presence of chemical (toxin production, see Table 1, reactive oxygen species, and anoxia), physical (decreased transparency, obstruction, or lacerations of fish gills) (Smayda, 1997), or biological agents (allelopathy, reduction of grazing pressure, and competition) (Kudela and Glober, 2012; Tang and Glober, 2012). Approximately 200 species of planktonic microalgae can produce toxins (Landsberg, 2002), and since they are primary producers in the food webs, their toxins can intoxicate or kill other organisms when consumed; humans may be affected if they consume contaminated fish or shellfish species (Hallegraeff, 2010). Other effects are due to the fact that when algae form blooms, they die quickly and bacterial decomposition of such biomass causes anoxia, which affects and kills aquatic animals at different trophic levels (Anderson, 2007). Additionally, other microalgae that produce blooms are harmful to fish because they have thick and sharp structures (spines, setae, horns) that damage or block gills or cause an irritation that produces thick mucus that suffocates fish (Corrales and Maclean, 1995).

Table 1: Cell density criteria for considering a Harmful Algae Bloom (HAB) of toxic or harmful phytoplankton species, including the type of poisoning and damage they produce to other organisms. *Phaeocystis antartica G. Karst., P. globosa Scherff. and P. pouchetii (Har.) Lagerh. ** In Alexandrium spp. and Karenia spp. the abundance of 5 x103cells L-1 can render oysters toxic and, therefore, a risk to human health. However, a bloom for these species is considered when their abundances exceed 20-50 ×103cells L-1 (Steidinger pers. comm.).

Taxa

Cell density

Toxin and effects

Bacillariophyta

Cerataulina pelagica (Cleve) Hendey

750 × 103cells L-1(Lorrain et al., 2000)

Harmful (non toxic)

Effect on shellfish growth

Chaetoceros spp.

10 × 103cells L-1(Sunesen et al., 2009)

Harmful (non toxic)

Cause fish suffocation

Cylindrotheca closterium (Ehrenb.) Reimann & J.C.Lewin

>10 × 103cells L-1(Merino-Virgilio et al., 2014)

Harmful (non toxic)

Cause fish suffocation

Hemiaulus hauckii Grunow ex Van Heurck

>11 × 103cells L-1(Villarreal et al., 2012)

Innocuous

Increase primary productivity

Pseudo-nitszchia spp.

1 × 103-1 × 04cells L-1(Bates et al., 1998, Lefebvre et al., 2002)

Domoic acid (DA)

Amnesic shellfish poisoning

Dinophyta

Gymnodinium catenatum Graham, Pyrodinium bahamense Plate, Alexandrium spp.

>5 × 103cells L-1(Negri and Inza, 1998)**

Saxitoxins (STX, GTX, dcGTX, doGTX)

Paralytic shellfish poisoning

Margalefidinium polykrikoides (Margalef) F. Gómez, Richlen & D.M. Anderson (= Cochlodinium polykrikoides Margalef)

0.5 × 106cells L-1 fish stress 300 × 103-0,5x106cells L-1(precaution or warning) (Whyte et al., 2001)

Reactive oxygen species (ROS)

Neurotoxic, hemolytic, hemagglutivative, damage to fish gills

Dinophysis caudata Kent

>1.8 × 102- 1x103cells L-1(Reguera, 2002; Reguera et al., 2014)

Okadaic acid (OA)

Diarrheal shellfish poisoning

Karenia spp.

> 5 × 103cells L-1(Reguera, 2002; Reich et al., 2015) **

Brevetoxins (PbTx)

Ictiotoxic, neurotoxic

Levanderina fissa (Lavander) O. Moestrup, Hakanen, G. Hansen, Daugbjerg & Ellegaard (=Gyrodinium instriatum Freud. & Lee)

1 × 105-1 × 106cells L-1(Zhu et al., 2004) >13 × 106cells L-1(Jiménez, 1993)

Innocuous

Anoxia and shrimp mortality, increase primary productivity

Lingulodinium polyedra (F. Stein) J.D. Dodge

>1 × 103cells L-1 (Paz et al., 2008)

Yessotoxins (YTX)

Liver damage

Noctiluca scintillans (Macartney) Kof. & Swezy

500 × 103cells L-1(La Barbera-Sánchez, 1991) 5.6 × 103cells L-1(Adnan, 1989)

Innocuous

Cause mortality in mussels (Perna perna (Linné, 1758), demersal fishes and benthic organisms

Prorocentrum micans Ehrenb.

1 × 106-1 × 107cells L-1(Matthews and Pitcherd, 1996)

Harmful

Cause anoxia in HAB along with Tripos furca

Scrippsiella acuminata (Ehrenb.) Kretschmann, Elbr., Zinssm., Soehner, Kirsch, Kusber & Gottschling (= S. trochoidea (F.Stein) A.R. Loebl.)

1 × 104cells L-1(Tang and Glober, 2012) Brown discoloration (Whitelegge, 1891)

Harmful

Causes mortality in bivalve larvae (Cassostrea virginica (Gmelin, 1791) and Mercenaria mercenaria (Linné, 1758)) by clogging feeding apparatuses with lipids and extracellular polysaccharides.

Causative of anoxia that produced mass mortality of fish and invertebrates

Tripos balechii (Meave, Okolodkov & Zamudio) F. Gómez

6 × 103-7.3 × 106cells L-1 (Pitcherd and Probyn, 2011)

Harmful

Cause mass mortality of rocklobster Jasus lalandii (H. Edwards, 1837)

Tripos furca (Ehrenb.) F. Gómez

1 × 107cells L-1 (Matthews and Pitcherd, 1996; Orellana-Cepeda et al., 2004)

Harmful

Increase Ammonium (1 mg L-1) and caused mass mortality in the tuna pens, fishes, lobsters, sea urchins, bivalves and limpets

Phaeocystis spp.*

1 × 106cells L-1(Schoemann et al., 2005)

Producer toxic foam

Affect fishing and tourism

Other taxa without density values or collected and evaluated with net samples

Relative abundance >60% (Present study)

Harmful due to the presence of sharp or pointed structures

Damage fish gills or causes anoxia

It is important to distinguish between bloom and harmful algal bloom (HAB), because even though a species might be classified as toxic or harmful, toxins are sometimes synthesized under certain environmental circumstances only (Trainer et al., 2012), or with the help of symbiotic bacteria (Azanza et al., 2006). In addition, because toxins do not affect the same type of organisms, classification of the harmfulness of a bloom also depends on the presence of a sensitive organism or a vector that passes the toxins to humans. Hence, the effect of noxiousness often occurs when the presence of a toxic or noxious algal strain in high density is combined with the organisms it affects. Formally, blooms are considered HABs only when they have a negative effect on the environment or when they pose a risk to human health (Hallegraeff, 2010). However, cell density alone can often be a good estimator for detecting HABs. Tesfay (2011) obtained a significant positive correlation between the cellular density of Prorocentrum lima (Ehrenb.) F. Stein and the production of its toxins; while Savela et al. (2016), studying Alexandrium ostenfeldii (Paulsen) Balech & Tangen, and its gene STXA4 involved in the production of saxitoxins, found that cell density was highly related to the number of copies of the gene in a natural bloom, and therefore the cell density predicted HAB toxicity very accurately.

Acapulco Bay, an important maritime cargo port located in the southern portion of the Mexican Pacific, is a major tourist destination in the country, with approximately nine million tourists per year (Ramírez-Sáiz, 1987). In this locality high densities of phytoplankton algae have been recorded in the water column at certain times. These blooms are generally composed of one or a few species (monospecific bloom), which can even cause changes in the water color, known as red tides (Meave del Castillo and Zamudio-Resendiz, 2014; Pérez-Cruz et al., 2014). Since most of the toxic algae that form HABs affect humans, it is important to record the species and seasons in which they produce HABs in Acapulco, in order to understand the risk that they pose to marine fauna or public health.

The objective of this study was to document the species which formed blooms in Acapulco between 2000 (when the authors began their studies in that location) and 2015, based on cell density and high relative abundance. The methodology consisted of recording dates and locations where such events occurred, maximum values of cell density, and whether such species have been reported as harmful or toxic elsewhere, in order to register blooms that could actually be classified as HABs, as well as observing the existence of these events with ENSO.

Material and Methods

Study area

Acapulco Bay is located on the coast of the state of Guerrero in the Mexican tropical Pacific (99°50'52"-99°56'00"W, 16°47'00"-16°51'40"N) and its shape is semicircular (10 × 7 km) (Fig. 1). Being surrounded by mountains, the bay resembles an amphitheater and has a depth that varies from 10 to 45 m near the mouth; the sediments are composed of thick sands that are thinner towards the mouth (Bolongaro, 2014). The climate is tropical rainy, with rains during the summer (Aw), temperatures higher than 18 °C throughout the year, and average rainfall greater than 100 mm (=165.4 mm) between June to October, and values close to 4 mm (=4.16 mm) between November to May (Mayo-Vera, 2004). Based on recorded data of temperature, water salinity, and precipitation, three different seasons occur in this portion of the Mexican Pacific: a rainy season (June to October), a dry-cold season (November to March) and a dry-warm season (April to May) (Zamudio-Resendiz et al., 2014).

Figure 1: Location of Acapulco Bay, Guerrero, Mexico, with collection sites, showing the topography surrounding the bay and bathymetry of the coastal zone. Black points correspond to collection sites from 2000 to 2008, red points to collection sites from 2009 to 2015.

Characteristics of the phytoplankton community of Acapulco

This small bay has a megadiverse phytoplankton flora (Meave-del Castillo et al., 2012). To date, 730 taxa have been recorded, including species, varieties, and forms (Meave-del Castillo et al., 2012; Rojas-Herrera et al., 2012a, b; González-Rivas, 2014; Zamudio-Resendiz et al., 2014; Pinzón-Palma, 2015), mainly of dinoflagellates and diatoms, the most studied groups in Acapulco. In addition to having a rich composition, the phytoplankton community of Acapulco is also diverse, as the calculated H´ values reach up to 4 (Zamudio-Resendiz, pers. comm.). This rich and diverse flora can be explained by the oligo-mesotrophic-trophic state prevailing in the bay (Varona-Cordero et al., 2013). Given the geomorphological characteristics of Acapulco, during the rainy season it receives runoffs enriched with solid and dissolved organic matter (4086.58 m3/year, Sampedro-Rosas et al., 2014). Yet this mesotrophic environment is partly preserved due to deep ocean currents, which enter and circulate within it with a cleansing effect (Dionni and Romo, 1984). Additionally, Meave-del Castillo et al. (2012) recorded that the phytoplankton community has a variety of nutrition types, 34% being heterotrophic or mixotrophic organisms, and several of them osmotrophs, consuming organic matter, which certainly helps depuration of the bay. Sometimes, algal communities of Acapulco are exposed to high concentrations of nutrients; in the rainy season phosphates rise considerably (Meave-del Castillo et al., 2012). The increase in nutrient concentration comes from the entry of contaminated water from multiple temporary streams (Fig. 1), loaded with sewage and garbage that descend from the mountains and drain into the bay (Sampedro-Rosas et al., 2014). In this respect, the phytoplankton flora of Acapulco has shown to be quite resilient; hence, in spite of the contamination and decrease of salinity in the surface layer of the column water to which the bay is exposed during the rains (that apparently affect the phytoplankton, because in August and September the community decreases), the community recovers shortly thereafter, in approximately two months (Meave del Castillo and Zamudio-Resendiz, 2013).

Collection, identification, and evaluation of algal density

A total of 526 samples were obtained in 35 collections at several locations from May 2000 to November 2015 (Fig. 1). Four hundred twenty-three samples were collected with Van Dorn bottle at different depths (1, 3, 5, 10, 30, and 50 m) and fixed in situ with Lugol’s iodine solution, while 103 were collected with a 54 μm mesh phytoplankton net, and fixed with formaldehyde at a final concentration of 4% (Table 2). In 2010, an intensive sampling was carried out, involving monthly collections with net and bottle in eight locations, four inside the bay and another four in the surrounding coastal area indicated in red in figure 1. The collection dates were classified in one of Acapulco’s three climate seasons: dry-warm, dry-cold, and rainy (Table 2). The highest number of collections was made in the dry-cold season (15), and the lowest during the dry-warm season (6). Simultaneously with the collections, physical-chemical parameters (temperature, salinity, pH, and dissolved oxygen) were measured with multiparameter water quality instruments (YSI-556MPS, YSI-550A, Yellow Springs, USA; Thermo-OrionStarTM, Thermo Fisher Scientific Inc., Yellow Springs, USA). Water collected with a Van Dorn bottle was filtered in situ with a Millipore filtration system (Merck KGaA, Darmstadt, Alemania) and Whatman GF/F filters and frozen immediately, to be evaluated later in the laboratory. We measured concentrations of phosphate, silicate, ammonium, nitrites, and nitrates. The techniques for evaluating the nutrients are described in Meave-del Castillo et al. (2012). Atmospheric temperature and precipitation values were obtained from the meteorological station No. 768050 of the National Meteorological System (NMS).

Table 2: Phytoplankton samples collected in Acapulco Bay, Guerrero, Mexico, from 2000 to 2015, and asterisk (*) indicates the dates on which a bloom was found.

Dry-warm Season

Net

Bottle

Rainy Season

Net

Bottle

Dry-cold Season

Net

Bottle

05/2000

8

-

06/2000*

5

-

11/2002

12

-

05/2003

5

-

09/2000

5

-

12/2002*

5

-

05/2008

-

10

10/2000*

5

-

11/2003

3

-

05/2010

10

41

06/2003*

2

-

11/2006

4

-

05/2011

-

1

06/2004

6

-

03/2007

2

-

08/2013

-

1

06/2007*

5

-

11/2007

-

1

07/2008*

-

27

02/2008

7

-

09/2008

-

11

02/2009

1

-

10/2009*

9

37

03/2010*

-

38

06/2010*

8

-

11/2010*

-

38

07/2010*

1

80

01/2011*

-

41

09/2010*

-

40

03/2013*

-

8

08/2010

-

5

11/2013

-

10

08/2011

-

1

03/2014*

-

30

11/2015*

-

3

Total collection

% Season

6

17.2%

14

40%

15

42.8%

Total samples/season

% samples/seasons

23

22%

53

12.5%

46

45%

201

47.5%

34

33%

169

40%

Total net samples

103

Total Van Dorn bottle samples

423

For the identification of the taxa, the samples were observed with an optical microscope (Leica DMLB, Wetzlar, Germany), with bright field, phase contrast, epifluorescence, and integrated digital camera. In some cases, the morphology of the organisms was studied with the SEM (JEOL JSM-5900LV, Tokyo, Japan). For this purpose, samples were first fixed in the field with 2.5% glutaraldehyde and subsequently subjected to a second fixation in the laboratory with osmium tetroxide. For sensitive organisms this method was followed to critical point drying (Boltovskoy, 1995). The species were identified from morphological and morphometric characters indicated in the specialized taxonomic literature. The cell density was evaluated with the Utermöhl method (Edler and Elbrächter, 2010), using chambers with 50 ml columns, and an inverted microscope (Motic AE31, Carlsbad, Canada). Relative abundance was estimated in both net and bottle samples by counting all the species under the microscope, or until reaching 400 cells and converting the absolute data into percentages.

Criteria for considering bloom

We used the parameter of cellular densities of the taxa recorded as HAB in the literature as a criterion for considering a bloom (Table 1). Since our intention was also to evaluate the risk to human health of these events, we obtained information from the literature regarding whether the species had or had not been reported as a harmful or toxic species in Mexico or anywhere else in the world and, in the case of toxic substances, the type of poisoning they produce (Table 1). To complement this information, we undertook a search in the literature for reports of microalgae blooms in Acapulco during the study period.

Relation of HAB to global climatic conditions

To observe whether there was a relation between global climatic factors (ENSO) and HABs, we located the dates of blooms in Acapulco in a temperature anomalies graph constructed with the standardized values of Multivariate ENSO Index (MEI) with 324 data points from 1989 to 2015 (Klause, 2016), obtained from the U.S. Department of National Oceanic and Atmospheric Administration (NOAA). In the case of Gymnodinium catenatum Graham and Pyrodinium bahamense var. compressum (Böhm) Steid., Tester & F.J.R. Taylor, the maximum abundances in each of the recorded HABs were plotted to visualize the relationship of the MEI not only with the presence of the HAB, but also with the maximum values of abundance reached by the species.

The lack of Gymnodinium catenatum and Pyrodinium bahamense var. compressum abundance data for dates when they do not produce bloom in Acapulco prevented using statistical tests to evaluate the significance of the relationship of the HAB with the standardized MEI values. Therefore, to evaluate the significance of the relationship, the nonparametric Olmstead-Tukey Corner Test of Association was used (Olmstead and Tukey, 1947; Steel and Torrie, 1980), evaluating the absolute value of quadrant sum obtained from the plot done. The method considered that “the extreme values are often the best indicators of an association between variables and this test gives them special weight” (Steel and Torrie, 1980) and the accuracy of the level of significance is independent of sample size (Olmstead and Tukey, 1947).

When the HAB lasted a long time, the maximum value of abundance was located in the middle of the event. In the case of Gymnodinium catenatum, a matrix was constructed with 16 values obtained from other authors and bi-monthly values obtained by us from March 2010 to January 2011. For Pyrodinium bahamense var. compressum the matrix had data for only eight abundances because this species sporadically occurred in the bay.

Results

According to the criteria used, we recorded 53 blooms and 37 microalgal outbreaks registered by other authors in the same period were added to the list, resulting in a total of 90 microalgal blooms in Acapulco during our study period (2000-2015). Hence, we registered 88.6% of the diatom blooms and 40% of the dinoflagellates ones, meaning that 58.8% of the collections performed in Acapulco during this study had at least one sample with a bloom (Tables 3, 4).

Table 3: Data of 35 blooms recorded in Acapulco Bay, Guerrero, Mexico (2000 to 2015), conformed of 21 diatom taxa. Harmful Algal Bloom/Toxin (HAB/Tox): without apparent harm (WAH), harmful (H), toxic (T), domoic acid (DA). Maximum density recorded in Acapulco (D), relative abundance of bloom species (RA), depth at which they were located (Z). Season (S): dry-cold (DC), rainy season (R). Sea surface temperature anomalies (AT): El Niño condition (+), La Niña condition (-). Reports of harmfulness in other regions: H1=Landsberg (2002); H2=Sunesen et al. (2009). Blooms marked with asterisks (*) are events reported of bloom in Acapulco by other authors.

Taxa

HAB/

Tox

D

(cells L-1)

RA

(%)

Site

Z

(m)

Date

S

AT

1. Chaetoceros curvisetus Cleve (Fig. 3A)

WAH

-

82

Centro

-

12/2002

DC

(-)

WAH

153 × 103

59

Centro

20

07/2010

R

(-)

WAH

660 × 103

42

Bocana

1

09/2010

R

(-)

WAH

448 × 103

45

Sinfonía

2

09/2010

R

(-)

WAH

516 × 103

50

Caleta

5

09/2010

R

(-)

WAH

536 × 103

52

P. Marqués

5

09/2010

R

(-)

2. C. debilis Cleve (Fig. 3B)

H1

17.7 × 103

3

P. Marqués

3

07/2010

R

(-)

3. C. laciniosus F. Schütt (Fig. 3C)

WAH

276 × 103

80

Centro

20

01/2011

DC

(-)

4. C. lorenzianus Grunow (Fig. 3D)

H2

91.3 × 103

7

P. Marqués

5

01/2011

DC

(-)

5. C. radicans F. Schütt (Fig. 3E)

WAH

266 × 103

80

Muelle

6

09/2010

R

(-)

6. C. socialis Lauder (Fig. 3F)

H1

60.4 × 103

4

Sinfonía

1

09/2010

R

(-)

7. C. tortissimus Gran (Fig. 3G)

WAH

364 × 103

81

Bocana

3

01/2011

DC

(-)

8. C. wighami Brightw. (Fig. 3H)

H1

12.5 × 103

1.2

Bocana

3

09/2010

R

(-)

9. Climacodium frauenfeldianum Grunow (Fig. 3I)

WAH

-

86

Bocana

-

06/2000

R

(-)

WAH

-

82

Muelle

-

10/2000

R

(-)

10. Guinardia delicatula (Cleve) Hasle (Fig. 3J)

H2

100 × 103

9

Centro

3

01/2011

DC

(-)

H2

83 × 103

01/2012*

DC

(-)

11. Hemiaulus hauckii Grunow ex Van Heurck (Fig. 3K)

WAH

56 × 103

4

Sinfonía

1

09/2010

R

(-)

WAH

-

08/2006*

R

(+)

12. Leptocylindrus danicus Cleve (Fig. 3L)

H2

-

91

Bocana

-

06/2003

R

(+)

13. L. minimus Gran (Fig. 3M)

H1

287 × 103

86

Bocana

6

03/2010

DC

(+)

14. Pseudo-nitzschia delicatissima (Cleve) Heiden (Fig. 3N)

T/DA

T/DA

13.3 × 104

-

11

Muelle

1

11/2010

02/2014*

DC

DC

(-)

(-)

15. P. pungens (Grunow ex Cleve) Hasle (Fig. 3O)

T/DA

17 × 104

9

P. Marqués

1

11/2010

DC

(-)

T/DA

-

02/2014*

DC

(-)

16. P. pseudodelicatissima (Hasle) Hasle (Fig. 3P)

T/DA

22 x103

20

Pta. Bruja

3

10/2009

DC

(+)

T/DA

10.5 × 103

8

P. Marqués

5

03/2010

DC

(+)

T/DA

172 × 103

37

Bocana

1

06/2010

R

(-)

T/DA

306 × 103

82

Muelle

3

11/2010

DC

(-)

T/DA

207 × 103

15

Pta. Bruja

10

01/2011

DC

(-)

17. P. seriata (Cleve) H. Peragallo (Fig. 3Q)

T/DA

56.9 × 103

9

P. Marqués

1

07/2010

R

(-)

18. P. subfraudulenta (Hasle) Hasle (Fig. 3R)

WAH

-

82

Muelle

-

12/2002

DC

(+)

19. Skeletonema pseudocostatum Medlin (Fig. 4A)

WAH

668 × 103

84

Sinfonía

6

07/2008

R

(-)

20. S. tropicum Cleve (Fig. 4B)

WAH

-

83

Oceánica

6

12/2002

DC

(+)

21. Thalassionema nitzschioides (Grunow) Mereschk. (Figs. 4C,D)

WAH

66 × 103

81

Sinfonía

3

07/2010

R

(-)

Table 4: Data of 55 blooms recorded in Acapulco Bay, Guerrero, Mexico (2000 to 2015) conformed of 19 dinoflagellates taxa. Harmful Algal Bloom/Toxin (HAB/Tox): without apparent harm (WAH), harmful (H), toxic (T), saxitoxin (STX), yesotoxin (YTX), okadaic acid (OA). Maximum density recorded in Acapulco (D), relative abundance of bloom species (RA), depth at which they were located (Z), season (S): dry-cold (DC), dry-warm (DW), rainy season (R). Sea surface temperature anomalies (AT): El Niño condition (+), La Niña condition(-). Blooms marked with asterisks (*) events reported of bloom in Acapulco by other authors see Tables 5-6. Abundance values with (?) = extremely high values that are doubtful.

Taxa

HAB/

Tox

D

(cells L-1)

RA

(%)

Site

Z

(m)

Date

S

AT

1. Akashiwo sanguinea (Hirasaka) G. Hansen & Moestrup (Fig. 5A)

T-H

T-H

-

-

80

Centro

-

06/2003

03/2006*

R

R

(+)

(+)

T-H

564 × 103

05/2009*

DW

(-)

T-H

10 × 106

05/2013*

DW

(-)

T-H

450 × 103

04/2014*

DW

(-)

2. Dinophysis caudata Kent (Fig. 5C)

T/OA

4.2 × 103

1.4

Pta. Bruja

1

03/2010

DC

(+)

T/OA

10.9 × 103

1.8

Bocana

5

11/2010

DC

(-)

T/OA

11.1 × 103

0.9

P. Marqués

1

01/2011

DC

(-)

3. Gymnodinium catenatum Graham (Fig. 5D)

T/STX

T/STX

T/STX

-

189 × 103

2.3 × 106

88

27

73

Naval

Pta. Bruja

Naval

-

6

1

06/2003

11/2010

03/2014

R

DCDC

(+)

(-)

(-)

Ten HAB of G. catenatm (see Table 5)

T/STX

T/STX

T/STX

-

-

-

11/2001*

06/2003*

2004*

DC

R

?

(-)

(-)

(+)

T/STX

-

12/2005-

2/2006*

DC

(-)

T/STX

-

12/2007*

DC

(-)

T/STX

-

06/2009*

R

(+)

T/STX

-

10-12/2009*

DC

(+)

T/STX

-

01/2014*

DC

(-)

T/STX

-

03-04/2014*

DW

(-)

4. Karenia longicanalis Yang, Hodgkiss & G. Hansen (Fig. 5E)

WAH

72.6 × 103

76

Sinfonía

3

03/2013

DC

(-)

5. Karenia sp.

¿?

88 × 106(?)

02/2012*

DC

(-)

6. Kareniaceae cf. Takayama

¿?

13 × 107(?)

12/2007*

DC

(-)

7. Levanderina fissa (Lavander) O. Moestrup, Hakanen, G. Hansen, Daugbjerg & Ellegaard

H

2.1 × 106

01/2012*

DC

(-)

8. Lingulodinium polyedra (F. Stein) J.D. Dodge (Fig. 5F)

T/YTX

T/YTX

286 × 103

6.4 × 106

37

Oceánica

3

03/2014

04/2014*

DC

DC

(-)

(-)

9. Margalefidinium polykrikoides (Margalef) F. Gómez, Richlen & D.M. Anderson (= Cochlodinium polykrikoides Margalef) (Fig. 5B)

T-H

T-H

T-H

T-H

-

-

-

1.3 × 106

82

61

P. Marqués

Centro

-

1

11/2002

06/2003

06/2007

11/2015

DC

R

R

DC

(+)

(-)

(-)

(+)

T-H

28.1 × 106

09-10/2011*

R

(-)

T-H

T-H

22.5 × 106

340 × 103

06/2012*

10/2012*

R

R

(+)

(+)

T-H

8 × 106

09/2013*

R

(-)

T-H

103 × 103

10/2014*

R

(+)

10. Noctiluca scintillans (Macartney) Kof. & Swezy

H

603 × 103

02/2012*

DC

(-)

11. Prorocentrum gracile F. Schütt (Fig. 5G)

WAH

-

80

Bocana

-

10/2009

R

(+)

WAH

5 × 106

04/2008*

DW

(-)

12. P. koreanum M.S. Han, S.Y. Cho & P. Wang (Fig. 5H)

H

-

83

Centro

-

10/2009

R

(+)

13. Protoperidinium crassipes (Kof.) Balech (Fig. 5I)

T/YTX

-

12/2007*

DC

(-)

14. Protoperidinium divergens (Ehrenb.) Balech (Fig. 5J)

WAH

-

80

Centro

-

06/2010

R

(-)

15. Pyrodinium bahamense var. compressum (Böhm) Steid., Tester & F.J.R. Taylor (Fig. 5K)

T/STX

T/STX

T/STX

774 × 103

(Table 6)

86

Centro

3

07/2010

11/2001*

12/2005-03/2006*

R

DC

DC

(-)

(-)

(-)

T/STX

12/213-01/2014*

DC

(-)

T/STX

03/2014*

DC

(-)

16. Scrippsiella acuminata (Ehrenb.) Kretschmann, Elbr., Zinssm., Soehner, Kirsch, Kusber & Gottschling (= S. trochoidea (F. Stein) A.R. Loebl.) (Fig. 5L)

H

121 × 103

81

Sinfonía

1

10/2009

R

(+)

17. Tripos balechii (Meave, Okolodkov & Zamudio) F. Gómez f. balechii (Fig. 5M)

H

H

-

-

80

Centro

06/2003

05/2009*

R

DW

(+)

(+)

H

12 × 106

02/2012*

DC

(-)

H

40 × 107 (?)

03/2012*

DC

(-)

18. T. balechii f. longus (Meave, Okolodkov & Zamudio) F. Gómez

H

-

81

Centro

06/2000

R

(-)

19. T. furca (Ehrenb.) F. Gómez (Fig. 5N)

H

-

86

Muelle

06/2000

R

(-)

H

69.5 × 103

03/2011*

DC

(-)

H

120 × 103

04/2012*

DW

(-)

Most (18) of the diatom blooms (51.4%) occurred during the rainy season, followed by the dry-cold season (48.6%) (Table 3), and were composed of centric species, usually organized in chains or filaments (such as Chaetoceros spp.), although we also recorded some of the pennate types, such as Pseudo-nitzschia spp. and Thalassionema nitzschioides (Grunow) Mereschk. (Table 3). Additionally, most of the dinoflagellate blooms occurred in the dry-cold season (50%), mainly by Dinophysis caudata Kent, Karenia longicanalis Yang, Hodgkiss & G. Hansen and Pyrodinium bahamense var. compressum, but other dinoflagellate outbreaks occurred in the rainy season (37%, Table 4): Akashiwo sanguinea (Hirasaka) G. Hansen & Moestrup), Margalefidinium polykrikoides (Margalef) F. Gómez, Richlen & D.M. Anderson (= Cochlodinium polykrikoides Margalef), Prorocentrum gracile F. Schütt, P. koreanum M.S. Han, S.Y. Cho & P. Wang, Scrippsiella acuminata (Ehrenb.) Kretschmann, Elbr., Zinssm., Soehner, Kirsch, Kusber & Gottschling (= S. trochoidea (F. Stein) A.R. Loebl.), and Tripos balechii f. longus (Meave, Okolodkov & Zamudio) F. Gómez among them. No diatom blooms occurred at the dry-warm season, and only seven (13%) outbrakes of dinoflagellates occurred at this season corresponding to the species: Akashiwo sanguinea, Gymnodinium catenatum, Prorocentrum gracile, Tripos balechii (Meave, Okolodkov & Zamudio) F. Gómez f. balechii, and T. furca (Ehrenb.) F. Gómez (Table 4).

We found that Gymnodinium catenatum was the dinoflagellate that reached the highest density (2.3 × 106cells L-1) in the bay of Acapulco during the study period, although reports of other authors mention maximum densities of Margalefidinium polykrikoides of 28.1 × 106cells L-1 in this location during September-October 2011 (Table 4). Although the number of cells that such species must reach to produce harmful effect on biota is different: 5 × 103cells L-1 vs 500 × 103cells L-1 (Table 1), the values reached by both species in Acapulco far exceed such numbers.

Thirty-five blooms were caused by diatoms (Table 3) and 55 by dinoflagellates (Table 4). Considering the damage caused by the taxa that created the blooms, 21 (17 formed by diatoms and 4 by dinoflagellates) were classified as WAH (without apparent harm), because no deleterious effect on aquatic organisms or humans has ever been mentioned. Another 20 (8 formed by diatoms and 12 by dinoflagellates) were harmful blooms (H) and 47 (10 formed by diatoms and 37 by dinoflagellates) were classified as toxic outbreaks (T) (Tables 3, 4). As a consequence, the highest percentage (48.6%) of diatom blooms in Acapulco is classified as WAH (Fig. 2A), while the highest percentage of dinoflagellate blooms is T (67.3%) (Fig. 2B).

Figure 2: A. Percentage of diatom blooms; B. Percentage of dinoflagellate blooms recorded in Acapulco Bay, Mexico (2000 to 2015); classified for its effect. Without apparent harm (WAH), harmful (H), toxic (T).

Blooms were composed of 40 taxa: 21 diatoms (Table 3, Figs. 3A-R, 4A-D) and 19 dinoflagellates (Table 4, Figs. 5A-N). Of the species, ten diatoms were classified as WAH (without apparent harm), seven as H (Harmful), and four as T (Toxic), while for dinoflagellates, three taxa were classified as WAH, seven as H, and seven as T species. Two dinoflagellate blooms could not be classified because the species were not properly identified (Table 4).

Figure 3: Diatom taxa that produce blooms in Acapulco, Guerrero, Mexico. A. Chaetoceros curvisetus Cleve, Light Microscopy (LM); B. C. debilis Cleve (LM); C. C. laciniosus F. Schütt (LM); D. C. lorenzianus Grunow (LM); E. C. radicans F. Schütt, Scanning Electron Microscopy (SEM); F. C. socialis Lauder (LM); G. C. tortissimus Gran (LM); H. C. wighami Brightw. (LM); I. Climacodium frauenfeldianum Grunow (LM); J. Guinardia delicatula (Cleve) Hasle (LM); K. Hemiaulus hauckii Grunow ex Van Heurck (SEM); L. Leptocylindrus danicus Cleve (LM); M. L. minimus Gran (LM); N. Pseudo-nitzschia delicatissima (Cleve) Heiden (LM); O. P. pungens (Grunow ex Cleve) Hasle (LM); P. P. pseudodelicatissima (Hasle) Hasle (LM); Q. P. seriata (Cleve) H. Peragallo (LM); R. P. subfraudulenta (Hasle) Hasle (LM). Scales: A, F, G, J, N-R=20 µm; B, E, H, L, M, T=10 µm; C, D, I=50 µm; K=5 µm.

Figure 4: Diatom taxa that produce blooms in Acapulco, Guerrero, Mexico. A. Skeletonema pseudocostatum Medlin, Scanning Electron Microscopy (SEM); B. S. tropicum Cleve (SEM). C-D. Thalassionema nitzschioides (Grunow) Mereschk. (SEM), Light microscopy. Scales: A=2 µm; B, C-D=5 µm.

Figure 5: Dinoflagellate taxa that produce blooms in Acapulco, Guerrero, Mexico. A. Akashiwo sanguinea (Hirasaka) G. Hansen & Moestrup, Light Microscopy (LM); B. Margalefidinium polykrikoides (Margalef) F. Gómez, Richlen & D.M. Anderson (= Cochlodinium polykrikoides Margalef) (LM); C. Dinophysys caudata Kent, Scanning Electron Microscopy (SEM); D. Gymnodinium catenatum Graham (LM); E. Karenia longicanalis Yang, Hodgkiss & G. Hansen (LM); F. Lingulodinium polyedra (F. Stein) J.D. Dodge (SEM); G. Prorocentrum gracile F. Schütt (SEM); H. P. koreanum M.S. Han, S.Y. Cho & P. Wang (SEM); I. Protoperidinium crassipes (Kof.) Balech (LM); J. P. divergens (Ehrenb.) Balech (SEM); K. Pyrodinium bahamense var. compressum (Böhm) Steid., Tester & F.J.R.Taylor (LM); L. Scrippsiella acuminata (Ehrenb.) Kretschmann, Elbr., Zinssm., Soehner, Kirsch, Kusber & Gottschling (SEM); M. Tripos balechii f. balechii (Meave, Okolodkov & Zamudio) F. Gómez (SEM); N. T. furca (Ehrenb.) F. Gómez (SEM). Scales: a, b, d, k, m=20 µm; C, E-J, L=10 µm; N=50 µm.

WAH Blooms

Thirteen taxa (34.2%) are WAH species: 10 diatoms (Chaetoceros curvisetus Cleve, C. laciniosus F. Schütt, C. radicans F. Schütt, C. tortissimus Gran, Climacodium frauenfeldianum Grunow, Hemiaulus hauckii Grunow ex Van Heurck, Pseudo-nitzschia subfraudulenta (Hasle) Hasle, Thalassionema nitzschioides, Skeletonema pseudocostatum Medlin, and S. tropicum Cleve), and three dinoflagellates (Karenia longicanalis, Prorocentrum gracile, and Protoperidinium divergens (Ehrenb.) Balech). Even these species can be beneficial for increasing primary productivity of the system.

The diatom Skeletonema pseudocostatum had the highest densities (668 × 103cells L-1) in Acapulco during July 2008 at Sinfonía station. Of the dinoflagellates only the density of Karenia longicanalis could be evaluated with maximum values of 72.6 × 103cells L-1.

Harmful Blooms

Fourteen (36.8%) taxa have been reported as Harmful (H), of which seven diatoms (Table 3): Chaetoceros debilis Cleve, C. lorenzianus Grunow, C. socialis Lauder, C. wighami Brightw., Guinardia delicatula (Cleve) Hasle, Leptocylindrus danicus Cleve, and L. minimus Gran, and seven dinoflagellates (Table 4): Levanderina fissa (Lavander) O. Moestrup, Hakanen, G. Hansen, Daugbjerg & Ellegaard, Noctiluca scintillans (Macartney) Kof. & Swezy, Prorocentrum koreanum, Scrippsiella acuminata, Tripos balechii f. balechii, T. balechii f. longus, and T. furca (Ehrenb.) F. Gómez.

The diatom Leptocylindrus minimus had the highest densities (287 × 103cells L-1) in Acapulco during March 2010 at Bocana station. Of the dinoflagellate blooms evaluated by us, Scrippsiella acuminata reached the maximum density in Sinfonía station with a value of 121 × 103cells L-1.

Toxic Blooms

Eleven species (28.9%) taxa have been reported as Toxic (T), four diatoms (Table 3) and seven dinoflagellates (Table 4).

The four toxic diatoms belong to the genus Pseudo-nitzschia and are domoic acid (DA) producers. Only P. pseudodelicatissima (Hasle) Hasle was recorded with high densities on several occasions, with values varying from 10.5 × 103 to 306 × 103cells L-1, and a relative abundance of 8 to 82% (Table 3).

Toxic dinoflagellates that cause HABs were Akashiwo sanguinea, Dinophysis caudata, Gymnodinium catenatum, Lingulodinium polyedra (F. Stein) J.D. Dodge, Margalefidinium polykrikoides, Protoperidinium crassipes (Kof.) Balech, and Pyrodinium bahamense var. compressum, whose type of poisoning and toxin is mentioned in Table 4.

There were three blooms of Akashiwo sanguinea whose density could not be evaluated, but whose relative abundance reached 80% in June 2003.

Two blooms of Margalefidinium polykrikoides (mainly a reactive oxygen species producer) were found, one during June 2007, with a relative abundance of 82%, and another in November 2015, with an abundance of 1.3 × 106cells L-1. Other red tides of this species (11/2002, 06/2003) were observed during the period, but their density could not be evaluated because the cells agglutinated quickly, although they were fixed in situ with Lugol’s iodine solution. Another five blooms were registered in the rainy season by Gárate-Lizárraga et al. (2016), in which these species reached higher densities (Table 4).

Three blooms of Dinophysis caudata, an okadaic acid (OA) producer, were registered during the dry-cold season, reaching a maximum density of 11.1 × 103cells L-1 in January 2011 in Pto. Marqués station. These blooms were not monospecific, since D. caudata was codominant with several species and its maximum relative abundance ranged from 0.9 to 1.8%.

Harmful Algal Bloom (HAB)

A single bloom of Lingulodinium polyedra, a yessotoxin (YTX) producer, was found in Acapulco in the dry-cold season, 27-28 March 2014, outside the Acapulco Bay at the station called Oceánica, i.e., with densities up to 280 × 103cells L-1. Four days later (April 1, 2014), Pérez-Cruz et al. (2014) recorded the species with a density of 6.4 × 106cells L-1. The relative abundance of these species was 37%, co-dominating with Karenia sp., Gymnodinium catenatum, and Leptocylindrus sp.

An outbreak of Protoperidinium crassipes was reported by Gárate-Lizárraga et al. (2016), but without relative abundance or density data. We found this species frequently in Acapulco, with low densities (67-96 cells L-1, Meave-del Castillo et al., 2012).

The dinoflagellate species that produce HAB in Acapulco are Pyrodinium bahamense var. compressum and Gymnodinium catenatum, both saxitoxin (STX) producers, the latter being the most frequent with 12 blooms registered in Acapulco during the study period. This species blooms at the end or beginning of the year and rarely during the rainy season (Table 4).

Three blooms of Gymnodinium catenatum, a saxitoxin producer, were recorded in the dry-cold season, reaching a maximum density of 2.3 × 106cells L-1, during March 2014, at la Naval; these blooms even caused a reddish discoloration of the water and a concentration of saxitoxins in shellfish of 478 μgSTXeq.100g-1 shellfish (Pérez-Cruz et al., 2014). The relative abundances in these events varied from 27 to 88%, with the highest value in June 2003. Another ten HAB of G. catenatum were recorded by other authors both in the dry-cold and rainy seasons (Tables 4-5), reaching a maximum density of 54.4 × 103cells L-1 in El Niño condition (Gárate-Lizárraga et al., 2016).

Table 5: Harmful Algae Blooms of Gymnodinium catenatum Graham reported in Acapulco Bay, Guerrero, Mexico. Data of maximum density, toxin concentrations in shellfish and sea surface temperature anomalies (AT): La Niña condition (-) or El Niño condition (+); are indicated. * This value seems to be overvalued because it was measured on the same dates as other authors and exceeds in two orders of magnitude such values (Bustamante-Gil, 2011; Rojas-Herrera et al., 2012b).

Date

Density

(cells L-1)

Toxins

(μgSXTeq 100g1).

AT

Reference

1997

640

Díaz-Ortiz et al. (2010)

03/1999

37.6 × 103

156

(-)

Cabrera-Mancilla et al. (2000)

11/2001

7309

(-)

Gárate-Lizárraga et al. (2007)

06/2003

125 × 103

540

(-)

Gárate- Lizárraga et al. (2009; 2016)

2004

22 × 103

388

Díaz-Ortiz et al. (2010); Gárate-Lizárraga et al. (2016)

12/2005 to 02/2006

10 × 106

217

(-)

Gárate-Lizárraga et al. (2009)

12/2007

1.9 × 106

1152

(-)

Gárate-Lizárraga et al. (2009)

06/2009

54.4 × 103

(+)

Gárate-Lizárraga et al. (2016)

10-12/2009

6.2 × 103

17.3 × 103

13 × 106*

(+)

Bustamante-Gil (2011)

Rojas-Herrera et al. (2012b)

Gárate-Lizárraga et al. (2016)

11/2010 to 01/2011

188 × 103

392-739

(-)

Meave del Castillo and Zamudio-Resendiz (2014)

01/2014

20 × 103

(-)

Pérez-Cruz et al. (2014)

03-04/2014

8 390 × 103

474

(-)

Pérez-Cruz et al. (2014); Gárate-Lizárraga et al. (2016)

Pyrodinium bahamense var. compressum was recorded throughout the month of July 2010, on July 10th reaching the highest density of 774 × 103cells L-1 at the center of the bay, at 3 m (Table 4). A week later (July 17th, 2010) it had already decreased its density (52.3 × 103cells L-1in Pta. Bruja, at 5 m). This HAB produced a toxin concentration up to 2092 μgSTXeq 100g-1 shellfish (COFEPRIS, 2010) (Table 6), which caused the Federal Commission for the Protection Against Health Risks (COFEPRIS, 2010) to declare a sanitary closure, since according to an emerging standard, alerts are emitted after 80 μgSTXeq 100g-1shellfish (SSA, 2001). This species reached values greater than 5 × 103cells L-1 at all stations within the bay and on external sites near the bay of 3 to 10 m deep (53% of the tested samples). However, no discoloration of the sea was observed during these events. In the open sea where Z>50 m, the species had values of 3 × 103cells L-1 at depths between 1 and 3 m. A week before (7/July/2010), Laboratorio Estatal de Salud Publica del Estado de Guerrero staff (COFEPRIS, 2010) registered the HAB with a density of 1.4 × 106cells L-1 at Puerto Marqués station, which indicates that the bloom had started some time before and was already decaying when we recorded it. During August, the density inside the bay was very low but began recovering in September until reaching 7 × 103cells L-1 (Center, 10 m). By November, it was present throughout the bay with values up to 16 × 103cells L-1 (Punta Bruja, 10 m) and just in January (Naval 1 to 3 m) reached and abundance of 22 × 103cells L-1.

Table 6: Harmful Algae Blooms of Pyrodinium bahamense var. compressum (Böhm) Steid. Tester & F.J.R. Taylor, reported in locations of the eastern tropical Pacific. Date, maximum densities, toxin concentrations in different animals, and sea surface temperature anomalies (AT): La Niña conditions (-) are indicated. * In this HAB three people died, seven became ill and 206 turtles died. 1Toxins evaluated in mollusks (Stomolophus meleagris L. Agassiz). 2Toxins evaluated in turtles (Lepidochelys olivaceae Eschscholtz and Chelonia sp.). 3Toxins evaluated in jelly fish.

Locality

Date

Density

(cells L-1)

Toxins

(μgSXTeq 100g1)

AT

Reference

Oaxaca-Chiapas, Mex.

12/1989

1.7 × 106

8111

(-)

Cortés-Altamirano et al. (1993)

Michoacán-Guerrero, Mex.

10-12/1995-02/1996

85491

(-)

Ramírez-Camarena et al. (1996); Orellana-Cepeda et al. (1998)

Guerrero, Oaxaca, Chiapas, Mex.

01/2001-02/2002

3.5 × 106

73091

(-)

Ramírez-Camarena et al. (2004)

Costa Rica

12/2005-02/2006

3.5 × 106

(-)

Meave del Castillo et al. (2008)

El Salvador*

11/05-03/2006

48.9 × 106

>40001

627.82

12.23

(-)

Licea et al. (2008)

Acapulco Bay,

11/2001

73091

(-)

Gárate-Lizárraga et al. (2007)

Guerrero, Mex.

12/2005-03/2006

9.5 × 102

2001

(-)

Meave del Castillo et al. (2008)

07/2010-01/2011

1.4 × 106

20921

(-)

Gárate-Lizárraga et al. (2012), Meave-del Castillo et al. (2012)

12/2013-01/2014

45 × 103

(-)

Pérez-Cruz et al. (2014)

03/2014

21 × 103

(-)

Pérez-Cruz et al. (2014)

Some algae blooms in Acapulco were multispecies; for example, in November 2010 the event recorded in La Bocana included Gymnodinium catenatum and Dinophysis caudata, the latter reached high densities (10.9 × 103cell L-1) but low values of relative abundance (1.8%). Also on the same date, blooms of different species were found in different locations. For example, in June 2003, Tripos balechii and Akashiwo sanguinea formed blooms at the center of the bay, while Gymnodinium catenatum bloomed in La Naval, and Leptocylindrus danicus in La Bocana.

We also observed that in some cases before a HAB, several species were co-dominating and later one of them produced a monospecific HAB. For example, on March 1, 2014, Gymnodinium catenatum (3.5-46.5%), Leptocylindrus danicus (15-27%), and Cylindrotheca closterium (Ehrenb.) Reimann & J.C. Lewin (18.5-48.8%) were recorded; and at the end of the month (March 27), Gymnodinium catenatum reached a relative abundance of 15-74%.

Another 52 phytoplankton taxa (Table 7) were recorded in Acapulco, which have caused HABs in other regions, but until now they have only been found in low densities at this location, and were thus considered as potential HAB-forming taxa. The maximum relative densities and abundance found in Acapulco, as well as the type of toxin or damage they produce are shown in Table 7, which lists 28 species that have the potential to be toxic and 24 to be harmful. Most of these dinoflagellates (44.2%) could form toxic HABs, whereas most diatoms would produce harmful blooms (36.5%). The other groups (Haptophyta, Raphidophyta, and Cyanophyta) belong to only 9.6% of the total species, but should they bloom, their HAB could be toxic.

Table 7: List of phytoplanktonic taxa potential forming Harmful algal blooms (HAB) in Acapulco Bay, Guerrero, Mexico (sorted by algal group and alphabetical order), recorded in the literature as harmful (H) or toxic (T). Toxin type: domoic acid (DA), saxitoxins (STX), okadaic acid (OA), dinophysis toxins (DTx), pectenotoxins (PTx), breve toxins (PbTx), brevisulcata toxins (KBTx, (DTx), brevesulcatic acid (BSX), superoxidant agents (ROS), yesotoxins (YTx), azaspiracides (AZP), chatonella toxins (CaTx), fibrocapsa toxins (FjTx) and polyunsaturated aldehydes (PUAs). Frequency data (Frec.) and maximum density (D) achieved in the bay are given; density not determined since the taxa was found only in net samples (ND). References: 1) Eilertsen and Raa (1995); 2) Shamsudin et al. (1996); 3) Balech (2002); 4) Landsberg (2002); 5) Fryxell and Hasle (2003); 6) Taylor et al. (2003); 7) Hallegraeff and Hara (2003); 8) Hansen et al. (2004); 9) Hsia et al. (2006); 10) Proenza et al. (2009); 11) Steidinger (2009); 12) Sunesen et al. (2009); 13) Guidi-Rontani et al. (2010); 14) Fowler et al. (2015); 15) Akselman and Fraga (2016); 16) Fraga (2016); 17) Hansen (2016); 18) Hoppenrath and Elbraechter (2016); 19) Lundholm (2016); 20) Moestrup (2016a); 21) Moestrup (2016b); 22) Zingone and Larsen (2016). *= Usually Phalacroma rotundatum is not a toxic species, but some authors reports that it may contain DTx (Zingone and Larsen, 2016).

Algae group/Taxa

HAB

Toxin

Reference

Frec.

(%)

D

(cells L-1).

Bacillariophyta

1. Cerataulina pelagica (Cleve) Hendey

H

-

4,5,12

46.6

21.7 × 103

2. Chaetoceros convolutus Castracane

H

-

4,5

0.9

ND

3. C. danicus Cleve

H

-

12

10.6

6.9 × 103

4. C. difficilis Cleve

H

-

4

1.5

ND

5. Coscinodiscus centralis Ehrenb.

H

-

5

7.3

739

6. C. concinnus W. Smith

H

-

5

3.3

82

7. C. wailesii Gran & Angst

H

-

5,12

0.6

ND

8. Cylindrotheca closterium

H

-

4,5,12

82.4

61.2 × 103

9. Ditylum brightwellii (T. West) Grunow

H

-

4

53.3

11.1 × 103

10. Pseudo-nitzschia multistriata (H. Takano) H. Takano

T

DA

4,5,19

ND

11. Pseudosolenia calcar-avis (A. Schultze) Sundström

H

-

12

20.3

5 × 103

12. Rhizosolenia setigera Brightw.

H

-

12

18.2

14.7 × 103

13. R. setigera f. pungens (Cleve) Brunel

H

-

12

62.5

20.7 × 103

14. Thalassiosira mala Takano

H

-

5,12

0.3

ND

15. T. minuscula Krasske

H

-

5

4.8

14.2 × 103

16. T. gravida Cleve

H

-

4

10.9

8.4 × 103

17. T. simonsenii Hasle & G. Fryxell

H

-

12

1.5

ND

18. T. subtilis (Ostenf.) Gran

H

-

5

2.4

1 × 103

Dinophyta

19. Alexandrium catenella (Whedon & Kof.)Balech

T

STX

3,6,16

0.3

ND

20. A. monilatum (Howell) Balech

T

Goniodomin A

3,6,9,16

ND

21. A. ostenfeldii (Paulsen) Balech & Tangen

T

STX

6,16

3.0

3 × 103

22. A. tamarense (M. Lebour) Balech

T

STX

3,6,16

19.1

2.6 × 103

23. Dinophysis acuminata Clap. & J. Lachm.

T

OA, DTx, PTx

3,6,22

1.5

171

24. D. fortii Pavill.

T

OA, DTx, PTx

3,6,22

8.2

1.6 × 103

25. D. infundibulus J. Schiller

T

PTx

22

0.3

20

26. D. ovum F. Schütt

T

OA

22

0.3

ND

27. D. sacculus F. Stein

T

OA

6,22

0.3

ND

28. Gonyaulax polygramma F. Stein

H

-

4

35.2

2.6 × 103

29. G. spinifera (Clap. & J. Lach.) Diesing

H

-

4,15

17.9

4.9 × 103

30. Karenia bicuneiformis Botes, Sym & Pitcher

T

PbTx

17

6.7

4.5 × 103

31. K. brevis (Davis) G. Hansen & Moestrup

T

PbTx

4,6,11,17

8.5

4.5 × 103

32. K. brevisulcata (F.H. Chang) G. Hansen & Moestrup

T

KBTx, BSX

4,6,17

7.3

1.5 × 103

33. K. mikimotoi (Miyake & Kominami ex M. Oda) G. Hansen & Moestrup

T

Gymnocin A + B

4,6,17

3.0

1.7 × 103

34. K. papilionacea Haywood & Steid.

T

PbTx

14,17

1.8

491

35. K. selliformis Haywood, Steid. & L. Mack.

T

Gymnodimina

11,17

11.8

9.4 × 103

36. Noctiluca scintillans (Macartney) Kof. & Swezy

H

-

4,6

11.2

3.1 × 103

37. Peridinium quadridentatum (F. Stein) G. Hansen (= P. quinquecorne Abé)

H

-

2

1.1 × 103

38. Phalacroma dolychopterigium G. Murray & Whiting

H

-

20

0.3

ND

39. P. mitra F. Schütt

T

DTx

3,6,22

2.7

38

40. P. rotundatum (Clap.et J. Lach.) Kof. & J. R. Michener

T

DTx*

3,6,22

6.0

721

41. Prorocentrum cordatum (Ostenf.) J.D. Dodge

T

Unknown

6,18

9.1

5.8 × 103

42. P. rhathymum A.R. Loebl., Sherley & R.J. Schmidt

T

Unknown

6,18

4.9

717

43. P. triestinum J. Schiller

H

-

4

3.0

7.4 × 103

44. Protoceratium reticulatum (Clap. & J. Lach.) Buetschli

T

YTx

6,15

6.9

571

45. Protoperidinium crassipes (Kof.) Balech

T

AZP

4

4.2

96

46. Takayama cladochroma (J. Larsen) de Salas, Bolch & Hallegr.

T

Unknown

17,19

0.3

ND

47. Tripos fusus (Ehrenb.) F. Gómez

H

-

6

58.2

3.1 × 103

Raphidophyta

48. Chattonella antiqua (Y. Hada) C. Ono

T

PbTx+CaTx+ROS

4,7,21

1.8

87

49. Fibrocapsa japonica Toriumi & Takano

T

PbTx+FjTx+ROS

4,7,13,21

0.6

ND

Haptophyta

50. Phaeocystis globosa Scherff.

T

PbTx+CaTx

1,4,20

6.9

202 × 103

51. Phaeocystis pouchetii (Har.) Lagerh.

T

PUAs

1,4,8,20

ND

Cyanophyta

52. Trichodesmium erythraeum Ehrenb. ex Gomont

T

STX+Microcystin

4,10

1.2

212 × 103

Physical-chemical parameters were obtained from 700 data in the monthly collections made in 2010 (Meave del Castillo, 2012) and the sporadic data measured during the samplings carried out during the entire study period (2000-2015). Water temperature had a range of 16.43-31.03 °C (=27.37 °C), with the highest values in August 2010. Beginning in April, water temperature rises and in September it decreases, with the lowest values in February-March. Salinity ranged from 29.5-38.31 throughout the year (=34.04); during the rainy season and until December, salinity is lower than in the dry season (November to May). Dissolved oxygen varied from 0.52 to 11.19 mg L-1 (=5.96 mg L-1), decreasing during the dry-cold season (December to March). Nutrients had the following concentrations: P-PO4=0.001-13.59 μM (=1.7 μM), N-NO2=0.001-22.33 μM (=0.53 μM), N-NO3=0.001-27.64 μM (=2.6 μM), N-NH4=0.0001-33.42 μM (=2.44 μM), SiO2=0.0001-8.42 μM (=0.79 μM), chlorophyll a=0.001-46.27 mgL-1 (=4.91 mgL-1). Generally in Acapulco, we have observed that phosphate increases in the rainy season, which coincides with the increase of air temperature in the water column. Ammonium and silicates have low values, which remain more or less constant throughout the year, while nitrites + nitrates increase in the dry-cold season.

Acapulco monthly rainfall data, obtained from the NMS (National Meteorological System), for a period of 30 years (1973-2010), show that August is the rainiest month of the year, with an average close to 200 mm. In particular, the year 2010 was very rainy, and in August values close to 500 were reached (Meave del Castillo, 2012; Meave-del Castillo et al., 2012).

The dates of the blooms on the graph of temperature anomalies show that the majority of blooms (75.6%) occurred during negative anomalies (La Niña conditions) of the historical average value of MEI obtained during 27 years (1989-2015) (Fig. 6A), for example, Pyrodinium bahamense var. compressum. On the other hand, twelve blooms of Gymnodinium catenatum were found eight in La Niña (66.7%) and four (33.3%) in El Niño conditions, e.g., at the end of 2009 (October to December). When the species occured in El Niño conditions, densities are low: maximum abundances were 6.2-17.3 × 103cells L-1 (Table 5, Fig. 6B). The value of 13 × 106cells L-1 reported by Gárate-Lizárraga et al. (2016) seems to be overvalued, because it was measured on the same dates as other authors and exceeds such values in two orders of magnitude.

Figure 6: A. Location of the dates of the HAB events of Gymnodinium catenatum Graham and Pyrodinium bahamense var. compressum (Böhm) Steid., Tester & F.J.R.Taylor in the tropical eastern Pacific, on the graphic of temperature anomalies of the Pacific. The graph was constructed with monthly values of the ENSO Multivariate Index (MEI) from 1989 to 2015. The MEI includes six climatic variables. Positive anomalies indicate that the temperature observed was warmer than the historical average, negative anomalies indicate that the observed temperature was colder than the historical average. Values above 1.0 or below -1.0 indicate conditions El Niño or La Niña respectively. B. Graphic of abundances of Gymnodinium catenatum and Pyrodinium bahamense var. compressum on the dates in which they produced HAB in Acapulco Bay, Mexico.

On the other hand, in Figure 7, corresponding to the Corner Test for Association, it is observed that quadrant sums resulted in a value of 13. Using the table of significance levels for magnitudes of quadrant sums contained in Olmstead andTukey (1947), this value was significant (p=0.000036), which means that despite the few data included in the analysis, the relationship of the development of HAB of these noxious species with climatic conditions tending to La Niña or even in La Niña can be accepted.

Figure 7: Location in the Olmstead-Tukey quadrants of the abundance levels with respect to the standardized MEI values for Gymnodinium catenatum Graham and Pyrodinium bahamense var. compressum (Böhm) Steid., Tester & F.J.R.Taylor when they formed HAB in Acapulco Bay, Mexico.

Discussion

Fifty-three blooms of 40 species were found. A literature review showed at least 30 additional blooms reported by other authors who work at local institutions and can make collections in the bay at any time (Rojas-Herrera et al., 2012a, b; Pérez-Cruz et al., 2014, 2016; Moreno-Díaz et al., 2015; Gárate-Lizárraga et al., 2016). This means that with the 35 collections that we made during the study period, we were able to record 63.4% of the algal blooms that occurred in Acapulco (2000-2015). Most blooms recorded by other authors included species that, on a different occasion, we also found as blooms or as species that we recorded but at low densities, such as Karenia spp., Levanderina fissa and Noctiluca scintillans (Gárate-Lizárraga et al., 2016).

Our results suggest that Acapulco blooms occurred in the rainy and dry-cold seasons; these results are due to the low number of collections (six) made during the dry-warm season, thus underestimating the results. Pérez-Cruz et al. (2014) and Gárate-Lizárraga et al. (2016) reported blooms of several dinoflagellates during this season, e.g. Gymnodinium catenatum in April 2012 (137 × 103cells L-1), May 2013 (2.72 × 106cells L-1), January 2014 (20 × 103cells L-1) and March-April 2014 (1.89 × 106cells L-1); Tripos furca (120 × 103cells L-1) in April 2012; Akashiwo sanguinea (10 × 106cells L-1) in May 2013; and Lingulodinium polyedra (6.4 × 106cells L-1) in March 2014.

Most diatom blooms occurred during the rainy season (Chaetoceros curvisetus, Climacodium frauenfeldianum, Leptocylindrus danicus, Skeletonema pseudocostatum and Thalassionema pseudonitzchioides) or the dry-cold season (Guinardia delicatula, Leptocylindrus minimus and Pseudo-nitzschia spp.). These data are consistent with the bloom of Pseudo-nitzschia spp. recorded in February 2014 by Gárate-Lizárraga et al. (2016). The only diatom species, which by its densities and type of damage could have produced a HAB, was Pseudo-nitzschia pseudodelicatissima in November 2010, reaching a density of 306 × 103cells L-1 at Muelle. However, apparently these blooms did not affect aquatic organisms or human health in Acapulco.

Likewise, 49% of dinoflagellate blooms occurred in the dry-cold season (Dinophysis caudate, Gymnodinium catenatum, a taxon of Kareniaceae family related to Takayama, Lingulodinium polyedra, and Pyrodinium bahamense var. compressum), while 37.7% occurred in the rainy season mainly from, Margalefidinium polykrikoides, Protopedinidium divergens and Scrippsiella acuminata.

The rainy and dry seasons contrast because their environmental parameters (temperature, precipitation, salinity, and nutrients) change drastically (Meave-del Castillo et al., 2012), which makes it difficult to understand what factors are leading to the blooms, especially for diatoms, since silica concentrations in general are low in Acapulco (=0.79 µM). It was found that most diatom blooms (85%) occurred in La Niña conditions or during a transition to La Niña. The only blooms that occurred in El Niño conditions were originated by Leptocylindrus minimus, Pseudo-nitzschia psedodelicatissima, Pseudo-nitzschia subfraudulenta, and Skeletonema tropicum. After recording the dates of the dinoflagellate blooms on the graph of temperature anomalies, we found that most occurred in La Niña conditions, although Akashiwo sanguinea, Dinophysis caudata, Prorocentrum gracile, Prorocentrum koreanum. Scrippsiella acuminata, and Tripos balechii bloom during El Niño conditions.

WAH Blooms

The Karenia longicanalis bloom reached a significant cell density of 72.6 × 103cells L-1, but was classified as WAH, because it did not produce any apparent damage in Acapulco. This agrees with the observation of the bloom of this species in Hong Kong during May 1998 that was also not harmful and characterized as a non-producing species of brevetoxins (PbTx) (Yang et al., 2001). We note the density values found by Gárate-Lizárraga et al. (2016) for the bloom of Karenia sp. and Kareniaceae cf. Takayama in February 2012 and December 2007, with 88 × 106 and 13 × 107cells L-1, respectively. These data seem to be overvalued because these species are relatively large (ca. 40 μm) and authors such as Yang et al. (2001) report densities of up to 180 × 103cells L-1 in massive blooms of K. longicanalis in China.

Prorocentrum gracile and Protoperidinium divergens classified as WAH were considered innocuous in spite of registering high relative abundance values (80%), because in the literature they have never been identified as producing toxins or causing anoxia.

Harmful blooms

The bloom of Levanderina fissa had high densities (2.1 × 106cells L-1) in Acapulco (January 2012); however, it was not considered a HAB producer at that time because its densities must exceed 13 × 106cells L-1 to produce anoxia (Jiménez, 1993). Additionally, the maximum density recorded in Acapulco by Noctiluca scintillans did not appear to be very high (603 × 103cells L-1), although it could have a negative effect on the environment, because its density exceeded the value of 500 × 103cells L-1 reported by Adnan (1989) to cause massive mortality of marine organisms. This species causes damage because it increases the ammonium concentrations in the water and reduces the O2 for its heterotrophic metabolism. All blooms can cause oxygen depletion when they decay because of decomposition of dead cells by bacteria.

Blooms of Prorocentrum koreanum (usually identified as P. micans Ehrenb.) showed that it was only relatively abundant (>80%). It was not possible to evaluate the risk of outbreak produced by this species in Acapulco, since harmful effects are mentioned when their densities are higher than 1 × 106cells L-1. Prorocentrum koreanum was recently identified as a distinct species from populations of Prorocentrum micans, both by molecular techniques (secuences of ITS) and morphological features such as pattern of pores of trichocysts on valves and periflagellar platelets (Han et al., 2016). Since all the reports in Acapulco relating to these taxa have been named P. micans, it would first be necessary to identify the Acapulco specimens properly to know if both species are present and which taxa produces the blooms and whether that species is harmful or not.

Scrippsiella acuminata is a species that frequently produces blooms that had been considered non-toxic or harmful, with only an old report that indicated it caused anoxia (Whitelegge, 1891). Recently, however, it has been found that even at low densities (1 × 104cells L-1) it affects larvae of bivalve mollusks, because it prevents their feeding (Tang and Glober, 2012). In October 2009 in Acapulco, abundance far surpassed (121 × 103cells L-1) these density values and since there are bivalve banks on the rocky shores of the bay, it is possible that this species could have a negative effect on these benthic communities.

Within the species of Tripos (= Ceratium) bloom producers, we recorded two in Acapulco (Tripos furca, Tripos balechii f. balechii and Tripos balechii f. longus). Tripos furca has been mentioned as a noxious species affecting fish either by anoxia or by increasing ammonium concentrations (Matthews and Pitcher, 1996; Orellana-Cepeda et al., 2004); however, in Acapulco this species did not reach the densities (1 × 107cells L-1) mentioned in those references that are necessary to produce harmful effects. Nevertheless, T. balechii in Acapulco reached densities of up to 12 × 106cells L-1 (Gárate-Lizárraga et al., 2016), which is considered a risk to benthic invertebrates because at St. Helena Bay, Africa, massive lobster mortality has been reported with densities of 7.3 × 106cells L-1 (Pitcherd and Probyn, 2011). The density data of 400 × 106cells L-1 recorded by Gárate-Lizárraga et al. (2016) during March 2012 may be incorrect, since the highest densities found by other authors on massive blooms are two orders of magnitude lower (Pitcherd and Probyn, 2011). Even in Mexico, the dense HAB of T. furca (a species of similar characteristics), that caused important harmful effects in the fauna of Baja California reported by Orellana et al. (2004), reached a maximum value of 1 × 106cells L-1.

Toxic Blooms

Unfortunately, in Acapulco it was not possible to evaluate the density of Akashiwo sanguinea blooms. However, during the event recorded in June 2003 it reached a relative abundance of 80%. The effects of this species that commonly forms red tides are contradictory in literature; older citations refer to it as toxic for mollusk larvae and adults and even fish (Nightingale, 1936; Tindall et al., 1984; Carlson and Tindall, 1985; Shumway, 1990). Landsberg (2002) points out that it is a producer of ROS, and Cortés-Altamirano and Hernández-Becerril (1998) maintain that it is a producer of PSP; both affirmations, however, seem to be erroneous. Other authors mention that Akashiwo sanguinea is not really toxic, but causes anoxia that can kill marine fish and invertebrates (Horner et al., 1997). The most modern references show that this species exhibits toxicity only to the larvae and embryos of abalone (Botes et al., 2003); relatively low densities of this species (3.1 × 105cells L-1) cause 50% larvae mortality. Furthermore, it has been reported that this species has caused seabird deaths on the Pacific coast of the USA (Monterrey, California, and Oregon) at densities of 4 × 105cells L-1 (Jessup et al., 2009; Du et al., 2011). The mortality is not due to a toxin but to a mechanism of saponification, produced by yellowish green foam that acts as a surfactant, stripping the oils from seabird feathers and causing death from hypothermia (Jessup et al., 2009).

Several blooms of Margalefidinium polykrikoides were found in Acapulco with maximum densities of 28.1 × 106cells L-1 and 82% relative abundance. This species is characterized as ichthyotoxic with negative effects on fish from 2.7 × 106cells L-1 (Whyte et al., 2001). Massive fish mortalities have already been reported at sites along the Mexican Pacific: in Bahía de La Paz with densities of 7 × 106cells L-1 (Gárate-Lizárraga et al., 2004) and in Bahía de Banderas with densities of 10.8 × 106cells L-1(Cortés-Lara et al., 2004). However, in Acapulco there has been no mortality of fish related to these blooms, probably because there are no feed cages for fish.

There are reports that Margalefidinium polykrikoides presents multiple ecophysiological attributes that allow it to develop in a variety of environmental conditions (e.g., eurythermal and euryhaline, withstand surface water photoinhibition, a mixotrophic diet combining phagotrophy and osmotrophy, and ability to use different sources of nitrogen) (Lee et al., 2001; Park et al., 2001; Kudela and Glober, 2012). Additionally, the species has multiple mechanisms that damage organisms of the aquatic community and different toxic agents (neurotoxic, hemolytic, hemagglutinationand zinc-bound PSP) (Onoue and Nozawa, 1989a, b), that also produces superoxide anions (O2-*), hydrogen peroxide (H2O2) that caused lipid peroxidation that kill fish, and secreted cytotoxic agents and mucus substances (polysaccharides) that cause fish to die (Kim et al., 2001). Toxins of Margalefidinium can target a broad range of organisms and tissue types. The most vulnerable are the smallest individuals and larvae of fish, shellfish, and plankton. The Margalefidinium HAB can last for long periods because it reduces grazing; their toxins cause the decrease of predators by producing the death of filtering bivalves and planctophagous fish. In addition, they have allelopathic effects that causes the decrease of several competing phytoplanktonic species facilitating the initiation of blooms (Kudela and Gobler, 2012).

In the case of the Dinophysis caudata bloom, there was no positive relationship between the density and relative abundance (RA). Hence, in the samples where D. caudata was present, it only reached less than 2% of RA (Table 4); however, it appears on the list of species that formed blooms in Acapulco, due to its cellular densities (4.2 × 103-11.1 × 103cells L-1), which exceeded the density of 1.8 × 102-1 × 103cells L-1, indicated by Reguera (2002) and Reguera et al. (2014), to consider a HAB of Dinophysis spp.

Although the density values of Lingulodinium polyedra measured in the bloom of March 2014 may seem low, the species was considered as a HAB, based on the criterion set out by Paz et al. (2008) who consider that this species produces HAB when its densities are greater than 1 × 103cells L-1.

Harmful algal blooms (HAB)

Although Pyrodinium bahamense var. compressum is not the most frequent species within toxic dinoflagellate species, due to the levels of toxicity that are produced in mollusks, is the most important species in terms of HABs in Acapulco, and fortunately it is sporadic. In the last 25 years (1989-2015), it has produced five HABs in the southern region of Mexican Pacific (MP) of which only three had an impact in Acapulco (Table 6), with maximum densities of 1.4 × 106cells L-1and maximum concentrations of saxitoxins of 7309 μgSTXeq 100g-1 shellfish.

Seventy six percent of the 17 HAB reported in Acapulco during 2000-2015 of the toxic species Pyrodinium bahamense var. compressum and Gymnodinium catenatum occurred in La Niña conditions, according to the graph of temperature anomalies using the MEI values (Table 4). The Olmstead-Tukey Corner Test of Association showed that the relation of the occurrence of the HAB with La Niña was significant for both species when the water temperature of the surface decreases. In the case of Pyrodinium bahamense var. compressum, these results seem to contradict those of Maclean (1989) who points out a relation of the occurrence of HAB in the western Pacific with El Niño conditions. Without exception, all dates on which the species produced HAB in the Mexican Pacific have coincided with La Niña conditions. This was confirmed by the palynological study of Sánchez-Cabeza et al. (2012) that included a long-time series (from 1938 to 2010) and found a positive correlation between the decrease in the water surface temperature and the flow of sedimented cysts. Another interesting aspect found by the same authors is that HAB development of Pyrodinium bahamense var. compressum correlates with rainfall conditions that exceed a monthly average of 400 mm. The monthly average recorded in the rainy season of 2010 when an important HAB of Pyrodinium bahamense var. compressum occurred in Acapulco was exceeded, reaching about 500 mm in August (Meave-del Castillo et al., 2012).

According to Usup et al. (2012), Pyrodinium bahamense var. compressum is not a good competitor for resources and in order to grow requires terrigenous supplements such as selenium that is introduced to the marine system by temporary drainage during rainfalls. This fact, together with the qualities of Pyrodinium bahamense var. compressum, i.e., eurythermal (20-36 °C) and euryhaline (24.7-38.5), probably allowed the development of the HAB in the bay (Usup et al., 2012). Another factor that could favor this HAB is the predominant nitrogen source, given that Pyrodinium bahamense var. compressum prefers the nitrate and has a low ammonium tolerance, and the oxygen conditions in Acapulco (=5.96 mg L-1) favor the predominance of oxidized forms of nitrogen (NO2+NO3).

HAB of Pyrodinium bahamense var. compressum match with the observations of other authors who have evaluated HABs of this species through their sedimented cysts (Flores-Trujillo et al., 2009).

The first Gymnodinium catenatum HAB reported for the Mexican Pacific (MP) occurred on the Gulf of California in April 1979 (Mee et al., 1986), also during La Niña conditions. Additionally, some observations indicate that a negative rate of temperature change favors the bloom of this species in Acapulco (Meave del Castillo and Zamudio-Resendiz, 2014).

In July 2010, Gymnodinium catenatum appeared along with P. bahamense var. compressum but in low concentrations (1.7 × 103cells L-1); later, in November, G. catenatum increased, reaching concentrations of 38.3 × 103cells L-1. Hallegraeff et al. (2012) indicate that G. catenatum prefers ammonium as a source of nitrogen. Generally in Acapulco, the forms of nitrogen oxidized with respect to ammonium predominate; however, at the end of the year and the start of the following year (during the dry-cold season), ammonium increases and reaches maximum values of 33.42 µM, since the average annual value in the bay is 2.44 µM. A relationship of increased toxicity has been found when G. catenatum consumes ammonium as a nitrogen source (Flynn et al., 1996), so a G. catenatum HAB that occurs in Acapulco from October to January may be more harmful due to an increase in its toxicity, as shown in Table 6.

Since Acapulco Bay is located in a tropical zone, changes in water temperature due to the ENSO do not vary drastically compared to “normal” years. For this reason, we assume that the HABs that occur in Acapulco in El Niño conditions are more influenced by the greater precipitation that comes under these conditions than merely by higher temperatures. This factor should be considered with the fact that torrential rains influence the nutrient concentration of the water column due to the terrigenous elements carried by the run-off from the mountains to the bay. Surely this is the reason why certain diatoms (Table 3) (Hemiaulus hauckii, Leptocylindrus danicus, Pseudo-nitzschia seriata, and other dinoflagellates (Table 4) (Akashiwo sanguinea, Margalefidinium polykrikoides, Prorocentrum gracile, P. koreanum, Scrippsiella acuminata, and Tripos balechii, which bloom under El Niño conditions, were present only during the rainy season. This demonstrates that in tropical marine oligo-mesotrophic areas such as Acapulco Bay, where several species compete for resources, harmful species may find a window of opportunity to bloom at any time; however, this may be masked because the high species richness decreases the abundance (absolute and relative) of the noxious species.

Table 7 shows 52 potential HAB-forming species, of which the most important to monitor are Alexandrium and Pseudo-nitzschia, since the low values of phosphorus and the availability of inorganic nitrogen compounds in Acapulco would favor such species. Some reports indicate that deficiencies in inorganic P and increased availability of organic N enhance the toxicity in Alexandrium (Matsuda et al., 1996). Moreover the decrease of phosphorus and silica increase the content of domoic acid in Pseudo-nitzschia (Anderson et al., 2009).

Given that the density values of the bloom-forming species in Acapulco, reported by Gárate-Lizárraga et al. (2016), are much higher than those found on similar dates by the authors of this study, by even a one, two or three order of magnitude, we consider that it is important to perform an intercalibration of methods to discard possible errors.

Author contributions

Both authors realized the collections and identification of algae. MEZR quantified the samples by Utermöhl method and developed the photographic plates and tables. MEMC drafted the manuscript. Both authors contributed to the discussion, review and approval of the final manuscript.

Funding

The Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) granted the financial support to develop the project “Diversity and dynamics of marine phytoplankton in Acapulco Bay, Guerrero” (HJ014).

Acknowledgments

We wish to thank the Laboratory of Coastal Ecosystems of the Universidad Autónoma Metropolitana, Unidad Iztapalapa, especially Francisco Varona, and Erick Ponce Manjarrez for assistance in the evaluation of water nutrients and phytoplankton biomass from Acapulco Bay. To Manuel A. Castillo Rivera for advicing on statistical analysis, José Sepúlveda Sánchez, for providing guidance during SEM manipulation. We thank Karen Steidinger for reviewing the paper. We also sincerely thank Saúl López Silva and Elizabeth Godoy Galeana, ex-Director and Director of the Laboratorio Estatal de Salud Pública del Estado de Guerrero (LESP-GRO.), and Celso Barrila Álvarez, Director of the Facultad de Ecología Marina de la Universidad Autónoma del Estado de Guerrero, for the loan of motor boats to carry out the sampling during the study.

Literature cited

Adnan, Q. 1989. Red tides due to Noctiluca scintillans (MacCartney) Ehrenb. and mass mortality of fish in Jakarta Bay. In: Okaichi, T., D. M. Anderson and T. Nemoto (eds.). Red tides, Biology, Enviromental Science and Toxicology. Elsevier. New York, USA. Pp. 53-55.

Akselman, R. and S. Fraga. 2016. Other Gonyaulacales. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Anderson, D. M. 2007. The ecology and oceanography of harmful algal blooms: multidisciplinary approaches to research and management. Intergovernmental Oceanographic Commission Technical Series 74: 1-28.

Anderson, C. R., D. A. Siegel, R. M. Kudela and M. A. Brzezinski. 2009. Empirical models of toxigenic Pseudo-nitzschia blooms: Potential use as a remote detection toll in the Santa Barbara Channel. Harmful Algae 8(3): 478-492. DOI: https://doi.org/10.1016/j.hal.2008.10.005

Azanza, M. P. V., R. V. Azanza, V. M. D. Vargas and C. T. Hedreyda. 2006. Bacterial endosymbionts of Pyrodinium bahamense var. compressum. Microbial Ecology 52(4): 756-764. DOI: https://doi.org/10.1007/s00248-006-9128-7

Balech, E. 2002. Dinoflagelados tecados tóxicos en el Cono Sur Americano. In: Sar, E. A., M. E. Ferrario and B. Reguera (eds.). Floraciones algales nocivas en el Cono Sur Americano. Instituto Español de Oceanografía. Madrid, España. Pp. 123-144.

Bates, S. S., D. L. Garrison and R. Horner. 1998. Bloom dynamics and physiology of Domoic-Acid-Producing Pseudo-nitzschia species. In: Anderson, D. M., A. D. Cembella and G. M. Hallegraeff (eds.). Physiological ecology of harmful algal blooms. Springer-Verlag. Heidelberg, Germany. Pp. 267-292.

Bolongaro, A. (coord.). 2014. Sección II Vulnerabilidad del destino turístico Acapulco. Estudio de la vulnerabilidad y programa de adaptación ante la variabilidad climática y el cambio climático en diez destinos turísticos estratégicos, así como propuesta de un sistema de alerta temprana a eventos hidrometeorológicos extremos. Consejo Nacional de Ciencia y Tecnología-Secretraria de Turismo. Cuernavaca, Morelos, México. Pp. 1-31. http://www.sectur.gob.mx/wp-content/uploads/2014/09/SECCION-II.-ACAPULCO.pdf (consulted April, 2017).

Boltovskoy, A. 1995. Técnicas en microscopía electrónica de barrido: aplicación a las microalgas. In: Alveal, K., M. E. Ferrario, C. E. Oliveira and E. Sar (eds.). Manual de Métodos Ficológicos. Anibal Pinto, S.A. Concepción, Chile. Pp. 119-138.

Botes, L., A. J. Smit and P. A. Cook. 2003. The potential threat of algal blooms to the abalone (Haliotis midae) mariculature industry situated around the South African coast. Harmful Algae 2: 247-259. DOI: https://doi.org/10.1016/s1568-9883(03)00044-1

Bustamante-Gil, C. 2011. Variación espacial y temporal de los dinoflagelados marinos (Dinophyta) en La Bahía de Acapulco en diferentes épocas de año. Tesis de maestría. Universidad Autónoma Metropolitana. México, D.F., México. 106 pp.

Cabrera-Mancilla, E., C. Ramírez-Camarena, L. Muñoz-Cabrera and A. Monreal-Prado. 2000. Primer registro de Gymnodinium catenatum Graham (Gymnodiniaceae) como causante de marea roja en La Bahía de Acapulco Gro., México. In: Ríos-Jara, E., E. Juárez-Castillo, M. Pérez-Peña, E. López-Uriarte, E. G. Robles-Jarero, D. U. Hernández-Becerril and M. Silva-Briano (eds.). Estudios sobre plancton en México y el Caribe. Sociedad Mexicana de Planctonología y Universidad de Guadalajara. México, D.F., México. Pp. 86-86.

Carlson, R. D. and D. R. Tindall. 1985. Distribution and periodicity of toxic dinoflagellates in the Virgin Islands. In: Anderson, D. M., A. W. White and D. G. Baden (eds.). Toxic dinoflagellates. Elsevier. New York, USA. Pp. 171-176.

COFEPRIS. 2010. Informe de Presencia de Marea Roja en Costas Nacionales durante 2010. Comisión Federal de Protección contra Riesgos Sanitarios. México. http://www.cofepris.gob.mx/AZ/Documents/MareaRoja/FAN2010.pdf (consulted April, 2016).

Corrales, R. A. and J. L. Maclean. 1995. Impacts of harmful algae on sea farming in the Asia-Pacific areas. Journal of Applied Phycology 7(2): 151-162. DOI: https://doi.org/10.1007/bf00693062

Cortés-Altamirano, R. and D. U. Hernández-Becerril. 1998. Especies responsables y probables de mareas rojas. In: Cortes-Altamirano, R. (ed.). Las mareas rojas. AGT editor, S.A. México, D.F., México. Pp. 43-80.

Cortés-Altamirano, R., L. Muñoz-Cabrera and O. Sotomayor-Navarro. 1993. Envenenamiento paralítico por marisco (PSP), causado por el dinoflagelado Pyrodinium bahamense var. compressum en la costa suroeste de México. Anales del Instituto de Ciencias del Mar y Limnología 20(1): 43-54.

Cortés-Lara, M. C., R. Cortés-Altamirano and A. P. Sierra-Beltrán. 2004. Presencia de Cochlodinium catenatum (Gymnodiniales: Gymnodiniaceae) en mareas rojas de Bahía de Banderas, Pacífico mexicano. Revista de Biología Tropical 52(Suppl. 1): 35-49.

Díaz-Ortiz, J. A., B. Pérez-Cruz, R. Valdovinos-Sánchez, M. A. Alarcón-Romero, S. López-Silva, L. Chávez-Almazán and J. L. García-Barbosa. 2010. Registro histórico de marea roja en la Bahía de Acapulco de 1992 a 2010. Red Sanitaria 7: 1-4.

Dionni, G. W. and R. A. Romo. 1984. Estudio de las corrientes en primavera y verano de la Bahía de Acapulco. Centro de Estudios Ecológicos, Secretaria de Hacienda y Recursos Hidraulicos (SARH). México, D.F., México. 30 pp.

Du, X., W. Peterson, A. McCulloch and G. Liu. 2011. An unusual bloom of the dinoflagellate Akashiwo sanguinea off the central Oregon, USA, coast in autumn 2009. Harmful Algae 10(6): 784-793. DOI: https://doi.org/10.1016/j.hal.2011.06.011

Edler, L. and M. Elbrächter. 2010. The Utermöhl method for quantitative phytoplankton analysis. In: Karson, B., C. Cusack and E. Bresnan (eds.). Microscopic and molecular methods for quantitative phytoplankton analysis. United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 13-20.

Eilertsen, H. C. and J. Raa. 1995. Toxins in seawater produced by a common phytoplankter Phaeocystis pouchetii. Journal of Marine Biotechnology 3(1): 115-119.

Flores-Trujillo, J. G., J. Helenes, J. C. Herguera and E. Orellana-Cepeda. 2009. Palynological record (1483-1994) of Gymnodinium catenatum in Pescadero Basin, southern Gulf of California, Mexico. Marine Micropaleontology 73(1-2): 80-89. DOI: https://doi.org/10.1016/j.marmicro.2009.06.009

Flynn, K. J., K. Flynn, E. H. John, B. Reguera, M. I. Reyero and J. M. Franco. 1996. Changes in toxins, intracellular and dissolved free amino acids of the toxic dinoflagellate Gymnodinium catenatum in response to change in organic nutrients and salinity. Journal of Plankton Research 18(11): 2093-2111. DOI: https://doi.org/10.1093/plankt/18.11.2093

Fowler, N., C. Tomas, D. Baden, L. Campbell and A. Bourdelais. 2015. Chemical analysis of Karenia papilionacea. Toxicon 101: 85-91. DOI: https://doi.org/10.1016/j.toxicon.2015.05.007

Fraga, S. 2016. Alexandrium & Pyrodinium. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO)-Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Fryxell, G. A. and G. R. Hasle. 2003. Taxonomy of harmful diatoms. In: Hallegraeff, G. M., D. M. Anderson and A. D. Cembella (eds.). Manual on Harmful Marine Microalgae. United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 465-510.

Gárate-Lizárraga, I., D. J. López-Cortes, J. J. Bustillos-Guzmán and F. Hernández-Sandoval. 2004. Blooms of Cochlodinium polykrikoides (Gymnodiniaceae) in the Gulf of California, Mexico. Revista de Biología Tropical 52(suppl. 1): 51-58.

Gárate-Lizárraga, I., J. A. Díaz-Ortiz, M. Alarcón-Tacuba, B. Pérez-Cruz, A. Torres-Jaramillo, M. A. Alarcón-Romero and S. López-Silva. 2007. Paralytic shellfish toxin marine mollusks from the Southwestern region of the Mexican coasts (1992-2006). 40th Annual Meeting of the Western Society of Malacologists. La Paz, México. Pp. 50-51.

Gárate-Lizárraga, I., J. A. Díaz-Ortiz, B. Pérez-Cruz, M. Alarcón-Tacuba, A. Torres-Jaramillo, M. A. Alarcón-Romero and S. López-Silva. 2009. Cochlodinium polykrikoides and Gymnodinium catenatum in Bahía de Acapulco, Mexico (2005-2008). Harmful Algae News 40: 8-9.

Gárate-Lizárraga, I., B. Pérez-Cruz, J. A. Díaz-Ortiz, M. Alarcón-Tacuba, L. A. Chávez-Almazán, M. A. Alarcón-Romero, S. López-Silva, J. J. Bustillos-Guzmán and S. Licea-Durán. 2012. Toxicity and paralytic toxin profile in Pyrodinium bahamense var. compressum and violet oyster in Bahía de Acapulco, Guerrero, Mexico. Harmful Algae News 45: 2-3.

Gárate-Lizárraga, I., B. Pérez-Cruz, J. A. Díaz-Ortiz, Y. B. Okolodkov and S. López-Silva. 2016. Florecimientos algales nocivos en las aguas costeras del estado de Guerrero, México. In: García-Mendoza, E., S. I. Quijano-Scheggia, A. Olivos-Ortiz and E. J. Núñez-Vázquez (eds.). Florecimientos algales nocivos en México. Centro de Investigación Científica y de Educación Superior de Ensenada. Ensenada, México. Pp. 228-241.

González-Rivas, D. A. 2014. Estudio de diatomeas de la clase Bacillariophyceae de la Bahía de Acapulco. Tesis de maestría. Facultad de Ciencias, Universidad Nacional Autónoma de México. Cd. Mx., México. 137 pp.

Guidi-Rontani, C., U. Maheswari, K. Jabbari and C. Bowler. 2010. Comparative ecophysiology and genomics of the toxic unicelular algal Fibrocapsa japonica. New Phytologist 185(2): 446-458. DOI: https://doi.org/10.1111/j.1469-8137.2009.03074.x

Hallegraeff, G. M. 2010. Ocean Climate Change, Phytoplankton community responses, and Harmful Algal Blooms: a formidable predictive challenge. Journal of Phycology 46(2): 220-235. DOI: https://doi.org/10.1111/j.1529-8817.2010.00815.x

Hallegraeff, G. M., S. I. Blackburn, M. A. Doblin and C. J. S. Bolch. 2012. Global toxicology, ecophysiology and population relationships of the chainforming PST dinoflagellate Gymnodinium catenatum. Harmful Algae 14: 130-143. DOI: https://doi.org/10.1016/j.hal.2011.10.018

Hallegraeff, G. M. and Y. Hara. 2003. Taxonomy of harmful marine Raphidophytas. In: Hallegraeff, G. M., D. M. Anderson and A. D. Cembella (eds.). Manual on Harmful Marine Microalgae. United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 511-522.

Han, M. S., P. Wang, J. H. Kim, S. Y. Cho, B. S. Park, J. H. Kim, T. Katano and B. H. Kim. 2016. Morphological and molecular phylogenetic position of Prorocentrum micans sensu stricto and description of Prorocentrum koreanum sp. nov. from Southerns coastal waters in Korea and Japan. Protist 167(1): 32-50. DOI: https://doi.org/10.1016/j.protis.2015.12.001

Hansen, G. 2016. Gymnodiniales. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Hansen, E., A. Ernstsen and H. C. Eilertsen. 2004. Isolation and characterization of a cytotoxic polyunsaturated aldehyde from the marine phytoplankter Phaeocystis pouchetii (Hariot) Lagerheim. Toxicology 199(2-3): 207-217. DOI: https://doi.org/10.1016/j.tox.2004.02.026

Hoppenrath, M. and M. Elbraechter. 2016. Prorocentrales. In: Moestrup, Ø., R. Akselmann,S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Horner, R. A., D. L. Garrison and F. G. Plumley. 1997. Harmful algal blooms and red tide problems on the U.S. west coast. Limnology and Oceanography 45(5, part 2): 1076-1088. DOI: https://doi.org/10.4319/lo.1997.42.5_part_2.1076

Hsia, M. H., S. L. Morton, L. L. Smith, K. R. Beauchesne, K. M. Huincik and P. D. R. Moeller. 2006. Production of goniodomin A by the planktonic, chain-forming dinoflagellate Alexandrium monilatum (Howell) Balech isolated from the Gulf Coast of the United States. Harmful Algae 5(3): 290-299. DOI: https://doi.org/10.1016/j.hal.2005.08.004

Jessup, D. A., M. A. Miller, J. P. Ryan, H. M. Nevins, H. A. Kerkering, A. Mekebri, D. B. Crane, T. A. Johnson and R. M. Kudela. 2009. Mass stranding of marine birds caused by a Surfactant-producing red tide. PLos ONE 4(2): e4550. DOI: https://doi.org/10.1371/journal.pone.0004550

Jiménez, R. 1993. Ecological factors related to Gyrodinium instriatum bloom in the inner estuary of the Gulf of Guayaquil. In: Smayda, T. J. and Y. Shimizu (eds.). Toxic Phytoplankton Blooms in the Sea. Proceedings of the 5th International Conference on Toxic Marine Phytoplankton. Elsevier. Amsterdam, Netherlands. Pp. 257-262.

Kim, C. S., S. G. Lee, H. G. Kim and J. S. Lee. 2001. Screening for toxic compounds in the Red Tide Dinoflagellate Cochlodinium polykrikoides: Is it toxic plankton? Algae 16(4): 457-462.

Klause, W. 2016. Extended Multivariate ENSO Index (MEI.ext). Earth System Research Laboratory. Physical Sciences Division. NOAA. www.esrl.noaa.gov/psd/enso/mei.ext/#Home (consulted November, 2017)

Kudela, R. M. and C. J. Glober. 2012. Harmful dinoflagellate blooms caused by Cochlodinium sp.: Global expansion and ecological strategies facilitating bloom formation. Harmful Algae 14: 71-86. DOI: https://doi.org/10.1016/j.hal.2011.10.015

La Barbera-Sánchez, A. S. 1991. Mussel toxicity caused by red tide of Noctiluca scintillans in Punta Patilla Bay, Sucre State, Venezuela. Red Tide Newlsett 4(2-3): 1.

Landsberg, J. H. 2002. The effects of Harmful Algal Blooms on Aquatic Organisms. Reviews in Fisheries Science 10(2): 113-390. DOI: https://doi.org/10.1080/20026491051695

Lee, C. K., H. C. Kim, S. G. Lee, C. S. Jung, H. G. Kim and W. A. Lim. 2001. Abundance of harmful algae, Cochlodinium polykrikoides, Gyrodinium impudicum and Gymnodinium catenatum in the coastal area of South Sea of Korea and their effects of temperature, salinity, irradiance and nutrient on the growth in culture. The Korean Society of Fisheries and Aquatic Science 34(5): 536-544.

Lefebvre, K. A., M. W. Silver, S. L. Coale and R. S. Tjeerdema. 2002. Domoic acid in planktivorous fish in relation to toxic Pseudo-nitzschia cell densities. Marine Biology 140(3): 625-631. DOI: https://doi.org/10.1007/s00227-001-0713-5

Licea, S., A. Navarrete, J. Bustillos and B. Martínez. 2008. Monitoring a Bloom of Pyrodinium bahamense var. compressum in the El Salvador and the southern coast of Mexico (November 2005-March 2006). In: Moestrup, Ø. (ed.). Proceedings of the 12th International Conference on Harmful Algae. International Society for the Study of Harmful Algae. Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 86-89.

Lorrain, A., Y. M. Paulet, L. Chauvaud, N. Savoye, E. Nézan and L. Guérin. 2000. Growth anomalies in Pecten maximus from coastal waters (Bay of Brest, France): relationship with diatoms blooms. Journal of the Marine Biological Association of the United Kingdom 80(4): 667-673. DOI: https://doi.org/10.1017/s0025315400002496

Lundholm, N. 2016. Bacillariophyceae. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Maclean, J. L. 1989. Indo-Pacific Red Tides, 1985-1988. Marine Pollution Bulletin 20(7): 304-310. https://doi.org/10.1016/0025-326X(89)90152-5

Matsuda, A., T. Nishijima and K. Fukami. 1996. Effects of nitrogen deficiency on the PSP production by Alexandrium catenella under axenic cultures. In: Yasumoto, T., Y. Oshida and Y. Fukuyo (eds.). Harmful and toxic Algal Blooms. Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 305-308.

Matthews, S. G. and G. C. Pitcher. 1996. Worst recorded marine mortality on the South African coast. In: Yasumoto, T., Y. Oshida and Y. Fukuyo (eds.). Harmful and toxic Algal Blooms. Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). París, France. Pp. 89-92.

Mayo-Vera, A. B. 2004. Estudio Ambiental de la bahía de Acapulco, Guerrero. Tesis de licenciatura. Facultad de Ingeniería, Universidad Nacional Autónoma de México. México, D.F., México. 76 pp.

Meave del Castillo, M. E. 2012. Diversidad y dinámica del fitoplancton marino en la bahía de Acapulco, Guerrero. Universidad Autónoma Metropolitana-Unidad Iztapalapa. Informe final Sistema Nacional de Información sobre Biodiversidad - Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, proyecto No. HJ014. México, D.F., México.

Meave del Castillo, M. E. and M. E. Zamudio-Resendiz. 2013. Efecto del ENOS en la ocurrencia de dinoflagelado Pyrodinium bahamense var. compressum en la región del Pacífico tropical mexicano. In: Gúzman Hernández, T. J. (ed.). Resúmenes VII Congreso de la Red Latinoamericana de Ciencias Ambientales. Instituto Tecnológico de Costa Rica. Alajuela, Costa Rica. Pp. 182-183.

Meave del Castillo, M. E. and M. E. Zamudio-Resendiz. 2014. Co-occurrence of toxic dinoflagellates Pyrodinium bahamense var. compressum and Gymnodinium catenatum in Acapulco Bay, Mexico. In: Kim, H. G., B. Reguera, G. H. Hallegraeff, C. K. Lee, M. S. Han and J. K. Choi (eds.). Harmful Algae 2012, Proceedings of the 15th International Conference on Harmful Algae. International Society for the Study of Harmful Algae. Busan, Korea. Pp. 112-115.

Meave del Castillo, M. E., R. S. Rodríguez-Salvador and M. Vargas-Montero. 2008. Blooms of Pyrodinium bahamense var. compressum along the Pacific Coast of Central America and southern Mexico. In: Moestrup, Ø. (ed.). Proceedings of the 12th International Conference on Harmful Algae. International Society for the Study of Harmful Algae and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). Copenhagen, Denmark. Pp. 212-215.

Meave-del Castillo, M. E., M. E. Zamudio-Resendiz and M. A. Castillo Rivera. 2012. Riqueza fitoplanctónica de la Bahía de Acapulco y zona costera aledaña, Guerrero, México. Acta Botanica Mexicana 100: 405-487. DOI: https://doi.org/10.21829/abm100.2012.41

Mee, L. D., M. Espinosa and G. Díaz. 1986. Paralytic shellfish poisoning with Gymnodinium catenatum red tide on the Pacific coast of Mexico. Marine Environmental Research 19(1): 77-92. DOI: https://doi.org/10.1016/0141-1136(86)90040-1

Merino-Virgilio, F. C., Y. B. Okolodkov, A. C. Aguilar-Trejo, I. Osorio-Moreno, E. Luc and J. A. Herrera-Silverira. 2014. Florecimientos de Cylindrotheca closterium (Bacillariophyceae) en el norte de Yucatán (2001-2014). Resúmenes del XXI Congreso Nacional de Ciencia y Tecnología del Mar. México, D.F., México.

Moestrup, Ø. 2016a. Haptophyta. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Moestrup, Ø. 2016b. Raphidophyceae. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Moreno-Díaz, G., A. A. Rojas-Herrera, J. González-González, J. Violante-González, J. L. Rosas-Acevedo and S. García-Ibañez. 2015. Temporal variation in the abundance and composition of phytoplankton species, collected with net in the Acapulco Bay, Mexico. Revista Bio Ciencias 3(2): 88-102.

Negri, R. M. and D. Inza. 1998. Some potentially toxic species of Pseudo-nitzschia in the Argentina Sea (35°-39°S). In: Reguera, B., J. Blanco, M. Fernández and T. Wyatt (eds.). Harmful Algae, Proceedings of the 8th International Conference on Harmful Algae. Xunta de Galicia & Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). Vigo, Spain. Pp. 84-85.

Nightingale, W. H. 1936. Red water organisms: their occurrence and influence upon marine aquatic animals, with special reference to shellfish in waters of the Pacific coast. Argus Press, Seattle. Washington, USA. 24 pp.

Olmstead, P. S. and J. W. Tukey. 1947. A corner test for association. Annals of Mathematical Statistics 18(4): 495-513. DOI: https://doi.org/10.1214/aoms/1177730341

Onoue, Y. and K. Nozawa. 1989a. Separation of toxins from harmful red tides occurring along the coast of Kagoshima Prefecture. In: Okaichi, T., D. M. Anderson and T. Nemoto (eds.). Red Tides, Biology, Environmental Science and Toxicology. Elsevier. New York, USA. Pp. 371-374.

Onoue, Y. and K. Nozawa. 1989b. Zinc-bound PSP toxins separated from Cochlodinium red tide. In: Natori, S., K. Hashimoto and Y. Ueno (eds.). Mycotoxins and Phycotoxins’ 88. Elsevier. Amsterdam, Netherlands. Pp. 359-366.

Orellana-Cepeda, E., E. Martínez-Romero, L. Muñoz-Cabrera, P. López-Ramírez, E. Cabrera-Mancilla and C. Ramírez-Camarena. 1998. Toxicity associated with blooms of Pyrodinium bahamense var. compressum in southwestern Mexico. In: Reguera, B., J. Blanco, M. Fernández and T. Wyatt (eds.). Harmful Algae, Proceedings of the 8th International Conference on Harmful Algae. Xunta de Galicia & Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). Vigo, Spain. Pp. 60-63.

Orellana-Cepeda, E., C. Granados-Machuca and J. Serrano-Esquer. 2004. Ceratium furca: One possible cause of mass mortality of cultures blue-fin tuna at Baja California, Mexico. In: Steidinger, K. A., J. Landsberg, C. R. Tomas and G. A. Vargo (eds.). Harmful Algae 2002. Proceedings of the 10th International Conference on Harmful Algae. Florida Fish and Wildlife Conservation Commission, Florida Institute of Oceanography and Intergovernmental Oceanographic Commission of United Nations Educational, Scientific and Cultural Organization (UNESCO). St Petersburg, USA. Pp. 514-516.

Park, J. G., M. K. Jeong, J. A. Lee, K. J. Cho and O. S. Kwon. 2001. Diurnal vertical migration of a harmful dinoflagellate, Cochlodinium polykrikoides (Dinophyceae) during a red tide in coastal waters of Namhae Island, Korea. Phycologia 40(3): 292-297. DOI: https://doi.org/10.2216/i0031-8884-40-3-292.1

Paz, B., A. H. Daranas, M. Norte, P. Riobó, J. M. Franco and J. J. Fernández. 2008. Yessotoxins, a group of marine polyether toxins: an overview. Marine Drugs 6(2): 73-102. DOI: https://doi.org/10.3390/md6020073

Pérez-Cruz, B., J. A. Díaz-Ortiz, M. A. Mata-Díaz and I. Gárate-Lizárraga. 2014. Proliferación de Microalgas en las costas del Estado de Guerrero (diciembre 2013-abril 2014). Foro de Estudios sobre Guerrero 1(1): 413-417.

Pérez-Cruz, B., M. A. Mata-Díaz, D. Garibo-Ruíz and J. A. Díaz-Ortíz. 2016. Evaluación de toxinas paralizantes (TP) durante cinco años (2010-2014) en Guerrero. Foro de Estudios sobre Guerrero 2(3): 23-27.

Pinzón-Palma, E. A. 2015. Estudio Taxonómico y ecológico de los dinoflagelados planctónicos del Orden Peridiniales de la Bahía de Acapulco, con énfasis en las familias Diplopsaliaceae y Protoperidiniaceae. Tesis de maestría. Universidad Autónoma Metropolitana. México, D.F., México. 278 pp.

Pitcherd, G. C. and T. A. Probyn. 2011. Anoxia in southern Benguela during the autumm of 2009 and its linkage to a bloom of the dinoflagellate Ceratium balechii. Harmful Algae 11: 23-32. DOI: https://doi.org/10.1016/j.hal.2011.07.001

Proenza, L. A. O., M. S. Tamanaha and R. S. Fonseca. 2009. Screening the toxicity and toxin content of blooms of the Cyanobacterium Trichodesmium erythraeum (Ehrenberg) in Northeast Brazil. Journal of Venomous Animals and Toxins including Tropical Diseases 15(2): 204-215. DOI: https://doi.org/10.1590/s1678-91992009000200004

Ramírez-Camarena, C., L. Muñoz-Cabrera, E. Cabrera-Mancilla, A. R. Castro-Ramos, P. López-Ramírez and E. Orellana-Cepeda. 1996. Identificación de la marea roja frente a la costa suroeste de México en oct-dic, 1995. I Reunión Internacional de Planctología y VIII Reunión Nacional de la Sociedad Mexicana de Planctología. Pátzcuaro, México. p. 47.

Ramírez-Camarena, C., A. Martínez-García, N. Juárez-Ruiz, R. Rojas-Crisóstomo and H. Ramírez-García. 2004. Impactos de Pyrodinium bahamense var. compressum durante el florecimiento algal nocivo 2001-2002, en la costa suroeste de México. XIII Reunión Nacional de la Sociedad Mexicana de Planctología, A.C. y VI Reunión Internacional de Planctología. Nuevo Vallarta, México. p. 62.

Ramírez-Sáiz, J. M. 1987. Turismo y medio ambiente: El caso de Acapulco. Estudios Demográficos y Urbanos 2(3): 479-512.

Reguera, B. 2002. Establecimiento de un programa de seguimiento de microalgas tóxicas. In: Sar, E. A., M. E. Ferrario and B. Reguera (eds.). Floraciones Algales Nocivas en el Cono Sur Americano. Instituto Español de Oceanografía. Pontevedra, España. Pp. 21-54.

Reguera, B., P. Riobó, F. Rodríguez, P. A. Díaz, G. Pizarro, B. Paz, J. M. Franco and J. Blanco. 2014. Dinophysis toxins: Causative organism, distribution and fate in shellfish. Marine Drugs 12(12): 394-461. DOI: https://doi.org/10.3390/md12010394

Reich, A., R. Lazensky, J. Faris, L. E. Fleming, B. Kirkpatrik, S. Watkins, S. Ullmann, K. Kohler and P. Hoagland. 2015. Assessing the impact of shellfish harvesting area closures on neurotoxic shellfish poisoning (NSP) incidence during red tide (Karenia brevis) blooms. Harmful Algae 43: 13-19. DOI: https://doi.org/10.1016/j.hal.2014.12.003

Rojas-Herrera, A. A., J. Violante-González, V. M. G. Sevilla-Torres, J. S. Gil-Guerrero, P. Flores-Rodríguez and A. A. Rendón-Dircio. 2012a. Species composition and abundance of phytoplankton communities in Acapulco Bay, Mexico. International Research Journal of Microbiology 3(9): 307-316.

Rojas-Herrera, A. A., J. Violante-González, S. García-Ibáñez, V. M. G. Sevilla-Torres, J. S. Gil-Guerrero and P. Flores-Rodríguez. 2012b. Temporal variation in the phytoplankton community of Acapulco Bay, Mexico. Microbiology Research 3(1): 13-19. DOI: https://doi.org/10.4081/mr.2012.e4

Sampedro-Rosas, M. L., A. L. Juárez-López and J. L. Rosas-Acevedo. 2014. Estimación de la contaminación por desechos antropogénicos en cauces de la ciudad de Acapulco, Guerrero, México. Tlamati 5(1): 35-42.

Sánchez-Cabeza, J. A., A. C. Ruiz-Fernández, A. de Vernal and M. L. Machain-Castillo. 2012. Reconstruction of Pyrodinium blooms in the tropical East Pacific (Mexico): are they related to ENSO? Environmental Science and Technology 46(12): 6830-6834. DOI: https://doi.org/10.1021/es204376e

Savela, H., K. Harju, L. Spoof, E. Lindehoff, J. Meriluoto, M. Vehniäinen and A. Kremp. 2016. Quantity of the dinoflagellate sxtA4 gene and cell density correlates with paralytic shellfish toxin production in Alexandrium ostenfeldii blooms. Harmful Algae 52: 1-10. DOI: https://doi.org/10.1016/j.hal.2015.10.018

Schoemann, V., S. Becquevort, J. Stefels, V. Roisseau and C. Lancelot. 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. Journal of Sea Research 53(1-2): 43-66. DOI: https://doi.org/10.1016/j.seares.2004.01.008

Shamsudin, S., M. A. Awang, A. Ambak and A. Ibrahim. 1996. Dinoflagellate bloom in tropical fish ponds of coastal waters of the South China Sea. Environmental Monitoring and Assessment 40: 303-311.

Shumway, S. E. 1990. A review of the effects of algal blooms on shellfish and aquaculture. Journal of the World Aquaculture Society 21: 65-104.

Smayda, T. J. 1997. What is a bloom? A commentary. Limnology and Oceanography 42 (5, part 2): 1132-1136. DOI: https://doi.org/10.4319/lo.1997.42.5_part_2.1132

SSA. 2001. Norma Oficial Mexicana de Emergencia NOM-EM-005-SSA1-2001. Salud Ambiental. Especificaciones sanitarias para el control de los moluscos bivalvos y otros moluscos expuestos a la marea roja. Criterios para proteger la salud de la población. Secretaría de Salud. Diario Oficial de la Federación. Cd. Mx., México. http://www.salud.gob.mx/unidades/cdi/nom/em5ssa11.html

Steel, R. G. D. and J. H. Torrie. 1980. Principles and procedures of statisctics. A Biometrical Aproach. McGraw-Hill, Inc. New York, USA. 633 pp.

Steidinger, K. A. 2009. Historical perspective on Karenia brevis red tide in the Gulf of Mexico. Harmful Algae 8(4): 549-561. DOI: https://doi.org/10.1016/j.hal.2008.11.009

Sunesen, I., A. Bárcena and E. A. Sar. 2009. Diatomeas potencialmente nocivas del golfo de San Matías (Argentina). Revista de Biología Marina y Oceanografía 44(1): 67-88. DOI: https://doi.org/10.4067/s0718-19572009000100007

Tang, Y. Z. and C. J. Glober. 2012. Lethal effects of Northwest Atlantic Ocean isolates of the dinoflagellate, Scrippsiella trochoidea, on Eastern oyster (Crassostrea virginica) and Northern quahog (Mercenaria mercenaria) larvae. Marine Biology 159(1): 199-210. DOI: https://doi.org/10.1007/s00227-011-1800-x

Taylor, F. J. R., Y. Fukuyo, J. Larsen and G. M. Hallegraeff. 2003. Taxonomy of harmful dinoflagellates. In: Hallegraeff, G. M., D. M. Anderson and A. D. Cembella (eds.). Manual on Harmful Marine Microalgae. United Nations Educational, Scientific and Cultural Organization(UNESCO). Landais, France. Pp. 389-431.

Tesfay, A. H. 2011. Evolution of cell density and toxin production of a Harmful Algal Bloom species in marine microcosms. Master degree thesis. Faculty of Bioscience Engineering, Ghent University. Flandes, Belgium. 45 pp.

Tindall, D. R., R. W. Dickey, R. D. Carlson and G. Morey-Gaines. 1984. Ciguatoxigenic dinoflagellates from the Caribbean Sea. In: Ragelis, E. P. (ed.). Seafood toxin. American Chemical Society Symposium Series 262: 225-240.

Trainer, V. L., S. S. Bates, N. Lundholm, A. E. Thessen, W. P. Cochlan, N. G. Adams and C. G. Trick. 2012. Pseudo-nitzschia physiological ecology, phylogeny, toxicity, monitoring and impacts on ecosystems health. Harmful Algae: 14: 271-300. DOI: https://doi.org/10.1016/j.hal.2011.10.025

Usup, G., A. Ahmad, K. Matzuoka, P. T. Lim and C. P. Leaw. 2012. Biology, ecology and bloom dynamics of the toxic marine dinoflagellate Pyrodinium bahamense. Harmful Algae 14: 301-312. DOI: https://doi.org/10.1016/j.hal.2011.10.026

Varona-Cordero, F., M. E. Zamudio-Resendiz, R. I. Herrera-Moro Chao, F. Gutiérrez-Mendieta and M. E. Meave del Castillo. 2013. Estado trófico de la Bahía de Acapulco basado en la calidad de agua y fitoplancton. Resúmenes de IV Congreso Mexicano de Ecología 2013. Sociedad Científica Mexicana de Ecología. Villahermosa, México. p. 156.

Villarreal, T. A., C. G. Brown, M. A. Brzesinski, J. W. Krause and C. Wilson. 2012. Summer Diatom blooms in the North Pacific Subtropical Gyre: 2008-2009. PLoS ONE 7(4): e33109. DOI: https://doi.org/10.1371/journal.pone.0033109

Whitelegge, T. 1891. On the recent discoloration of the waters of Port Jackson. Records of the Australian Museum 1: 179-192.

Whyte, J. N. C., N. Haigh, N. G. Ginther and L. J. Keddy. 2001. First record of blooms of Cochlodinium sp. (Gymnodiniales, Dinophyceae) causing mortality to aquaculture salmon on the west coast of Canada. Phycologia 40(3): 298-304. DOI: https://doi.org/10.2216/i0031-8884-40-3-298.1

Yang, Z. B., I. J. Hodgkiss and G. Hansen. 2001. Karenia longicanalis sp. nov. (Dinophyceae): a new bloom-forming species isolated from Hong Kong, May 1998. Botanica Marina 44(1): 67-74. DOI: https://doi.org/10.1515/bot.2001.009

Zamudio-Resendiz, M. E., D. A. González-Rivas and M. E. Meave del Castillo. 2014. Evaluation of Pseudo-nitzschia spp. in a tropical bay of the Mexican Pacific. In: Kim, H. G., B. Reguera, G. M. Hallegraeff, C. K. Lee, M. S. Han and J. K. Choi (eds.). Harmful Algae 2012, Proceedings of the 15th International Conference on Harmful Algae. International Society for the Study of Harmful Algae. Busan, Korea. Pp. 33-36.

Zhu, X. S., B. Yi, Y. H. Dong and L. F. Yang. 2004. A primary study on one of the “bilateral” red tide at Chi Bay of Pearl River Estuary. Marine Enviromental Science 23(4): 41-44.

Zingone, A. and J. Larsen 2016. Dinophysiales. In: Moestrup, Ø., R. Akselmann, S. Fraga, M. Hoppenrath, M. Iwataki, J. Komárek, J. Larsen, N. Lundholm and A. Zingone (eds.). Intergovernmental Oceanographic Commission - United Nations Educational, Scientific and Cultural Organization (UNESCO) - Taxonomic Reference List of Harmful Micro Algae. http://www.marinespecies.org/HAB (consulted November, 2016).

Enlaces refback

  • No hay ningún enlace refback.


Copyright (c) 2018 Acta Botanica Mexicana

Licencia de Creative Commons
Este obra está bajo una licencia de Creative Commons Reconocimiento-NoComercial 4.0 Internacional.

 

Cintillo Legal

Acta Botanica Mexicana, Núm. 124, julio 2018. Publicación trimestral editada por el Instituto de Ecología, A.C., a través del Centro Regional del Bajío. www.inecol.mx

Editor responsable: Marie-Stéphanie Samain. Reservas de Derechos al Uso Exclusivo No. 04-2016-062312171000-203, ISSN electrónico 2448-7589, ambos otorgados por el Instituto Nacional del Derecho de Autor.

Responsable de la última actualización: Marie-Stéphanie Samain. Ave. Lázaro Cárdenas 253, C.P. 61600 Pátzcuaro, Michoacán, México. Tel. +52 (434) 1 17 95 13, fecha de última actualización, 6 de septiembre de 2018.

ISSN electrónico: 2448-7589

Licencia Creative Commons

Esta obra está bajo una Atribución-No Comercial (CC BY-NC 4.0 Internacional).

Basada en una obra en abm.ojs.inecol.mx