Taxocoenosis of epibenthic dinoflagellates in the ...

Marine Pollution Bulletin 119 (2017) 396–406

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Taxocoenosis of epibenthic dinoflagellates in the coastal waters of the northern Yucatan Peninsula before and after the harmful algal bloom event in 2011–2012 Ana C. Aguilar-Trujillo a,⁎, Yuri B. Okolodkov b, Jorge A. Herrera-Silveira a, Fany del C. Merino-Virgilio a, Citlalli Galicia-García b,c a Centro de Investigación y Estudios Avanzados – Instituto Politécnico Nacional, Unidad Mérida, Departamento de Recursos del Mar, Laboratorio de Producción Primaria, Carretera Antigua a Progreso km 6, Col. Gonzalo de Guerrero, C.P. 97310 Mérida, Yucatán, Mexico b Instituto de Ciencias Marinas y Pesquerías, Universidad Veracruzana, Laboratorio de Botánica Marina y Planctología, Calle Hidalgo No. 617, Col. Río Jamapa, C.P. 94290 Boca del Río, Veracruz, Mexico c Instituto Tecnológico de Boca del Río, Laboratorio de Biología, km 12 Carretera Veracruz-Córdoba, C.P. 94290 Boca del Río, Veracruz, Mexico

a r t i c l e

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Article history: Received 2 August 2016 Received in revised form 23 February 2017 Accepted 27 February 2017 Available online 22 March 2017 Keywords: Epibenthic dinoflagellates Eutrophication Gulf of Mexico Harmful algal blooms Microalgae Microphytobenthos

a b s t r a c t Eutrophication causes the major impact in the coastal waters of the state of Yucatan. In general, loss of water quality and biological communities and massive development of toxic microorganisms are some of the consequences of this phenomenon. To reveal changes in species composition and cell abundance of the taxocoenosis of epibenthic dinoflagellates before and after a harmful algal bloom event in the water column that lasted about 150 days (August–December 2011) in the Dzilam – San Crisanto area (northern Yucatan Peninsula, southeastern Gulf of Mexico) were the main objectives of the present study. In August 2011 and September 2012, sampling along 20 transects perpendicular to the coastline along the entire northern Yucatan coast, starting from 20 sampling sites from El Cuyo in the east to Celestún in the west, at a distance of 50, 150 and 250 m from the coast, was carried out. Physicochemical characteristics measured before and after the bloom were within the ranges previously reported in the study area. Salinity was the most stable characteristic, with mean values of 36.25 and 36.42 in 2011 and 2012, respectively. Phosphates were the only parameter that showed a wide range with higher values before the bloom (0.03–0.54 μM/l). A total of 168 macrophyte (seaweeds and seagrasses), sponge and sediment samples (105 in 2011 and 63 in 2012) that included associated microphytobenthos were taken by snorkeling from 0.7 to 5 m depth. Six substrate types were distinguished: Chlorophyta, Phaeophyceae, Rhodophyta, Angiospermae (seagrasses), Demospongiae (sponges) and sediment. Chlorophytes dominated the collected samples: 38 samples in 2011 and 23 in 2012. Avrainvillea longicaulis f. laxa predominated before the bloom and Udotea flabellum after it. In total, 25 epibenthic dinoflagellate species from 11 genera were found. The genus Prorocentrum was the most representative in terms of the number of species. The highest total dinoflagellate cell abundances were observed in the sites with different types of macrophytes (up to 2441 cells/g substrate wet weight in 2011 and up to 1068 cells/g in 2012). The lowest cell densities were observed in the areas with scarce or no macrophytes on sandy seafloor. Before the bloom, Prorocentrum rhathymum (up to 4995 cells/g) and P. cf. sipadanensis (up to 5275 cells/g) were the most abundant, and after the bloom the latter was dominant (up to 3559 cells/g); in 2012, both variety of substrates and dinoflagellate cell abundance diminished. A canonical correspondence analysis revealed significant relationships between the physicochemical variables and epiphytic/benthic dinoflagellate species either before or after the bloom. The pelagic bloom resulted in the loss of substrate for epiphytic dinoflagellates, which caused replacement of the dominant species and a decrease in cell abundance of the whole taxocoenosis. © 2017 Elsevier Ltd. All rights reserved.

⁎ Corresponding author. E-mail addresses: [email protected] (A.C. Aguilar-Trujillo), [email protected] (Y.B. Okolodkov), [email protected] (J.A. Herrera-Silveira), [email protected] (F.C. Merino-Virgilio), [email protected] (C. Galicia-García).

http://dx.doi.org/10.1016/j.marpolbul.2017.02.074 0025-326X/© 2017 Elsevier Ltd. All rights reserved.

Harmful algal blooms (HABs) have been increasing globally in extension, species diversity and economic impact (Smayda, 1990; Anderson et al., 2002; Anderson et al., 2012). These HABs may cause adverse effects such as oxygen depletion, reduction in water quality, fish mortality or toxicity (Granéli and Turner, 2006).

A.C. Aguilar-Trujillo et al. / Marine Pollution Bulletin 119 (2017) 396–406

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Fig. 1. The NOAA/AOML satellite images showing the distribution of chlorophyll-a in surface waters in the Gulf of Mexico from 10 August 2011 to 16 February 2012. Note the westward movement of the patch along the northern Yucatan coast and higher chlorophyll-a concentrations in August–November.

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Fig. 3. Number of samples by type of substrate in the collections of 2011 and 2012 in the northern Yucatan Peninsula.

Fig. 2. Study area: 20 sampling sites along the northern coast of the Yucatan Peninsula, in 2011–2012.

Pelagic-benthic coupling in HAB dynamics is important. The shallowness of the coastal zone compared with deep waters of the open sea increases the possibility for benthic dinoflagellate species to contribute to pelagic HABs. Shallow benthic habitats provide adequate substrates for colonization by epiphytic dinoflagellates (Anderson et al., 2010). The Yucatan Peninsula and, in particular, the state of Yucatan show a wide range of marine and coastal ecosystems with diverse macroalgal and seagrass species. The climate of the region is characterized by three seasons associated with rainfall patterns: the dry season (March to May), the rainy season (June to October) and the northern wind season (Herrera-Silveira, 1993), which favors the development of the epiphytic/benthic dinoflagellate taxocoenosis. The HAB events in the state of Yucatan have been reported almost every year since 2001, covering an area of up to 6000 km2 (Merino-Virgilio et al., 2014). The most recent large-scale HAB event caused by

Prorocentrum minimum since February 2011 lasted 150 days. Others were reported in 2001 (10 days of duration), 2003 (15 days) and 2008 (45 days), impacting the environment and local fishermen's families, and causing marine fish, crustacean and mollusc kills (lobster and octopus, respectively). The August–December 2011 pelagic HAB event covered an area of about 150 km2 from the coastline entering the marinas from Dzilam de Bravo (Dzilam, for short) westward to San Crisanto. Although the NOAA/AOML satellite images (Fig. 1) did not allow us to distinguish this local bloom event from others, the zone with higher chlorophylla (chl-a) concentration (the first nine images taken from June 15 to November 8) tended to move westward along the northern Yucatan coast. In the Dzilam – San Crisanto area the maximum chl-a concentrations occurred on August 8 and 30, and on October 7. During this event, 28 phytoplankton (diatoms, dinoflagellates and chlorophytes) species were observed, diatoms being dominant. Among them, Chaetoceros gracilis F. Schütt (up to 3.21 × 108 cells/ l), Cylindrotheca closterium (Ehrenb.) Reimann et J.C. Lewin (1.35 × 10 8 cells/l) and Dactyliosolen fragilissimus (Bergon) Hasle (1.48

Table 1 Substrates collected in the coastal waters of the northern Yucatan Peninsula in 2011–2012 (for sampling sites see Fig. 2). Substrate type

Species

Sites 2011

Rhodophyta Rhodophyta Rhodophyta Rhodophyta Rhodophyta Rhodophyta Phaeophyceae Phaeophyceae Phaeophyceae Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Chlorophyta Angiospermae Angiospermae Angiospermae Demospongiae Sediment

Acanthophora sp. Bryothamnion sp. Gracilaria sp. Halymenia floresia (Clemente) C. Agardh Heterosiphonia gibbesii (Harvey) Falkenberg Laurencia (?) Dictyota dichotoma (Hudson) J. V. Lamour. Padina gymnospora (Kütz.) Sonder Sargassum pteropleuron Grunow Acetabularia crenulata J. V. Lamour. Avrainvillea longicaulis (Kütz.) G. Murray et Boodle f. laxa D. S. Littler et M. M. Littler Caulerpa ashmeadii Harvey Caulerpa paspaloides var. laxa Weber-van Bosse Caulerpa prolifera (Forsskål) J. V. Lamour. Caulerpa sertularioides (J. F. Gmelin) Howe Codium sp. Halimeda incrassata (Ellis et Solander) J. V. Lamour. Penicillus capitatus Lamarck Penicillus dumetosus (J. V. Lamour.) Blainville Udotea flabellum (J. Ellis et Solander) J. V. Lamour. Udotea spinulosa Howe Halodule wrightii Ascherson Syringodium filiforme Kütz Thalassia testudinum Banks ex König Sponge (unidentified species) –

10, 12 1, 10, 12, 14 1, 5, 6, 9 12 1, 11 3 9 5, 6, 7, 8, 10 6, 7 9 10 3, 5, 6, 9, 10, 13 9 5, 6, 8–10, 13 5, 8–13 5 3, 5, 9–12, 14 6–12 6, 8–12 5 1–20

2012 2, 4, 14, 15 2, 10, 13, 16 11 13 4, 5, 13 4, 6, 11, 13, 17 10

5, 6, 7 6, 7, 8, 10, 18 6 8, 10 13, 18 5, 6, 10 8 1, 5, 7, 9, 10 5, 11, 13 5, 6, 8, 11 10, 12, 13 6 1–20


399

Fig. 4. Physicochemical parameters recorded in the coastal waters of the northern Yucatan Peninsula in August 2011 and September 2012. The line within the box is the mean; the top and the bottom of the box are 25% and 75% (quartiles); whiskers are 5% and 95%.

× 106 cells/l) were the most abundant. Of dinoflagellates, Scrippsiella trochoidea (F. Stein) A.R. Loebl. reached the maximum abundance (1.27 × 10 6 cells/l). Unidentified chlorophytes reached an abundance of 2.32 × 108 cells/l. Apart from a negative impact on local economy and losses of pelagic fish and invertebrate species (fishes: Epinephelus morio, Mycteroperca bonaci, Ocyurus chrysurus, Lutjanus synagris, Lachnolaimus maximus, and invertebrates: Octopus maya and Isostichopus badionotus), the prolonged duration of this event resulted in degradation, loss and changes in species composition of submerged aquatic vegetation (SAV) as well as accumulation of organic matter on the sea bottom, which, in turn, made the epiphytic dinoflagellates unable to adhere to the substrate (Merino-Virgilio et al., 2014). To identify the epiphytic/benthic dinoflagellates inhabiting different types of substrate and to determine their temporal-spatial occurrence and abundance before and after the 2011 HAB event in the northern Yucatan Peninsula were the main objectives of the present study. The study area is characterized by the predominance of limestone karstic soils of high permeability where sedimentary rocks of the geological formations of limestone are typical (INEGI, 1986). Sandy soil of beaches is classified as regosol-calcareous, with N 90% calcium carbonate (Espejel, 1984). The northern Yucatan Peninsula has no river runoff and comprises a wide carbonated continental shelf extending up to 100 miles from the coastline (Merino-Ibarra, 1992).

Sampling was performed in August 2011 before the pelagic HAB event and in September 2012 after it to determine the pelagic HAB effect on the taxocoenosis of the epibenthic dinoflagellates in the northern Yucatan coastal waters. Twenty transects perpendicular to the coastline, starting from 20 sampling sites from El Cuyo in the east to Celestún in the west, at a distance of 50 m, 150 m and 250 m from the coast, were sampled (Fig. 2). This sampling was a part of a yearly survey along the northern coast of Yucatan usually performed in late summer–early autumn. A total of 168 macrophyte (seaweeds and seagrasses), sponge and sediment samples (105 in 2011 and 63 in 2012) that included associated microphytobenthos were taken by snorkeling from 0.7 to 5 m depth. Macrophytes were collected manually from sandy substrate or cut with a knife and placed in a plastic 500 ml bottle together with seawater from the sampling site, one species per bottle. As many different substrates (macrophyte species) as possible were collected at each site. Depending on the macrophyte coverage, an area of several square decimeters to several square meters was sampled. Some sampling sites (mainly in the western part of the study area) were lacking in SAV, so only sediment was sampled. Bottom sediment was collected from a 5 cm surface layer directly with a plastic bottle. The samples were fixed on the boat with formalin to a final concentration of 4%. The samples were analyzed in the laboratory following previously used techniques (Okolodkov et al., 2007). An Olympus

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Table 2 Epibenthic dinoflagellates in the coastal waters of the northern Yucatan Peninsula in 2011 and 2012 (toxicity data are taken from literature). Species

Code

Amphidinium sp. Amphidinium cf. carterae Hulburt

Ampsp Not toxic? Ampcar Produces hemolysins and ichthyotoxins Byscap Not toxic

Bysmatrum caponii (Horiguchi et Pienaar) Faust et Steindinger Cabra cf. aremorica Chromérat, Couté et Nézan Cabra cf. matta Shauna Murray et D.J. Patterson Coolia sp. Durinskia capensis Pienaar, Sakai et Horiguchi Gambierdiscus caribaeus Vandersea, Litaker, Faust, Kibler, Holland et Tester Ostreopsis heptagona Norris, Bomber et Balech Plagiodinium belizeanum Faust et Balech Prorocentrum cf. belizeanum Faust Prorocentrum cf. concavum Fukuyo Prorocentrum cf. foraminosum Faust Prorocentrum hoffmannianum Faust Prorocentrum lima (Ehrenb.) Dodge

Prorocentrum rhathymum Loeblich III, Sherley et Schmidt Prorocentrum sculptile Faust Prorocentrum cf. sipadanensis Mohammad-Noor, Daugbjerg et Moestrup Prorocentrum sp. Sinophysis ebriola (Herdman) Balech Sinophysis microcephala Nie et Wang Sinophysis sp. Sinophysis stenosoma Hoppenrath (?)Togula sp. Flø Jørgensen, S. Murray et Daugbjerg Unidentified species

Cabare

Toxicity

Not toxic

Cabmat Not toxic Coosp Durcap

Produces cooliatoxin (ichthyotoxic) Not toxic

Gamcar Produces ciguatoxins, causes CFP

Osthep

Toxic to mice

Plabel

Not toxic

Probel Procon Profor Prohof Prolim

Prorha

Not toxic Produces OA, causes DSP Not toxic? Produces OA and FAT Produces OA, DTX1, DTX2, prorocentrolides and FAT; causes CFP and DSP Toxic?

Proscu Prosip

Not toxic Not toxic?

Prosp Sinebr

Some species produce OA and prorocentrolides, causes DSP Not toxic

Sinmic

Not toxic

Sinsp Sinste Togsp

Not toxic Not toxic Not toxic

Dinsp1

CFP: ciguatera shellfish poisoning; DSP: diarrheic shellfish poisoning; DTX1: dinophysistoxin-1; DTX2: dinophysistoxin-2; FAT: fast-acting toxins; OA: okadaic acid.

CKX41 inverted microscope equipped with the phase-contrast objectives 10 ×/0.25, 20 ×/0.40 and 40 ×/0.55 was used for preliminary species identification and counting. The results were expressed as the number of cells per gram (cells/g) of substrate wet weight (SWW). A JEOL JSM-7600f Field Emission scanning electron microscope (SEM) was used at 5 kV to study the thecal morphology of dinoflagellate species in some samples. Nutrient concentrations (ammonium, nitrates, phosphates, silicates and urea) were determined following spectrophotometric techniques (Strickland and Parsons, 1972). Chl-a was determined by extraction of pigments using a 90% acetone solution followed by spectrophotometric determination and recalculation formula (Jeffrey and Humphrey, 1975; Parsons et al., 1984). Based on the information on dinoflagellate species composition and their cell abundances, ecological descriptors such as species richness and abundance distribution were applied to the whole taxocoenosis (Magurran, 1988). For the purpose of observing variation of hydrochemical characteristics before and after the 2011 HAB event, graphics (box diagrams) were analyzed using the R program. In addition, a canonical correspondence analysis (CCA) was used to reveal relationships between species of epiphytic

dinoflagellates and environmental parameters. All the data were log10 (data + 1) transformed prior to analysis. Canoco for Windows 4.5 was used for this analysis. CCA was run with Montecarlo tests of the first, and all canonical axes were performed using 1000 permutations under a reduced model to maintain type I error in small data sets (Braak and Šmilauer, 2002). Six substrate types were distinguished: Chlorophyta (green algae), Phaeophyceae (brown algae), Rhodophyta (red algae), Angiospermae (seagrasses), Demospongiae (sponges) and sediment. In total, 24 macrophyte species were identified (Table 1). Chlorophytes dominated the collected samples: 38 samples in 2011 and 23 in 2012 (Fig. 3). In the study area, Avrainvillea longicaulis f. laxa predominated before the HAB event and Udotea flabellum after it. Most hydrochemical variables did not exhibit significant differences (P = 0.05), showing, in general, higher mean values after the HAB event (Fig. 4). Salinity was the most stable characteristic, with mean values of 36.25 and 36.42 in 2011 and 2012, respectively. Phosphates were the only parameter that exhibited a wide range, showing higher values before the bloom (0.03–0.54 μM/l). In 2011 the ranges of physicochemical characteristics were as follows: water temperature 24.4 °C (Chuburná) to 37.2 °C (Las Coloradas), salinity 32.65 (Dzilam) to 36.77 (Chabihau), dissolved oxygen (DO) 1.01 mg/l (Sisal) to 9.6 mg/l (Punta Bass), nitrates 0.44 μm/l (Xixim) to 16.22 μm/l (Dzilam), ammonium 0.052 μm/l (Chabihau) to 30.73 μm/l (Punta Bass), phosphates 0.03 μm/l (Celestún) to 0.83 μm/l (Bocas 1), silicates 0.76 μm/l (Progreso) to 14.07 μm/l (Punta Bachul), urea 0.04 μm/l (Rio Lagartos) to 6.07 (Telchac), and chl-a 0.47 (Punta Bass) to 12.76 mg/m3 (Bocas 2). In 2012 the following ranges of the same variables were observed: temperature 28.8 °C (Chabihau) to 32.4 °C (Bocas 2), salinity 34.95 (Dzilam) to 36.95 (Punta Bachul), DO 4.27 mg/l (Chabihau) to 7.49 mg/l (San Felipe), nitrates 0.02 μm/l (San Felipe) to 21.59 (Sisal) μm/l, ammonium 0.1 μm/l (Río Lagartos) to 3.15 μm/l (EL Cuyo), phosphates 0.03 μm/l (Celestún) to 0.21 μm/l (Celestún), silicates 1.63 μm/l (El Cuyo) to 61.35 μm/l (El Cuyo), urea 0.04 μm/l (Palmar) to 6.16 (Río Lagartos), and chl-a 0.703 mg/m3 (Chabihau) to 8.95 mg/m3 (16 km Cuyo). In total, 25 epiphytic dinoflagellate species from 11 genera were found (Table 2, Figs. 5–7). The genus Prorocentrum was the most representative in terms of the number of species (P. cf. belizeanum, P. cf. concavum, P. cf. foraminosum, P. hoffmannianum, P. lima, P. rhathymum, P. sculptile, P. cf. sipadanensis and other Prorocentrum spp.). Before the HAB event (in 2011), 24 species were observed, and Prorocentrum rhathymum (up to 4995 cells/g SWW) and P. cf. sipadanensis (up to 5275 cells/g) were the most abundant (Fig. 8A). After the bloom (in 2012), both variety of substrates and dinoflagellate cell abundance diminished, P. cf. sipadanensis being the dominant (up to 3559 cells/g) of 23 observed species (Fig. 8B). The identification of some species was preliminary due to the absence of data on the morphology of the periflagellar area in the Prorocentrum species. Spatial variation of the total dinoflagellate cell abundance varied between 1 and 2441 cells/g before the bloom and from 3 to 1068 cells/g after it. Before the HAB event, the lowest cell density was observed at El Palmar due to Sinophysis stenosoma, while the highest abundance was found at Dzilam due to Prorocentrum rhathymum (Fig. 9A). After the bloom, the cell abundance also varied from site to site, with the lowest value observed at Xixim due to Amphidinium sp. and the highest value at San Felipe due to Plagiodinium belizeanum (Fig. 9B). The predominant species remained the same in 2012 compared to those in 2011: Prorocentrum hoffmannianum, P. concavum, P. cf. sipadanensis, P. rhathymum and (?)Togula sp. (Fig. 8). Their abundances were at the same level. In addition, Plagiodinium belizeanum showed higher abundance in 2012. None of the species showed an average cell abundance of N500 cells/g. However, the total cell abundances per locality were noticeably lower in 2012, in particular,


401

Fig. 5. Epibenthic dinoflagellates of Yucatan: A–B – Cabra cf. matta: A – right-side view; B – anterior end of the cell; C – Durinskia capensis, ventral view; D – Coolia sp., apical view; E–F – Gambierdiscus caribaeus: I – complete theca in apical view; F – sulcul area in antapical view. Scale bar: 10 μm (A, C and E), 1 μm (B, D and F).

between Uaymitún and San Felipe and at El Cuyo (Fig. 9). In the zone between San Felipe and El Cuyo in the eastern part of the sampling area and from Uaymitún westward, the difference in abundance is not clearly seen or is negligible. CCA showed relationships between various species of epiphytic dinoflagellates and environmental parameters (Montecarlo test: first canonical axis F-ratio = 4.98, P = 0.027; all canonical axes F-ratio = 2.26, P = 0.001) (Fig. 10). The most abundant P. rhathymum and P.cf. sipadanensis were related to low nutrient concentrations. In addition to the negative impact on the local economy and to pelagic fish mortalities, the prolonged HAB event resulted in degradation, loss and changes in composition of the SAV as well as accumulation of the organic matter on the sea bottom, which in turn resulted in the loss of substrate for epiphytic dinoflagellates. SAV communities are not static and are affected by cascade effects. After events such as the northerly winds, hurricanes or HABs, both water column and solid substrate characteristics change; some specimens of vegetation are removed and others get buried (Herrera-Silveira et al., 2010).

The number of macrophyte species (Table 1) and the dominance of the Chlorophyta in terms of both species richness and abundance during the present study are in accordance with Herrera-Silveira et al. (2010) who mention the species of Penicillus, Caulerpa, Halimeda, Acetabularia and Udotea as the most common macroalgae along the coast of Yucatan. Eutrophication causes the major impact in the coastal waters of the state of Yucatan (Herrera-Silveira et al., 2004; Aranda-Cirerol et al., 2006). In general, loss of the water quality and biological communities and massive development of toxic microorganisms are some of the consequences of this phenomenon (Epstein, 1995). Physicochemical characteristics measured before and after the bloom were within the ranges previously reported in the study area (Herrera-Silveira et al., 2004). They did not show any significant differences between 2011 and 2012 (P = 0.05), but the mean values registered before the bloom were slightly lower in general (Fig. 4). Both temperature and salinity showed a seasonal variation: the highest temperature and the lowest salinity values were observed

402


Fig. 6. Epibenthic dinoflagellates of Yucatan: A–B, Ostreopsis heptagona: A – apical view; B – antapical view; C-D – Plagiodinium belizeanum: C – complete theca, right-side view; D – epitheca; E – Sinophysis stenosoma, left-side view; F – Sinophysis microcephala, left-side view. Scale bar: 10 μm (A, B, E and F), 1 μm (C and D).

in summer (the rainy season). In contrast, winter in the northern Yucatan is characterized by low precipitation and temperature and higher salinity and wind speed (Delgado et al., 2010). Some large oceanic, coastal and estuarine zones are nitrogen-limited (Justic et al., 1995; Paerl, 1997; Philippart et al., 2000). A decrease in Si:P ratio is accompanied by an increase in microalgal proliferation, and diatoms as the dominant group in terms of phytoplankton biomass are replaced by small-sized flagellates (Smayda, 1990). In some cases, HAB events develop (Páez-Osuna et al., 1998), as happened in 2011 in the northern Yucatan. In this area, Morales-Ojeda et al. (2010) distinguish four hydrochemical zones: zone I (Celestún - Punta Bass y San Felipe - Dzilam) is characterized by high salinity and low nutrient concentrations; zone II (Sisal, Telchac - Progreso) by low DO, high salinity and nitrate and silicate concentrations; zone III (Dzilam - Bocas) by low salinity and high nutrient concentrations, which favor the development of HABs; and zone IV (Río Lagartos - El Cuyo) by high salinity and low nitrate and chl-a concentrations.

On the whole, the dinoflagellate species composition was typical in terms of the prevalence of Prorocentrum spp. in both species richness and cell abundance. Numerous Prorocentrum spp. inhabit shallow tropical and subtropical waters and lagoons of the Greater Caribbean and adjacent areas (Carlson and Tindall, 1985; Mitchell, 1985; Faust, 1993a, 1993b, 1996, 2004; Tindall and Morton, 1998; Faust et al., 1999; Turquet et al., 2001; Delgado et al., 2002; Faust et al., 2005; Delgado et al., 2006; Okolodkov et al., 2007, 2014; Almazán-Becerril et al., 2012, 2015; Aguilar-Trujillo et al., 2014). Prorocentrum belizeanum is a pantropical species (Faust and Gulledge, 2002) reported from the Caribbean Sea and the northern coast of Cuba (Dickey et al., 1990; Faust, 1993a; Delgado et al., 2002; Almazán-Becerril et al., 2012, 2015), the Pacific (Okolodkov and Gárate-Lizárraga, 2006; Parsons and Preskitt, 2007) and the Indian Ocean (Turquet et al., 2001), and it is generally associated with floating detritus (Faust, 1993a). Prorocentrum concavum is typical of mangroves and tropical neritic waters (Faust, 1990; Steindinger and Tangen, 1996; Almazán-Becerril et al., 2012, 2015). Prorocentrum foraminosum is reported for Belize and Malaysia (Faust, 1993b; Faust et


403

Fig. 7. Epibenthic dinoflagellates of the genus Prorocentrum from Yucatan: A – Prorocentrum foraminosum; B – Prorocentrum sp.; C – P. hoffmannianum; D – P. lima; E – P. rhathymum; F – P. sculptile. Scale bar: 10 μm (A–C, E and F), 1 μm (D).

al., 1999; Mohammad-Noor et al., 2007). Prorocentrum hoffmannianum was originally described from the mangroves in Belize (Faust, 1990, 1993a), and it is considered common in the Caribbean (Faust and Gulledge, 2002; Almazán-Becerril et al., 2012, 2015). Prorocentrum lima is a widely distributed species inhabiting both temperate and tropical waters (Faust and Gulledge, 2002; Heredia-Tapia et al., 2010; Taylor et al., 2003; Foden et al., 2005; Okolodkov, 2005; Maranda et al., 2007; Okolodkov et al., 2007, 2014; Parsons and Preskitt, 2007). Prorocentrum rhathymum is common in tropical and subtropical waters of both the Atlantic and Pacific (Faust and Gulledge, 2002; Levasseur et al., 2003; Aligizaki and Nikolaidis, 2006; Okolodkov et al., 2007, 2014; Almazán-Becerril et al., 2012, 2015; Mohammad-Noor et al., 2016). Prorocentrum sculptile was originally reported from Central America (Faust, 1994), and it can be easily confused with P. emarginatum Fukuyo; the latter was reported for the Mexican Caribbean coast (Almazán-Becerril et al., 2012, 2015). Prorocentrum sipadanensis was originally described from Malaysia as an inhabitant of seagrasses (Mohammad-Noor et al., 2007). Thus, the

geographic distribution of most Prorocentrum spp. found in the present study is limited to the tropical zone. The three potentially toxic species from other genera, Gambierdiscus caribaeus, Ostreopsis heptagona and Amphidinium cf. carterae (Table 2), found in this study have been recently also observed in the Mexican Caribbean (Almazán-Becerril et al., 2012, 2015, 2016a, 2016b). Previous studies have shown that availability of macrophytes as substrate affect the distribution of epiphytic dinoflagellates, while precipitation, temperature and nutrients are only temporarily important (Carlson and Tindall, 1985; Tindall and Morton, 1998). Increase in abundance of adherent cells may result from the colonization of a substrate by free-living cells or from the growth in situ of the cells adhering to the substrate, whereas decrease in cell abundance may result from the mortality of the adhering cells or from the loss of the substrate (Levasseur et al., 2003), as occurred in 2012 when a considerable loss of macrophytes occurred, presumably due to the intense bloom.

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Fig. 8. Average cell abundances per epibenthic dinoflagellate species with standard error bars in coastal waters of the northern Yucatan Peninsula before the HAB event (above) and after it (below), in 2011 (A) and 2012 (B). Cells g−1 SWW = cells per gram of a substrate wet weight. For abbreviations of species see Table 2. The right vertical axis corresponds to the light gray bars. Note the difference in scale between 2011 and 2012.

During both surveys, in 2001 and 2012, the highest dinoflagellate cell abundances were observed at the sites with different types of macrophytes. The lowest cell densities were found in the areas with scarce or no macrophytes on sandy sea floor. The data on the abundance of epiphytic dinoflagellates obtained are in accordance with Morales-Ojeda et al. (2010) who mention that the western part of the northern Yucatan coast (from Chabihau to Celestún) shows a lesser coverage by SAV, probably, due to bottom trawling, port urban and tourist activities, coupled with the low water quality. The eastern part (from Dzilam to El Cuyo) is characterized by high SAV coverage combined with low-intensity water currents and high nutrient input due to numerous groundwater discharges that favor HAB development. Of the dominant species, P. rhathymum is associated with low nutrient concentrations (Okolodkov et al., 2014), indicating that reduced cell abundances of this species may be related to eutrophication of the coastal zone caused by the HAB event (Merino-Virgilio et al., 2014), which confirms results obtained in this study. Therefore, P. rhathymum can be considered an indicator of waters not eutrophized in the southern Gulf of Mexico. It can be replaced by harmless or even more toxic dinoflagellates than P. rhathymum. As is known, it produces hemolytic substances not toxic to mice (Nakajima et al., 1981), but a water soluble acetone precipitate is toxic to them (Carlson and Tindall, 1985). Haemolysis assays and intraperitoneal mouse bioassays revealed fast acting toxins with mice dying in b20 min (Pearce et al., 2005). In addition, some P. rhathymum strains, including those of Florida waters, have been linked to the production of okadaic acid (An et al., 2010; Caillaud et al., 2010).

Both natural and anthropogenic factors intervene in the growth of epiphytic dinoflagellates and their hosts, macroalgae and seagrasses. In turn, macrophyte development can be controlled by invertebrates and fishes, sea turtles, types of sea bottom, water currents, waves, sediment load, algal blooms, and meteorological factors such as cold fronts and hurricanes. The HAB event of 2011 resulted in the loss of substrate for epiphytic dinoflagellates, which caused replacement of the dominant species and decrease in cell abundance of the whole taxocoenosis. Acknowledgments We are thankful to Manuel A. González-Salas (Dzilam) and Iliana Osorio-Moreno (CINVESTAV-IPN, Mérida) for field logistics and chemical analyses, Dora A. Quintanilla-Huerta and Ana R. Cristóbal-Ramos (CINVESTAV-IPN, Mérida) for technical support with the SEM, Marcia M. Gowing (University of California at Santa Cruz, California, USA) for improving the writing style, to Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico, for giving a stipend to ACAT, to Gobierno del Estado de Yucatán for financial support to the FOMIX CONACYTYucatán project “Análisis de las causas, dispersión y consecuencias ambientales de la marea roja en Yucatán” (No. 108897; 2009–2012) given to JAHS, the FOMIX CONACYT-Yucatán (No. 108160) and CONACYT LAB-2009-01 (No. 123913) projects of the Laboratorio Nacional de Nano y Biomateriales (CINVESTAV-IPN, Mérida) given to Patricia Quintana-Owen.


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Fig. 9. Cell abundances averaged per site (including all species) of epibenthic dinoflagellates in coastal waters of the northern Yucatan Peninsula: before the HAB event (above) and after it (below), in 2011 (A) and 2012 (B). Cells g−1 SWW = cells per gram of substrate wet weight. The right vertical axis corresponds to the light gray bars. Note the difference in scale between 2011 and 2012.

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