Environmental Forcing on the Flux of Organic-Walled Dinoflagellate Cysts

Science of the Total Environment 621 (2018) 548–557

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Science of the Total Environment

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Environmental forcing on the ﬂux of organic-walled dinoﬂagellate cysts in recent sediments from a subtropical lagoon in the Gulf of California

Tomasa Cuellar-Martinez a, Rosalba Alonso-Rodríguez b,⁎, Ana Carolina Ruiz-Fernández b, Anne de Vernal c, Lourdes Morquecho d, Audrey Limoges e,MaryseHenryc, Joan-Albert Sanchez-Cabeza f a Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Av. Ciudad Universitaria 3000, C.P. 04510, Coyoacán, Ciudad de México, Mexico b Unidad Académica Mazatlán, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, 82040 Mazatlán, Sinaloa, Mexico c Geotop, Université du Québec à Montréal, CP 8888, succ. Centre-ville, Montréal, Québec H3C 3P8, Canada d Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Av. I.P.N. 195, Col. Playa Palo de Santa Rita Sur, La Paz, Baja California Sur. 23096, Mexico e University of New Brunswick, Department of Earth Sciences, 2 Bailey Drive, Fredericton, New Brunswick E3B 5A3, Canada f Unidad Académica Procesos Oceánicos y Costeros, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Ciudad de México 04510, Mexico

HIGHLIGHTS GRAPHICAL ABSTRACT

• A 210Pb-dated sediment core used to reconstruct dinocyst fluxes in San José Is- land • Dinocyst fluxes were evaluated vs. rain, temperature, ENSO and terrigenous input. • Cyst of Pyrodinium bahamense atoxic dinoflagellate increased over ca. 50 years ago • Dinocyst fluxes responded to terrigenous input and minimum atmospheric temperature.

article info abstract

Article history: To evaluate the relationship of changes in organic-walled dinoflagellate cyst (dinocyst) fluxes to sediments with Received 20 July 2017 environmental variables (air and sea surface temperatures, El Niño conditions, rainfall, and terrigenous index), Received in revised form 23 November 2017 cyst assemblages were analyzed in a 210Pb-dated sediment core (~100 years) from the pristine San José Lagoon Accepted 24 November 2017 − (San José Island, SW Gulf of California). The dinocyst abundance ranged from 3784 to 25,108 cysts g 1 and fluxes Available online 29 November 2017 were of the order of 103–104 cysts cm−2 yr−1. Lingulodinium machaerophorum, Polysphaeridium zoharyi and Editor: Daniel Wunderlin Spiniferites taxa accounted for 96% of the total dinocyst assemblages, and the abundances of these species increased towards the core surface. P. zoharyi fluxes increased from about 1965 onwards. Redundancy analyses, Keywords: showed that mean minimum air temperature and terrigenous index were the key factors governing dinocyst Sediment fluxes. In this study, dinocyst fluxes of dominant taxa had responded to changes in climate-dependent environ- Dinocyst mental variables during the past ~20 years; this may also be the case in other subtropical coastal lagoons. San José Island © 2017 Elsevier B.V. All rights reserved. Polysphaeridium zoharyi Lingulodinium machaerophorum Climatic variability

1. Introduction

ﬂ ⁎ Corresponding author. Dino agellates are eukaryotic microorganisms with complex life cy- E-mail address: [email protected] (R. Alonso-Rodríguez). cles and diverse ecological roles. They are important contributors to

https://doi.org/10.1016/j.scitotenv.2017.11.269 0048-9697/© 2017 Elsevier B.V. All rights reserved. T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557 549 marine primary production (Bravo and Figueroa, 2014), although most A dated sediment core spanning about 100 years, collected in a pris- dinoflagellate species are mixotrophic, which is the combination of tine coastal lagoon on an island in the southwestern Gulf of California, phototrophy and phagotrophy as a nutritional strategy (Jeong et al., was used to reconstruct temporal changes in dinocyst assemblages, 2010). Approximately, 100 dinoflagellate species are known to form with the purpose to evaluate the influence of environmental variables harmful algal blooms (Moestrup et al., 2009), some of them producing on the variations in dinocyst assemblages and fluxes, with a special toxins that affect to marine organisms and humans (Van Dolah, 2000). focus on potentially harmful species. About 200 dinoflagellate species produce resting cysts (hereafter dinocysts) during their life cycle (Head, 1996; Matsuoka and Head, 2. Regional setting 2013); these are deposited in the sediments and serve as a source of seeds to initiate blooms (Usup et al., 2012 and references therein); San José Lagoon (SJL) is a small and shallow coastal lagoon (2.7 km they can provide historical evidence of blooms (Matsuoka, 1999). The length, 5 to 10 m depth; Fig. 1) in the southern part of San José Island organic-walled dinoflagellates are preserved in the sediments owing (24°52′-25°06′ N; 110°43′-110°35′ W). This is the third largest island to the presence of dinosporin in the cyst wall. in the Gulf of California (Lawlor et al., 2002), and is inhabited by a Dinocysts have been used as indicators of oceanographic variables small local community (~70 residents; Espinosa-Gayosso and Alvarez- [productivity, sea ice cover, salinity, temperature (e.g., de Vernal and Castañeda, 2006) and its surrounding waters support a carbonate-rich Marret, 2007; Durantou et al., 2012; Cormier et al., 2016)], and of an- biota with abundant coralline red algae, molluscs and hermatypic corals thropogenic pollution and eutrophication (Dale, 2001; Pospelova et al., (Halfar et al., 2004; Hetzinger et al., 2006). 2002), and to reconstruct past climatic conditions (e.g., Rochon et al., San José Island is the largest insular mangrove ecosystem in the Gulf 1999; de Vernal et al., 2001; Candel et al., 2017). of California (~1.09 km2: Bourillón-Moreno et al., 1988; In the Gulf of California, the main species of cyst-forming dinoflagel- González-Zamorano et al., 2012). The connection of SJL to the sea lates that produce algal blooms are Gymnodinium catenatum, (Fig. 1) mainly occurs through a 1.5 km-long channel in the north- Pyrodinium bahamense and Lingulodinium polyedra (Páez-Osuna et al., northwest, and an intermittent outlet in the southwest (Morquecho 2016 and references therein). There is no information available about et al., 2012). The climate is warm and dry, with mean annual tempera- dinocyst records in sediment cores from the coastal lagoons, since the ture from 13.7 °C to 31.0 °C (Ruiz et al., 2006), and mean annual rainfall dinocyst studies have focused on surface sediment samples from 125 mm to 400 mm (UNAM, 1990). The lagoon has been a natural (Martínez-Hernández and Hernández-Campos, 1991; Morquecho and protected area since 1978 (SG, 1978), and it is considered to still remain Lechuga-Devéze, 2003; Limoges et al., 2010) and Quaternary sediment as a pristine environment (Cuellar-Martinez et al., 2017). cores from deep basins (Flores-Trujillo et al., 2009; Price et al., 2013; Price and Pospelova, 2014). 3. Materials and methods Variations in the cyst abundance of the above mentioned species in recent sediments, have been related to climatic variables such as rainfall, sea 3.1. Sampling surface temperature, and El Niño-Southern Oscillation (Flores-Trujillo et al., 2009; Sanchez-Cabeza et al., 2012), as well as to anthropogenic in- One sediment core (SJ core, 42 cm long, 7 cm inner diameter) was fluences (Peña-Manjarrez et al., 2001; Vásquez-Bedoya et al., 2008). collected by scuba diving with an acrylic tube in February 2015, in the

Fig. 1. Study area: a) location of San José Island in SW Gulf of California (arrow); b) location of the lagoon at the southern end of the island (arrow); c) collection site of sediment core (●); main (1) and intermittent (2) lagoon mouth; the dark gray shading indicates area covered by mangrove forests. 550 T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557 inner zone of the lagoon (24°52′29.7″ N, 110°33′3.3″ W) at 8 m depth at 1000× magnification. On average, 346 (range: 281–437) dinocysts per low tide (Fig. 1). The sediment was extruded and sliced at 1 cm inter- sample were counted. One specimen of P. zoharyi was isolated onto a vals. Samples were freeze-dried at −50 °C and 0.11 mbar for 72 h, glass slide, subsequently air-dried, and observed with a Hitachi S- and stored in plastic bags until analysis. 3400N scanning electron microscope (SEM). Cysts were identified following Rochon et al. (1999), Radi et al. (2013), Zonneveld and 3.2. Core dating Pospelova (2015) and Limoges et al. (accepted). Some specimens were unidentifiable to the species level, owing to Core chronology and mass accumulation rates (MAR, g cm−2 yr−1) either i) the cyst orientation on the glass slide, which prevented the ob- for the SJ core were calculated by 210Pb dating. 210Pb was analyzed servation of critical taxonomic features, or ii) the over-abundance of de- through its descendant 210Po by alpha spectrometry (Ortec-Ametek bris adhered to the cyst wall or processes. In such cases, specimens were 576A Dual Alpha Spectrometer) following the method described by pooled according to their morphological and morphometric characteris- Ruiz-Fernández and Hillaire-Marcel (2009). Analyses were conducted tics into Spiniferites spp. or Echinidinium spp. The abundance of by the first author between May and October 2015 at Laboratorio de dinocysts is reported as the number of cysts per gram (cyst g−1) dry Geoquímica Isotópica y Geocronología (Unidad Académica Mazatlán, weight. Abundance uncertainty was calculated according to Stockmarr Universidad Nacional Autónoma de México). The sediment chronology (1971). The equivalent vegetative stages were based on Head (1996) was obtained through the Constant Flux model (Sanchez-Cabeza and (Table 1). Dinocyst fluxes were quantified by multiplying the 210Pb- Ruiz-Fernández, 2012) and uncertainties were computed by Monte derived MAR (g cm−2 yr−1) by the dinocyst concentration (cysts g−1) Carlo simulation with 30,000 iterations (Sanchez-Cabeza et al., 2014). (Pospelova et al., 2002). To corroborate 210Pb dating, 239 + 240Pu was analyzed following the method described by Ruiz-Fernández et al. (2014) and references there- 3.4. Geochemical analysis in. The 210Pb-derived chronology of the SJ core is described in further detail in Cuellar-Martinez et al. (2017); the results are summarized in The concentrations of terrigenous element indicators (Al, Fe, Mn) Fig. 2. were determined with an X-ray fluorescence system (Spectro™ Xepos) (results published in Cuellar-Martinez et al., 2017). These ele- 3.3. Palynological analysis ment indicators were used to calculate the terrigenous index [Iterr = Al / (Al + Fe + Mn)], which reflects the relative contribution of conti- Palynological analyses were performed at GEOTOP-UQAM, followed nental versus oceanic detritus (Böstrom et al., 1973). Carbon and nitro- the procedure described by de Vernal et al. (2010).Briefly, one tablet of gen concentrations were determined with an elemental analyzer at the Lycopodium clavatum spores (Batch 177745) with a known number of Laboratorio de Paleoecología, Paleoclimatología y Cambio Climático, spores was added to approximately 4 g of dry sediment. The sediment Instituto de Ciencias de la Tierra, Instituto de Geofísica-UNAM. To ana- was sieved through a 106 μm mesh metal sieve and a 10 μm mesh lyze δ13C, inorganic carbon was removed by overnight washing with nylon sieve. The fraction retained in the 10 μm mesh was successively 1 N HCl. Afterwards, samples were rinsed with deionized water and treated at room temperature with hydrochloric (10% HCl) and hydrofluoric (49% HF) acids to eliminate carbonate and silicate particles, Table 1 respectively. The residue was rinsed with distilled water. A second siev- Dinoflagellate cyst species in the SJ core (San José Island, SW Gulf of California). ing, again through 106 μmand10μm mesh sieves was performed to further clean the residue from crystals and organic remains. Finally, the Cyst species Dinoflagellate motile/vegetative stage (Paleontological name) (Biological name) residue was mixed with glycerin jelly (Kaiser, 1880) to prepare perma- nent slides. Phototrophic species The identification and counting of dinocysts was performed with a Spiniferites belerius Gonyaulax scrippsae Spiniferites bentorii Gonyaulax digitalis light microscope (LM, Leica DMR, Wetzlar, Germany) at 400× to Spiniferites delicatus Gonyaulax sp. Spiniferites hainanensis Gonyaulax sp. Spiniferites hyperacanthus Gonyaulax spinifera 210 -1 -2 -1 Pb (Bq kg ) MAR (g cm yr ) Spiniferites mirabilis Gonyaulax spinifera 515250.1 0.3 0.5 0.7 0.9 Spiniferites ramosus Gonyaulax spinifera Spiniferites spp. Gonyaulax spinifera group 0 2015 cf. Achomosphera Gonyaulax spinifera Cyst of Gymnodinium catenatum Gymnodinium catenatuma 5 a b 2005 Impagidinium aculeatum Gonyaulax sp. 10 1992 Lingulodinium machaerophorum Lingulodinium polyedra Nematosphaeropsis rigida Gonyaulax spp. 15 1971 Operculodinium centrocarpum Protoceratium reticulatuma Operculodinium israelianum ? Protoceratium reticulatuma 20 1934 Cyst of Pentapharsodinium dalei Pentapharsodinium dalei

> 97 years 97 > Cyst of Polykrikos kofoidii Polykrikos kofoidii 25 Polysphaeridium zoharyi Pyrodinium bahamensea

Depth (cm) 30 Heterotrophic species 35 Echinidinium aculeatum Indet. Pb210Pb Echinidinium delicatum Indet. Echinidinium granulatum Indet. 40 Pu239+240 Pu Echinidinium spp. Indet. 45 Echinidinium transparantum Indet. 15 65 115 Cyst of Protoperidinium sp. Protoperidinium sp. Quinquecuspis concreta Protoperidinium leonis 239+240Pu (mBq kg-1) Selenopemphix quanta Protoperidinium conicum Stelladinium stellatum Protoperidinium compressum Tectatodinium pellitum Gonyaulax spiniferaa Fig. 2. 210Pb-derived chronology of the SJ core (San José Island, SW Gulf of California): Tuberculodinium vancampoae Pyrophacus steinii a) depth profiles of 210Pb and 239 + 240Pu activities, and b) mass accumulation rates Votadinium spinosum Protoperidinium claudicans (MAR). Horizontal dashed line: year 1918 ± 9, oldest 210Pb-derived age. Data source: Cuellar-Martinez et al. (2017). a Potentially harmful dinoflagellates according to Moestrup et al. (2009). T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557 551 freeze-dried at −50 °C and 0.11 mbar for 72 h several times until acid- (2013–2011) (Fig. 5a). Except for S. belerius, most species showed in- ification treatment residues were removed. Samples were analyzed creasing fluxes towards the core surface. P. zoharyi fluxes increased with an Elementar Vario Micro Cube elemental analyzer (Elementar from about 50 years ago (16–17 cm; 1969–1961), with the highest Analysensysteme GmbH, Hanau, Germany) interfaced to a PDZ Europa value at 2–3cm(Fig. 5b). L. machaerophorum, Spiniferites spp. and 20 – 20 isotope ratio mass spectrometer (Sercon Ltd., Cheshire, UK) at T. pellitum fluxes increased from section 6–7cm(2003–2000) upward, UC Davis Stable Isotope Facility. Values are relative to the international although the highest fluxes were observed in section 21–23 cm reference standard Vienna Pee Dee Belemnite. The average standard de- (1929–1921) (Fig. 5b, c, d). viation based on replicate analyses of internal standards was b0.1‰. δ13 C data were used to estimate the proportion of terrestrial and ma- 4.2. Geochemical analysis rine organic carbon in the sediment (terrigenous input) using a binary mixing model in which the end-members were: i) terrestrial carbon −3 The Ntot values ranged from 0.07% to 0.15%, Norg from 2 × 10 %to3 (δ13C=−27‰; Westerhausen et al., 1993) and ii) precipitated carbon- −3 ×10 %(Fig. 6a), and Corg from 0.2% to 0.3% (Fig. 6b). The Corg/Ntot δ13 ‰ ate ( C=0 ; Nelson and Smith, 1996 and references therein). values remained low but their depth profile showed an upward increase from the core bottom to 9–10 cm, and then decreased to the core top 3.5. Climatic variables 13 (Fig. 6b). The δ C values displayed a similar trend as Corg/Ntot (Fig. 7a). The δ13C values were high (−3.17‰ to −1.54‰). These values fl The temporal variation of dinocyst uxes was analyzed in relation to were comparable to those of carbonate platforms such as the Great the regional climate variability, using air and sea surface temperatures, Bahamas Bank (−2.4‰ to 3.4‰; Swart and Eberli, 2005) and the rainfall and the Multivariate ENSO Index (MEI). Annual precipitation Belize Barrier Reef (−1.5‰ to 4.7‰; Gischler et al., 2009); this is consis- and annual mean maximum and minimum values of air temperature tent with the geological features surrounding San José Island (Hetzinger were obtained from La Soledad meteorological station (Baja California et al., 2006). Sur, 25 km from San José Island; SMN, 2015). Sea surface temperature The terrigenous index (Iterr) ranged from 81.4 to 116.0 and data from the area adjacent to the lagoon and MEI were obtained from displayed high values from section 6 cm towards the core surface, sug- NOAA (NOAA, 2016a, 2016b). The MEI is commonly used to monitor gesting an increase in the terrigenous contribution to sediments. The the occurrence of El Niño Southern Oscillation. High negative values δ13C-derived terrigenous input was small (6%–12%), and the distribu- represent the cold ENSO phase (La Niña); high positive values, the tion depth profile was consistent with Iterr (Fig. 7b). warm ENSO phase (El Niño) (Wolter and Timlin, 2011). 4.3. Climatic variables 3.6. Statistical analysis The available climatic records spanned from 1961 to 2015 (Fig. 7). Redundancy Analysis (RDA) evaluated the relationship between Annual rainfall ranged from 156 mm to 608 mm, with peak values be- dinocyst fluxes (response variables) and environmental variables (ex- tween 2000 and 2015 (Fig. 7d). The minimum values of the Multivariate planatory factors). The statistical significance of the relationship (p b ENSO Index (MEI min) ranged from −2.0 to 0.1, with the lowest values 0.05) was investigated by a Monte Carlo permutation test with 999 ran- were recorded during 2008–2011 and 1973–1980; the maximum dom permutations (Lepš and Ŝmilauer, 2003). The environmental vari- values (MEI max) ranged from 1.0 to 3.0, with the highest values ables used for the RDA included the terrigenous index and climatic data being recorded between 1998–2003 and 1980–1988 (Fig. 7e). Sea sur- available between 1961 and 2015. Climatic data were averaged for the face temperature ranged from 23.7 °C to 25.6 °C with the highest values time period represented by each core section. All data were transformed observed in 2014–2015 (Fig. 7f). The mean minimum air temperature to log (y + 1) to reduce data asymmetry (Zar, 1999; Legendre and (Tmin) ranged from 13.3 °C to 17.7 °C, and the highest values were ob- Legendre, 2012). served between 2000 and 2015. The mean maximum air temperature (Tmax) ranged from 29.9 °C to 32.6 °C, with peak values from 1994 to 4. Results 2006 (Fig. 7g). 4.1. Dinocyst assemblages 4.4. Dinocysts and environmental variables Thirty dinocyst species were identified in the SJ core (Table 1). Pho- ˂ tomicrographs of selected dinocyst taxa are shown in Fig. 3.The The RDA explained 92% of the total variance (Monte Carlo test: p fi dinocyst assemblage was dominated by Lingulodinium machaerophorum 0.05). The rst axis accounted for 85% of the data variations. The signif- (34%), Polysphaeridium zoharyi (33%), Spiniferites belerius (13%), icant environmental variables, with negative correlation values with Spiniferites spp. (7%), Nematosphaeropsis rigida (4%), Tectatodinium axis 1 were, Tmin and Iterr. Fluxes of most dinocyst species also showed pellitum (3%), and Spiniferites bentorii (2%), which altogether account a negative correlation with axis 1 (Table 2, Fig. 8). The second axis ex- fi for 96% of all dinocysts. Raw counts are available as online supplemen- plained only 7% of the database variability; the most signi cant vari- tary material (Appendix 1). ables were rainfall and sea surface temperature, with positive values Dinocyst abundance in surface sediments was 4090 ± 550 cysts g−1 (Table 2). (Fig. 4a), whereas down the core it ranged from 3784 ± 552 cysts g−1 at 8–9cm(1998–1996) to 25,108 ± 3577 cysts g−1 at 22–23 cm (1927– 5. Discussion 1923). P. zoharyi and Spiniferites spp. concentrations increased towards the core surface. In contrast, L. machaerophorum and S. belerius showed 5.1. Dinocyst assemblage low values towards the core surface. L. machaerophorum recorded the highest concentration and percentages between 18.5 cm and 30.5 cm The species richness and the dominant taxa in the SJ core were com- (Fig. 4b, c, e, f). N. rigida and T. pellitum abundances and percentages parable with those in sediments from the Gulf of California (Wall, 1986; showed a greater variability across the core (Fig. 4d, g). Heterotrophic Morquecho and Lechuga-Devéze, 2003; Limoges et al., 2010; Price et al., taxa showed a very low abundance (~3%, Appendix 1) relative to 2013) and other estuarine environments in North America (Pospelova phototrophic taxa (N97%). et al., 2005). Lingulodinium machaerophorum and Polysphaeridium Dinocyst fluxes ranged from 1396 ± 340 cysts cm−2 yr−1 at 16– zoharyi are associated with warm tropical and subtropical waters, al- 17 cm (1969–1961) to 11,876 ± 2397 cysts cm−2 yr−1 at 2–3cm though L. machaerophorum can also be abundant in temperate coastal 552 T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557

Fig. 3. Micrographs of selected dinocyst taxa. 1. Echinidinium delicatum,2.E. transparantum,3.Nematosphaeropsis rigida,4.Lingulodinium machaerophorum,5–6. P. zoharyi LM and SEM, respectively, 7–8. Lower (7) and upper (8) focal levels of Spiniferites bentorii,9–10. Lower (9) and upper (10) focal levels of S. belerius, 11. S. delicatus,12–13. Lower (12) and upper (13) focal levels of S. hainanensis,14–15. Upper (14) and lower (15) focal levels of S. hyperacanthus, 16. S. mirabilis, 17. Cyst of Pentapharsodinium dalei, 18. Quinquecuspis concreta,19. Selenopemphix quanta,20.Tectatodinium pellitum. Scale bars: 10 μm. T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557 553

Fig. 4. Total and major species dinocyst concentration (cyst g−1) [a, b, c, d] and relative abundance (%) [e, f, g] in the SJ core (San José Island, SW Gulf of California). Lmac: L. machaerophorum; Pzoh: P. zoharyi;Sbel:S. belerius;Sspp:Spiniferites spp.; Tpel: T. pellitum; Nrig: N. rigida. The horizontal dashed line depicts the oldest 210Pb-derived age (1918 ± 9). areas of regions in the northern hemisphere (Peña-Manjarrez et al., 5.2. Environmental conditions and cyst flux 2005; Zonneveld et al., 2013). The high abundance of P. zoharyi in the SJ core was similar to values The San José Lagoon is a natural protected area described as a pris- reported from other studies in tropical and subtropical coastal environ- tine environment (Cuellar-Martinez et al., 2017). Therefore, changes ments (Vásquez-Bedoya et al., 2008; Furio et al., 2012; Morquecho et al., in the dinocyst assemblages could be related to natural causes, rather 2012; Limoges et al., 2013, 2015) and temperate estuaries (Price et al., than to local anthropogenic effects. 2016). The dinocyst fluxes in the SJ core (1395–11,848 cysts cm−2 yr−1) Temperature is a key variable with a strong influence on the compo- were similar to those in Alvarado Lagoon, Mexico (Limoges et al., 2015), sition of both the phytoplankton community (Wells et al., 2015) and and Apponagansett, on the eastern coast of the USA (Pospelova et al., dinocyst assemblages (e.g., Rochon et al., 1999; de Vernal et al., 2001; 2002). Pospelova et al., 2004). According to the RDA, mean minimum air tem- Although the study area is mesotrophic (Halfar et al., 2004), dinocyst perature (Tmin) was the variable that best explained the cyst flux abundance in the SJ core (~2 × 104 cysts g−1) was comparable to that in changes in virtually all species (Fig. 8). high-productivity sites located in Mexican coastal areas such as Bahía de The vegetative cells of the three dominant dinocyst species in the SJ La Paz (Limoges et al., 2010) and Alvarado Lagoon (Limoges et al., 2015), core (L. macharophorum, P. zoharyi and Spiniferites spp.) have produced as well as in the Mediterranean Sea (Fertouna-Bellakhal et al., 2014)and blooms in Mexico. Blooms of Lingulodinium polyedra (=L. in western Canadian coasts (Radi et al., 2007; Krepakevich and machaerophorum) are frequently observed on the northwestern Pacific Pospelova, 2010). coast of Baja California at sea surface temperature ranging between 15 In addition, the SJ core showed the dominance of phototrophic taxa; °C and 22 °C (Peña-Manjarrez et al., 2001; Peña-Manjarrez et al., these have been associated with high availability of macronutrients 2009; Ruiz-de la Torre et al., 2013). In the Mexican Central Pacific, one such as organic nitrogen, and are inversely correlated with the abun- event for each L. polyedra and Gonyaulax spinifera (=Spiniferites taxa) dance of phytoplankton competitors, e.g. diatoms (Godhe and was reported at 30 °C and 25 °C, respectively (Ortiz-Lira and Jimenez- McQuoid, 2003). Nonetheless, under adverse conditions of low light Quiroz, 2006), and another G. spinifera bloom was observed in the penetration and limited nutrient availability, some phototrophic taxa Gulf of California at 31 °C (Gárate-Lizárraga et al., 2014). However, might also adopt a heterotrophic behavior and feed on other microor- there are no records of L. polyedra or G. spinifera blooms in the SJL. ganisms (e.g. bacteria, diatoms, other dinoflagellates, heterotrophic pro- In the case of Polysphaeridium zoharyi (=Pyrodinium bahamense), in tists and metazoans). Therefore, even phototrophic taxa such as laboratory assays the vegetative cells grow when water temperature Gonyaulax spinifera and Lingulodinium polyedra could be referred as ranging from 20 °C to 36 °C, and cyst germination of SJL strains occurs mixotrophic dinoflagellates (Burkholder et al., 2008 and references from 20 °C to 35 °C (Morquecho et al., 2014). In Florida and coastal la- therein; Jeong et al., 2010). goons in the Gulf of California (including SJL), P. bahamense blooms

Fig. 5. Total and major-species dinocyst fluxes (cyst cm−2 yr−1) in the SJ core (San José Island, SW Gulf of California). a) Total dinocyst flux, b) flux of L. machaerophorum (Lmac) and P. zoharyi (Pzoh), c) flux of S. belerius (Sbel) and Spiniferites spp. (Sspp), d) flux of T. pellitum (Tpel) and N. rigida (Nrig). 554 T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557

Table 2 Statistical summary of the Redundancy Analysis of dinocyst ﬂuxes (by species) from the SJ core (SW Gulf of California) and data for environmental variables.

Axis 1 Axis 2

Eigenvalue 0.54 0.05 Correlation of species with environmental variables 0.85 0.81 Cumulative percent variance of species data 53.7 58.3 Cumulative percent variance of species-environment 85.2 92.3 Correlation of environmental variables with axes Rainfall 0.07 0.60 Tmin −0.54 0.35 Iterr −0.48 0.04 Tmax 0.20 −0.06 SST 0.14 0.74 MEImax 0.40 −0.17 MEImin 0.27 0.56 Dinoﬂagellate cyst species scores with axes P. zoharyi −0.77 0.00 L. machaerophorum −0.76 −0.34 S. belerius −0.73 0.01 N. rigida −0.76 0.24 Spiniferites spp. −0.73 −0.12 T. pellitum 0.06 −0.23

Tmin: mean minimum air temperature, Tmax: mean maximum air temperature, SST: sea surface temperature, MEImax: maximum Multivariate ENSO Index, MEImin: minimum Fig. 6. a) Percentages of Norg and Ntot,b)Corg and Corg/Ntot depth profiles in the SJ core (San José Island, SW Gulf of California)., Multivariate ENSO Index, Iterr: terrigenous index. Bold numbers correspond to parameters that significantly correlate to axes. occur when water temperature reaches 25 °C or above (Usup et al., 2012; Morquecho et al., 2012). In Manila Bay, Philippines, P. zoharyi higher than in the sea outside (Morquecho et al., 2012). RDA showed fluxes have been related to warmer sea surface and air temperatures that dinocyst fluxes are associated primarily with atmospheric tempera- (Siringan et al., 2008). ture, mainly Tmin (Fig. 8), rather than with oceanic (SST) temperature. In the present study, the steady increase of dinocyst fluxes since the Sea surface temperature in the open ocean around San José Island mid-1960s, with peak values in the late 1990s, was especially conspicu- ranged between 23.1 °C and 25.8 °C (NOAA, 2016b), which lies within ous for P. zoharyi (Figs. 5b and 7c). Therefore, the recent atmospheric the temperature range reported to promote the growth of vegetative warming might be a plausible explanation for the increasing cyst fluxes cells of the dominant cyst species found in the SJ core (Peña-Manjarrez recorded in the SJ core, according to inland meteorological records near et al., 2001; Ortiz-Lira and Jimenez-Quiroz, 2006; Peña-Manjarrez et al., SJL, Tmin during 1998–2015 ranged from 14.1 °C to 17.7 °C, being signif- 2009). icantly higher vs. 1961–1998, when Tmin ranged from 13.3 °C to 14.1 °C In SJL and in lagoons on the Atlantic coast, the Pyrodinium bahamense (Cuellar-Martinez et al., 2017). blooms occur during the rainy season, associated with higher nutrient Water temperature variability in coastal water bodies results pri- concentrations derived from runoff (Phlips et al., 2006; Morquecho marily from insolation, surface air temperature, water depth, and local et al., 2012; Soler-Figueroa and Otero, 2015). Contrary to expectation, hydrodynamics such as rates of water exchange with the open ocean the correlation between rainfall (Fig. 7d) and dinocyst fluxes in the SJ (Sicard-González et al., 2012). The atmosphere, through heat fluxes, ex- core was not significant. erts an important effect on water temperature patterns inside shallow The RDA showed that Iterr (terrigenous index, Fig. 8), calculated lagoons (Salas-Pérez and González-Gándara, 2016). from concentrations of terrigenous element indicators, was positively As coastal lagoons have limited water exchange with the open sea, correlated with cyst fluxes on the first axis. Iterr and terrigenous input water temperature in the lagoon is likely dominated by atmospheric tem- (obtained from binary mixing model) indicated an increased terrige- perature (Newton et al., 2014) rather than by sea surface temperature, nous contribution during the past ~20 years. The increased terrigenous which only reflects open seawater conditions. Although there are no con- contribution is most likely associated with a higher input of nutrients, tinuous seawater temperature records available for SJL, during the thus promoting dinoflagellate growth (Azanza and Taylor, 2001). In warmest months water temperature in the lagoon can be up to 3.1 °C SJL, terrigenous materials are provided mostly by rainfall runoff,

δ13C (‰) Terrigenous index (Iterr) P. z oh a ryi flux (cyst cm-2 yr -1) Rainfall (mm) Multivariate ENSO Index SST (°C) Minimum air temperature (°C) -3.3 -2.7 -2.1 -1.5 70 95 120 03000600090000 200 400 600 -4 0 4 23 24 25 26 11 16 21 0 2015 Terrigenous 2 index 2012 Terrigenous 4 input 2007 6 2002 8 1997 10 1992

Depth (cm) Depth 12 1986 14 1977

16 a b c d e f g 1965 18 min max min max 1950

57911 29 31 33 Terrigenous input (%) Maximum air temperature (°C)

Fig. 7. Depth proﬁles from the SJ core (San José Island, SW Gulf of California): δ13C (a); terrigenous index and terrigenous input (b); P. zoharyi ﬂux (c); and environmental variables included in the Redundancy Analysis: rainfall (d); Multivariate ENSO Index (e); sea surface temperature (SST, f); and air temperature (g). T. Cuellar-Martinez et al. / Science of the Total Environment 621 (2018) 548–557 555

warming may exacerbate the occurrence of harmful algal blooms in pristine lagoons in the Gulf of California. The sedimentary reconstruction of temporal variations in dinocysts abundance provides a powerful tool to evaluate how climatic variability in coastal lagoons might affect dinoﬂagellate communities, and to better understand the occurrence of harmful algal blooms. Supplementary data to this article can be found online at https://doi. org/10.1016/j.scitotenv.2017.11.269.

Acknowledgments

This work was supported by the grants CONACYT 196813, PAPIIT- UNAM IN112914 and PROMEP/103.5/13/9335, IAEA-ARCAL RLA 7014. TCM thanks to Posgrado en Ciencias del Mar y Limnología, UNAM and CONACYT which provided the Ph. D. fellowship (307783). The authors thank E. Calvillo-Espinoza, J. Angulo-Calvillo, A. González-Peralta for their help provided in field work; M. Hernández-Vázquez and L.H. Pérez-Bernal for laboratory analysis; G. Ramírez-Reséndiz, C. Suárez, E. Cruz-Acevedo for data management and artwork; and D. Oviedo and H. Rojas for bibliographic research assistance. M. E. Sánchez-Salazar Fig. 8. Redundancy Analysis (RDA) ordination biplot of environmental data (bold line and A. Grant contributed to the edition of the English manuscript. We al- fl arrows) and dinocyst uxes (dashed arrows) in the SJ core (San José Island, SW Gulf of so appreciate to anonymous reviewers for their thorough and construc- California). tive reviews. although rainfall here area is scarce and occurs over a short period in References summer (SMN, 2015), the main causes of sediment transport and de- Alonso-Rodríguez, R., Mendoza-Amézquita, E., Velásquez-López, S.A., Seim, J.A., Martínez- posit along the Baja California Peninsula are tropical storms and hurri- Rodríguez, V.M., 2015. Florecimientos algales nocivos producidos por Pyrodinium – – canes (Martínez-Gutiérrez and Mayer, 2004). bahamense en Oaxaca, México (2009 2010). Salud Publica Mex. 57 (4):343 351 Available from:. http://www.scielo.org.mx/pdf/spm/v57n4/v57n4a13.pdf (Accessed The relationship between rainfall and Iterr values along the SJ core 05/03/2017). was not significant (p N 0.05); however, the highest values of both var- Azanza, R.V., Taylor, F.J.R.M., 2001. 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