Spatial distribution of organic-walled dinoflagellate

1

Spatial distribution of organic-walled dinoflagellate cysts in surface sediments from the southern Caribbean Sea and eastern tropical Pacific Ocean V. Ramírez-Valenciaa, A. Amézquitaa, C. González a*

a Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 N° 18A 12. Bogotá, Colombia* Corresponding author. ABSTRACT Numerous global studies of organic walled dinocyst distribution and their relation with the environment have been done across temperate regions, however neotrotropical oceans, are underrepresented, and the paleoceanography, paleobiogeography and paleoecology of region has been underdeveloped. Caribbean Sea and Pacific Ocean present a complex interaction between atmospheric circulation and oceanic currents that have effects in global climate (e.g. North Atlantic Ocean dynamics and ENSO), being a region with valuable paleoecological information deposited in sediments to study climate, sea level and geographic changes and also, to explore interactions between many organisms in several geologic periods. We analyzed 34 modern surface sediment samples from the Caribbean Sea and the tropical east Pacific Ocean (equator–16ºN, and 62ºW–85ºW) to assess the spatial distribution of organic-walled dinoflagellate cysts assemblages in relation to surface oceanographic conditions (temperature, salinity, oxygen, nutrients, water depth, and distance to coast). Sediment samples display different cyst concentrations with values ranging from 51 to 6036 cysts/cm3 of sediment. A higher diversity of dinocysts was found near the Equator line for the Pacific Ocean. The dinoflagellate assemblage composition and cyst concentration showed a clear separation between the two regions. Partial redundancy analyses (pRDA) illustrated that geographic location (Caribbean/Pacific), phosphates, and sea surface salinity (SSS) were the most important factors controlling cyst assemblage distribution in the area. The variance explained by the environment was 41%, by location 21%, and by joint environment and location 45%. The terrestrial influence (river discard) was analyzed from the pollen grains and spores of ferns counted of each sample and using a terrestrial/marine index. This study represents the first survey of recent organic-walled dinoflagellate cysts in the Caribbean and eastern tropical Pacific waters, and provides a regional dinocyst baseline that could be used in tropical paleoceanographical, paleoenvironmental and paleobiogeographical reconstructions. Keywords: northern South America, dinocyst, marine productivity, palynology, environmental parameters, pRDA.

2

1. Introduction

Oceans cover about two thirds of the Earth's surface, controlling not only the planet’s climate and global carbon cycle but also hosting a great diversity of microorganisms such as phytoplankton, which constitute the basis of complex food webs supporting most of the marine life (Barton et al. 2010). In the tropics, oceans play an important role in regulating the Earth´s climate system. They distribute heat from the Equator to higher latitudes, warming different areas across the globe, helping to regulate atmospheric CO2 (Kump et al., 2004), and containing the greatest phytoplankton biodiversity of the world (Barton et al., 2010). However, over the last decades, tropical oceans have been suffering dramatic changes due to global change. These include a rise in temperatures, reduction in upwelling nutrients to surface waters, and strong declines of phytoplankton blooms (Taylor et al., 2012).

Despite the current problem associated to climate change, tropical oceans remain largely

unexplored, especially in deep ocean areas (Kunzig, 2007). This is not only in terms of biodiversity (Irigoien et al., 2004), but in the opportunity to understand historical climate variation using marine proxies as phytoplankton fossil remains (Wefer et al., 1999). Studies of marine tropical fossil phytoplankton communities deposited in ocean surface sediments allow us to understand and reconstruct past climates, environmental conditions, water productivity, and even human activities (e.g. Bouimetarhan et al., 2009; González et al., 2006; Limoges et al., 2013). In order to infer such historical changes, it is crucial, however, to first understand the present distributions and ecology of modern taxa. Currently, the dominant species of marine phytoplankton are diatoms, dinoflagellates, and coccolithophorids (Parsons et al., 1984). Together, they represent the major primary production in marine environments, playing a significant role in marine ecosystem dynamics (Dale, 2001). In neritic zones, where the high carbonate dissolution restricts the use of calcareous proxies like foraminifera and coccolithophorids, marine microfossil assemblages of organic dinoflagellate cysts become a valuable tool for historical environmental reconstructions (de Vernal et al., 1997; Vernal et al., 2001).

Numerous global organic-walled dinocyst distribution studies have been done across temperate marine environments (Bouimetarhan et al., 2009; Devillers and De Vernal, 2000; Head, 2007; Höll et al., 2000; Narale et al., 2013; Orlova et al., 2004; Zonneveld et al., 2013). These studies have shown close relationships between assemblages of organic walled-dinoflagellate cysts (dinocysts) and environmental conditions in the upper water column, thus constituting a baseline for environmental, hydrological, and climatic reconstructions (e.g. Head, 2007; Höll et al., 2000). Unfortunately, tropical oceans, especially from northern South America are underrepresented and still have no data (Fig. 2a) despite the global efforts to integrate information of modern global dinoflagellate cyst distributions (Zonneveld et al., 2013).Here, we present palynological analyses undertaken

3

on 34 surface sediment samples from selected areas of the Caribbean Sea and eastern tropical Pacific Ocean. We related the spatial distribution of organic-walled dinocyst assemblages with environmental parameters of the upper water column. In particular, this study aims 1) to describe the species distribution and composition of organic-walled dinoflagellate cysts in the Caribbean and tropical Pacific waters, 2) to relate their spatial distribution with surface oceanographic conditions (temperature, salinity, oxygen, nutrients, water depth, and distance to coast) and preliminarily terrestrial influence (e.g. river discard), and 3) to develop a regional Dinocyst baseline that will serve for paleoenvironmental and paleoceanographical reconstructions at different time-scales. 2. Regional setting

The studied area is located the north of South America, in the tropical eastern Pacific Ocean and Caribbean Sea, extending from 0º N to16º N. This is a region with a complex interaction between atmospheric circulation and oceanic currents (Restrepo and Lopez, 2008) (Fig. 1). The main atmospheric circulation features in the region are the Intertropical Convergence Zone (ITCZ) (Fig. 1(1a, 1b)) and the trade winds (Fig. 1(b)), which impacts the rainfall annual seasonality and controls the humid tropical climate (Poveda et al., 2006). The principal oceanic currents are the Caribbean (Fig. 1(f)) and Equatorial currents (Fig. 1(h)), responsible for recycling and distributing nutrients influenced by the prevailing wind systems.

Fig. 1a. Simplified map of the atmospheric circulation (yellow) and main sea currents (red) of

the Tropical Pacific Ocean and Caribbean Sea. ITCZ June (a1), ITCZ January (a2), trade winds (b), Caribbean low level jet (c), Choco Jet stream (d), Guajira upwelling (e), Caribbean current (f), Pacific current (g), Equatorial current (h), ENSO (i), Magdalena river delta (j), Atrato river delta (k), San Juan river delta (l), Patia river delta (m). 1b. The location of the surface sediment samples (yellow stars).

4

2.1 Caribbean Sea

The Caribbean Sea is characterized by oligotrophic and translucid waters. It is associated with coral reefs and calcareous sediments, nutrient-depleted surface waters, and seasonal SSS variations (Restrepo et al., 2014). The main atmospheric and oceanographic characteristics are (Fig. 1): the Guajira upwelling system (e): when trade winds hit the Guajira Peninsula and nutrients are carried from the northern Caribbean Sea (Hu et al., 2004). It increases when the trade winds are intensified during December-March (Andrade & Barton 2005). The Caribbean low-level jet (c): transports humidity from the Caribbean to the Pacific through the Isthmus of Panama, which promotes the upwelling near the north of Colombia. In the Pacific region, it affects the tropical convective systems, such as easterly waves and their organization in tropical cyclones (Poveda et al., 2006). River influence (j-k): the Magdalena and Atrato rivers are the longest rivers that flow into the region, having an important role in discharging freshwater, nutrients, and sediments that promote local eutrophication near to the rivers mouths (Restrepo et al., 2014) (e.g. Bocas de Ceniza In Barranquilla and Golfo de Urabá in Antioquia). 2.2 Eastern equatorial Pacific Ocean

The Pacific Ocean is richer in nutrients and presents turbid waters, low oxygen content, and higher levels of organismal diversity than the Caribbean sea (Restrepo and Lopez, 2008). It is characterized by a north–south precipitation and sea surface temperature (SST) gradients, with stratified waters in the north of the equator (Eastern Pacific Warm Pool- EPWP) (Poveda et al., 2006). The main atmospheric and oceanographic variables are presented in Fig. 1, as follows: ENSO (i): El Niño Southern Oscillation is the main forcing mechanism of interannual and interdecadal climatic variability in tropical South America. It refers to unusual warming of SST and it has been associated with important climatic variations in the region from decades to millennia (Poveda et al., 2006). ENSO affects the distribution of SST semi periodically, causing warmer tropical waters around the world oceans. It also influences the hydrology of northernmost South America rivers by inducing drier conditions in environment that ultimately are reflected on low river flows and discharge. The Choco Jet stream (d): centered at 5°N, this low level jet transports large quantities of moisture inland. Its strength is modulated by the annual cycle, being especially strong in October-November. It is the entity that provides large amounts of fresh water to the Pacific, that causes partially lower SST compared to the Caribbean (Poveda et al., 2006).; River influence (l-m): the San Juan and Patia rivers are the longest rivers that flow into the region, and they have an important role in discharging high volumes of freshwater and nutrients (Restrepo and López, 2008).

According to NOOA (2014), the mean SST in the region range between 26 ºC to 30 ºC, the bottom water oxygen ranges from 0 ml/L to 4 ml/L, phosphates from 0.1 µmol/L to 1

5

µmol/L, and nitrates from 0 µmol/L to 5 µmol/L in both the Caribbean and Pacific superficial waters, without major drastic differences. The sea surface salinity, however, presents important differences ranging from 33 psu in the Pacific to 36 psu in the Caribbean (Fig. 2).

Fig. 2. Summary of global samples used in the latest compilation of modern surface sediments

dinoflagellate cyst distribution (blue circles), extracted from Zonneveld et al. 2013 (a). Global distribution of: annual sea surface salinity (psu) (b), annual sea surface temperature (ºC) (c), annual sea surface oxygen (ml/l) (d), annual sea surface phosphate (µmol/l) (e), and annual sea surface nitrates (µmol/L) (f). Decadal average 1955-2012 (World Ocean Atlas 2013). 3. Material and methods

We studied 34 marine surface sediment samples (0-1 cm) (Table 1). Samples were collected mainly by gravity coring and drilling during different cruises: Vema and Robert D. Conrad by Lamont-Doherty Earth Observatory (LDEO), ships: KNR-176-2 and Joides Resolution 165, 312, 334, 340 by Ocean Drilling Program (ODP), Ergoro and Merayana by Instituto Colombiano de Petróleo (ICP) and Uniandes expeditions (Table1) in different years since 1958 to 2014. These samples are assumed to be recent, but may represent different time intervals depending upon sedimentation rates and biological mixing. Thus, we assumed that the upper first centimeter probably represents the present sediment accumulation on the sea floor. The samples were raised from water depths ranging between 4–3797 meters below sea level (mbsl). The core top sediment was mainly composed of calcareous clays. After requesting samples to marine repositories, wet and dry sediments were stored in a refrigerator (4ºC) until palynological treatments were performed.

6

Table 1. Studied surface sediment samples. Lamont–Doherty Earth Observatory (LDEO), Ocean Drilling Program (ODP), Laboratorio de Palinología y Paleoecología tropical (PPT), Laboratorio de Biología Molecular Marina (BIOMAR), Instituto colombiano de petróleo (ICP), Universidad EAFIT (EAFIT).

Sample number

Sample name

Repository Location Collection year

Latitude °N

Longitude °W

1 13 LDEO Caribbean 1964 9.4 -77.55

2 115 LDEO Caribbean 1970 13.93 -72.36

3 148 LDEO Caribbean 1970 11.74 -74.28

4 032 LDEO Caribbean 1967 11.2 -76.1

5 007 ODP Caribbean 1958 11.5 -75.83

6 1000A ODP Caribbean 1996 16.55 -79.86

7 1397A ODP Caribbean no data 14.9 -61.42

8 U1396A ODP Caribbean no data 16.5 -62.45

9 Zapsurro PPT/Uniandes Caribbean 2014 8.83 -77.49

10 Necoclí PPT/Uniandes Caribbean 2014 8.41 -76.79

11 Cuevas BIOMAR/Uniandes Caribbean 2014 10.25 -75.62

12 Laguna varadero BIOMAR/Uniandes Caribbean 2014 10.3 -75.58

13 25 LDEO Pacific 1965 5.71 -81.05

14 253 LDEO Pacific 1966 6.51 -79.4

15 11 LDEO Pacific 1958 7.75 -79.05

16 MC4 LDEO Pacific no data 7.27 -78.24

17 JPC9 LDEO Pacific no data 6.82 -77.9

18 216 LDEO Pacific 1965 5.25 -77.6

19 65 LDEO Pacific 1965 2.51 -79.25

20 JPC32 LDEO Pacific no data 4.67 -77.96

21 U1381B LDEO Pacific 2011 8.42 -84.15

22 015 LDEO Pacific 2009 6.95 -84.28

23 Merayana2 ICP Pacific 2009 4.59 -77.47




27 Ergoro1 ICP Pacific 2009 2.51 -78.6




31 Kama1 EAFIT Pacific no data 0.26 -80.71




7

Surface samples (1 cm3) were processed for dinocyst analysis according to standard palynological preparation procedures (de vernal et al., 1999), which include decalcification with 10% hydrocloric acid (HCl) and removal of the siliceous fraction using 40% hydrofluoric acid (HF). Two tablets of Lycopodium spores (20848 spores/ tablet) were added to each sample during the decalcification process in order to calculate palynomorph concentrations based on one cubic centimeter of sediment (cm3). The residue was sieved through a 7µm mesh size sieve using an ultrasonic bath (2 min) to remove clay particles. An aliquot of 40 µl was mounted on a gelatine-glycerine for microscope investigation.

Cyst specimens were counted using a Zeizz Imager A.2 optical microscope at 400x to 1000x magnification. In general one to four slides were analyzed per sample. We established the minimal count at 50 specimens in total for locality for the inclusion in the dataset and statistical analysis. Results are expressed as relative abundances (%) and concentration of specimens per cubic centimeter of sediment. Cyst identification was made using original descriptions (Bujak et al., 1980; Bütschli, 1873; Lentin and Williams, 1993; Reid, 1974; Sarjeant, 1970; Wall and Dale, 1966; Wall, 1967; Zonneveldd, 1997; Zonneveldd and Jurkschat, 1999) and following the modern dinocysts web key (MARUM, 2013) and the web data base (DINOFLAG2, 2015). Dinocysts concentration per cubic centimeter of sediment was calculated based on the proportion of exotic Lycopodium spores counted to the initial number of Lycopodium spores added (20848 spores per tablet) and the original volume of the sample (1 cm3) (Maher, 1981).

Additionally, pollen grains, fern spores and foraminiferal organic linings concentrations

was calculated to estimate a broad and preliminarily measure of the terrestrial influences on the sites (e.g. river discharge, wind flows, seawards, etc.) (Limoges et al., 2013) using the terrestrial to marine ratio. This index is useful to explore both, continental and oceanic environmental activities and their relation. The terrestrial /marine ratio was calculated as follows: the sum of the total concentration of pollen grains and fern spores was divided by the sum of the total concentration of dinocysts and organic forams linings.

3.1 Statistical analyses

We used two quantitative matrix to describe the relationships between sea surface water parameters (predictive matrix) and organic-walled dinocyst composition in the sediments (response matrix) using the R software (R core Team, 2015, package Vegan). A partial redundancy analysis (pRDA) was performed on relative dinocyst abundances and measurements of environmental variables using the landscape position (latitude/longitude) of each sample point as co-variable in order to explore any potential spatial autocorrelation of the environmental factors. Relative abundance data were Hellinger–transformed and the environmental variables were scale–transformed prior to the analysis in order to increase their statistical weight. We considered most counted taxa, with the exception of those

8

presenting very low occurrences (%<1), such as: Echinidinium spp., Stelladinium sp., and Selenopemphix quanta. The significance of each environmental parameter was evaluated based on the length of its gradient in the ordination space and their correlation to the main axes. The parameters used for these analyses included sea surface temperature, sea surface salinity, sea surface dissolved oxygen, sea surface phosphates and nitrates, water depth and distance to coast (Table 2). Also, regressions for the best environmental variable were explored in relation to dinocyst concentrations. 3.1.2 Oceanographic parameters

Temperature, dissolved oxygen, salinity, nitrate, and phosphate variables were obtained

from the WOA 2013 database (WOA, 2013). We used general trends (annual average from 1952 to 2012) and the geographic location of each sample at 0 m depth (Table 2). The distance from the coast was measured using Google Earth software (version 7.1.2.2041) and water depth was measured in situ (provided by repositories). Distribution maps were drawn using Surfer for Windows version 13 with the Kriging method. 4. Results 4.1 Dinocyst concentrations and palynological assemblages

A total of 12 dinoflagellate cyst taxa were recorded in the sediment samples along both the Caribbean and Pacific regions (Table 3, Fig. 3, Annex 1) with moderate to high dinocyst concentrations (between 51 to 6036 cysts/cm3) (Fig 4). Seven of these 12 cyst types were identified to species level (Bitectatodinium Spongium, Spiniferites pachydermus, Echinidinium aculeatum, Nematosphaeropsis labyrinthus, Operculodinium centrocarpum sensu estricto, Operculodinium centrocarpum–isrraelianum? and Selenopemphix nephroides), two to genus level (Brigantedinium spp. and Spiniferites spp.) and the remaining were identified as Aff. And Cief. (Aff. Lingulodinium machaerophorum, Aff. Echinidinium sp. and Cief. Cyst of Polykicos schwartzii–kofoidd?).

Relative cyst abundances were higher near the Equator (Table 4, Fig. 5). Heterotrophic

cysts dominated the assemblages over phototrophic taxa in most samples. A group composed of Brigantedinium spp. that includes specimens of Brigantedinium simplex, Brigantedinium cariacoense and unidentified Brigantedinium species (Brigantedinium spp.) accounted for 58% of the total assemblages and predominated in high productivity zones. Other taxa presenting relatively large abundances were Bitectatodinium spongium (17%), Echinidinium aculeatum (7%), and Aff. Lingulodinium machaerophorum (6%).

9

Table 3. Organic dinoflagellate cysts reported from surface samples studied and their trophic behavior (P/H: phototrophic or heterotrophic) (Vásquez-Bedoya et al., 2008).

Dinoflagellate species Abrev P/H

Bitectatodinium spongium Bitec P

Spiniferites pachydermus Spinp P

Spiniferites spp. Spinach P

Aff. Lingulodinium machaerophorum Lingum P

Operculodinium centrocarpum sensu estricto Opercse P

Operculodinium centrocarpum–isrraelianum? OpercsWD P

Nematosphaeropsis labyrintus Nema P

Brigantedinium spp. Briga H

Selenopemphix nephroides Selen H

Echinidinium aculeatum Echin H

Cief. Cyst of Polykicos schwartzii–kofoidd? Polsch H

Aff. Echinidinium sp. Polyha H

The Caribbean and Pacific samples were also characterized by terrestrial (pollen grains,

fern spores) and marine (foraminiferal organic linings and dinocysts) components (Table 4). Pollen grains and fern spores reached maximum values near river mouths (Fig. 9 b, c), especially in the Pacific Ocean and near the coast, while relative abundance of organic foraminiferal linings was higher in the Caribbean (Fig. 9 d). From our data, shallower sites have a higher input of terrestrial palynomorphs compared to more off shore sites.

The pRDA shows that the fractions of the environmental component explained 41%, the site location 21%, and the joint environmental and site location fraction 45% of the total dinocyst assemblage variation, corroborating the necessity to do the partial redundance analysis to avoid autocorrelation by the spatial distribution of the samples. The most prominent environmental factors that explained the distribution of dinocyst assemblages according axis 1 of RDA were: site location (Caribbean /Pacific) (0.9459), phosphates (0.89 %) and SSS (-0.733) (Table 6). The geographic location, phosphates concentration, and SSS correlate with axis 1, whereas distance to coast and water depth were linked to axis 2 (Table 6).

Two distinct assemblage groups were well-defined from the redundancy analysis

diagram that respectively corresponded to Caribbean and Pacific regions (Fig. 7 a,b). Axis 1 is defined by negative scores of Spiniferites spp., Nemathosphaeropsis labyrinthus, Bitetactodinium spongium, and Aff. Lingulodinium machaerophoru and by positive scores of Brigantedinium spp., Operculodinium centrocarpum sensu wall et Dalle (1966), Operculodinium centrocarpum–isrraelianum, Echinidinium aculeatum and Selenoprmphix nephroides (Table 6, 7; Fig. 9, 10). Axis 2 is characterized by negative scores of

10

Spiniferites pachydermus and by positive scores of Aff. Echinidinium sp. and Cief. Cyst of Polykrikos schwartzii-kofoid? (Table 7).

Fig. 3. Bright field light micrographs of studied dinocyst taxa. Bitetactodinium spongium (a–b),

Spiniferites pachydermus (c–d), Spiniferites spp. (e–f), Aff. Lingulodinium machaerophorum (g–h), Operculodinium centrocarpum sensu estricto (i–j), Operculodinium centrocarpum–isrraelianum? (k–l), Nematosphaeropsis labyrintus (m–n), Brigantedinium spp. (o–p), Selenopemphix nephroides (q–r), Echinidinium aculeatum (s–t), Aff. Echinidinium sp. (u–v), and Cief. Cyst of Polykikos schwartzii–kofoidd? (x–y).

11

Table 2. Environmental parameters corresponding to the database sampling sites, annual average 1955–2012 in the surface: temperature (SST) (ºC), salinity (SSS) (psu), Oxygen (SSO) (ml/L), sea surface phosphate (SSP) (µmol/L), sea surface nitrate (SSN) (µmol/L), from the World Ocean Atlas 2013 (WOA, 2013), and water depth (WD) (mbsl), distance to coast (DC) (m), and sediment description.

Sample SST

SSS

SSO

SSP

SSN WD

DC

Sediment description

1 28.53 34.99 4.61 0.014 0.133 1739 47280 90% clay, 10% silt, with carbonaceous lamellae and calcareous and sells content, color light brown, consolidated.

2 28.29 32.18 4.79 0.056 0.300 2109 48820 50% clay, 50% silt, color light brown, unconsolidated.

3 27.08 35.7 4.44 0.015 0.717 1257 47865 50% silt, 50% clay, color light brown, consolidated.

4 28.06 35.97 4.51 0.000 0.100 2704 95100 50% silt, 50% clay, color light brown, consolidated with micro calcareous fragment content.

5 27.08 35.9 4.54 0.010 0.000 2869 100960 100% silt with apparent fossiliferous content, color light brown, moderately consolidated.

6 28.11 34.78 4.32 0.065 0.000 916 1310 80% silt, 20% clay, color light brown, moderately consolidated.

7 27.55 35.00 4.62 0.113 0.460 2482 651830 50% clay, 50% very fine grain sand, color dark brown, moderately consolidated.

8 27.23 35.37 4.65 0.120 0.000 3180 440820 33% fine sand, 33% clay, 33% silt, color reddish light brown, moderately consolidated.

9 27.27 35.66 4.6 0.014 0.133 30 186770 33% clay, 33% silt, 33% very fine grain sand, color dark grey, unconsolidated.

10 28.5 33.69 4.29 0.010 0.100 15 1260 100% clay with silt traces, color medium brown, unconsolidated.

11 28.69 34.37 4.32 0.020 0.100 4 182 20% clay, 20% silt, 60% sand, color light brown, unconsolidated.

12 28.69 34.37 4.32 0.020 0.100 4 886 80% clay, 20% silt, color medium grey brownish, unconsolidated.

13 27.50 31.79 4.76 0.239 1.853 1359 386100 100% silt, color medium brown to grey, unconsolidated.

14 27.59 32.06 4.71 0.303 0.933 3259 207700 50% silt, 50% clay, color light grey, moderately consolidated.

15 26.05 33.22 4.7 0.230 0.410 249 78210 100% very fine grain sand, color light brown, moderately consolidated.

16 28.65 30.22 4.68 0.162 0.244 2121 29080 100% clay, with silt traces, color light brown, moderately consolidated.

17 26.92 27.02 4.62 0.268 1.152 288 22140 100% clay, color medium brown, unconsolidated.

18 27.40 28.39 4.60 0.240 6.033 761 22330 80% silt, 20% clay, color light grey, consolidated.

19 26.45 32.36 4.37 0.382 1.892 2074 78030 50% clay, 50% silt, color light brown, consolidated to moderately consolidated.

20 23.17 30.74 4.66 0.355 1.165 2195 69610 100% clay with silt traces, color medium brown, unconsolidated.

21 28.53 34.99 4.61 0.360 1.100 2069 49928 90% clay, 10% silt, color dark green to medium brown, unconsolidated.

22 27.63 32.77 4.7 0.160 0.500 1736 190181 50% silt, 50% clay, color light brown with micro calcareous fragment content, consolidated.

23 28.1 26.65 4.75 0.355 1.165 94 17050 90% clay, 10% silt, color medium grey, unconsolidated.

24 26.6 29.99 4.75 0.355 1.165 1534 61714 90% clay, 10% silt, color medium Brown to dark green, unconsolidated.

25 26.97 27.6 4.75 0.240 6.033 1519 35057 80% clay, 20% silt; color medium Brown to dark green, unconsolidated.

26 28.69 28.23 4.6 0.240 6.033 66 9830 90% clay, 10% silt, color dark brown to medium grey, unconsolidated.

12


28 26.47 29.42 4.9 0.382 1.892 653 32170 80% clay, 20% silt, color dark brown to medium grey, unconsolidated.


30 26.23 32.39 4.37 0.382 1.892 686 33811 50% clay, 30% sand, 20% silt, color dark brown to medium grey, moderately unconsolidated.



33 25.84 33.17 4.53 0.236 0.002 3797 99071 90% clay, 20% silt, color medium green to medium brown, unconsolidated.

34 26.27 34.57 4.79 0.313 3.854 1623 47138 20% silt, 80% clay, color medium brown to medium green, unconsolidated.

Fig. 4. Percentages of phototrophic taxa (black) (%) and heterotrophic taxa (yellow) (%),

dinoflagellate cyst concentrations (cyst/cm3), pollen grain concentrations (grains/cm3), fern spore concentrations (spores/cm3), foraminiferal organic lining concentrations (linings/cm3) in Caribbean Sea and eastern tropical Pacific Ocean.

13

Fig. 5. Dinocyst concentration (a), ratio of phototrohic to heterotrophic cysts (b) %

phototrophic cysts (c) % heterotrophic cysts (d). Black circles denote the location of the surface sediment samples.

Fig. 6. Relative abundances of the main organic-walled dinoflagellate taxa expressed in

percentages of total cysts from marine surface sediments.

14

4.2 Statistical analyses

The RDA analysis documents that the highest relative abundances of B. spongium in the Pacific Ocean were observed at sites characterized by high SSN and SSP concentrations and relative low sea surface salinity and temperature. The relative abundances of Operculodinium spp. and Spiniferites spp. were observed at sites characterized by high SSS and SST and low nutrients. Based on the statistical analysis, two groups of species can be recognized.

Caribbean group: Is represented by high concentrations of heterotrophic Brigantedinium

spp. and phototrophic Spiniferites pachydermus and Operculodinium centrocarpum. Samples presented low pollen grain and fern spore concentrations compared to the Pacific Ocean, but higher organic foraminiferal linings associated to high values of SSS and SST (Fig, 9, 10).

Pacific group: The dominant Pacific cysts were Bitectatodinium spongium (Phototropic),

Brigantedinium spp., and Echinidinium aculeatum (heterotrophic) (Fig, 9, 10). Samples showed higher pollen grain and fern spore concentrations than in the Caribbean, and these taxa were associated with high nutrient contents (nitrates, phosphates) and were influenced by river outflow.

Fig. 7. Results of the Redundance analysis (RDA). Diagram of species and environmental

parameters according to axes, axis 1 (66%) and axes 2 (12%) of the variance (a) in blue: Caribbean samples, in red: Pacific samples. The abbreviations of taxa names are in Table 5. Ordination diagram of sample scores according to axis 1(b).

15

Table 4. Caribbean Sea and east Pacific Ocean organic-walled cyst dinoflagellate, pollen grains, fern spores, and organic foraminiferal linings (concentration /cm3).

Sample Dinoflagellate cysts (cysts/cm3)

Pollen grains (grains/cm3)

Ferns spore (spores/cm3)

Organic linings (linings/cm3)

1 61 421 139 868

2 213 533 107 224

3 509 632 308 231

4 326 465 295 124

5 51 89 79 135

6 639 3566 114 1037

7 889 3073 473 3227

8 220 958 142 610

9 1039 2688 397 11455

10 1632 3146 505 3650

1 493 1980 184 3341

12 1103 11266 58 3775

13 3206 1625 546 1481

14 2174 1076 399 898

15 505 715 255 155

16 4230 3320 3257 3257

17 1951 2353 1243 2085

18 2547 5661 2417 1437

19 1465 1198 753 1028

20 1656 2786 943 1360

21 2069 2977 761 1736

22 606 345 268 394

23 1630 5314 4145 1541

24 2912 4148 1765 684

25 2195 5377 2112 1865

26 2850 2932 1612 456

27 2531 4522 2157 1286

28 6036 5608 2397 3938

29 2548 8082 2136 849

30 4211 5115 723 1550

31 5609 4079 935 5439

32 3008 2345 1020 7054

33 4224 2338 373 3105

34 2408 3283 1094 963

Relative abundances of Brigantedinium spp. were higher in the Caribbean near the coast

and in the Pacific samples far from the coast (Fig. 9f); similar to S. nephroides (Fig. 10f),

16

Spiniferites spp., (Fig. 10g), S. pachydermus (Fig. 10h), O. centrocarpum sensu estricto (Fig. 10 b), and O.centrocarpum–israelianum? (Fig. 10c) that prevails in the Caribbean but not in the Pacific. While B. spongium (Fig. 9e), E. aculeatum (Fig.9g), Aff. L. machaerophorum (Fig. 9h), N. labyrintus (Fig. 10a), Cief. cyst of Polykicos schwartzii–kofoidd? (Fig. 10d), and Aff. Echinidinium sp. (Fig. 10e) were higher in Pacific waters and mostly have high associations with river discharges.

5. Discussion

Before discussing dinocyst species distribution in sediments it is important to emphasize

the possible effect of long-range cyst transport and cyst preservation on the ocean floor which may cause a wrong interpretation (Bouimetarhan et al., 2009). However, like pollen grains distribution is reflected on the ocean floor and are a comparable sedimentological particle to dinocysts (Hooghiemstra et al., 2006), we assume that large scale transport did not considerably affect dinocyst distribution due pollen grains do not show large scale transport (very well associated to river discard and the proximity to the coast) and due to the presence of relatively closed basins (Panama Basin, Caribbean Basin).

All studied samples are assumed to be recent, but may represent different time intervals (1958 to 2014) depending upon sedimentation rates and biological mixing, for that reason in order to reduce any temporal change in fossil assemblages in relation to the instrumental data, we used mean trends of oceanographic variables obtained from the World Ocean Atlas database (WOA, 2013). Accordingly, the “modern” assemblage postulated here might have, therefore, introduced a source of error when comparing the dinocyst data to oceanographic data obtained through instrumental measurements and will be an internal variation that could affect the data and introduce uncertainties in the results. However, when we compare our data with previously reported studies for temperate species composition in the Atlantic and Pacific Oceans with specific collection date and measurement data (de Vernal et al., 2007; Rochón et al., 1999) we found similar patterns (e.g. higher dinocyst concentrations in the Pacific Ocean (Fig. 5a, 8a) and dinocyst assemblages), suggesting no big effect due the biological and environmental variation. Also, we do not find relation between collection years with the dinocysts concentrations (data not shown).

The concentration of dinoflagellate cyst (51 to 6036/cm3 sediment) along the Caribbean

Sea and Pacific Ocean compared with the dinoflagellate cyst abundance reported along different parts of the world (Furio et al., 2012) are moderate to high possibly due the proximity to Equator were there are global reports of higher concentrations (Zonneveld et al., 2013), possibly due the proximity with currents with high amount of nutrients (e.g. Humboldt current).

17

5.1 Characteristics of palynological assemblages

The phototrophic Operculodinium centrocarpum and Spiniferites spp. (includes Spiniferites pachydermus and Indeterminate Spiniferites spp.) were the most abundant taxa in the Caribbean Sea, similar to that previously reported for the north Atlantic Ocean and adjacent seas, where the same genera also dominated the total assemblages (Rochón et al., 1999). In this way, this species can be useful in studies from this site, indicating the presence of ridges. Spiniferites spp. mainly occur in costal zones (MARUM, 2013), however from our data, we find they are in open waters, far to the coast and probably in oligotrophic environments (Fig. 10 g–h), suggesting idem there could be other factors not studied here that could influence their distribution in the study zone as the high input of nutrients and sediments in the region (e.g. Canal del Dique in Cartagena) or to the global climate change (Taylor et al., 2012). Like it is autotrophic and needs photosynthesis to live, they could be a good indicator of low turbid waters and due that need stay away to the river mouths.

Pacific Ocean assemblages were dominated by the phototrophic B. spongium and Aff. L.

machaerophorum and heterotrophic E. aculeatum, similar to that found in previous dinocyst community studies on the eastern tropical Pacific waters (Vásquez-Bedoya et al., 2008). All of these taxa, are indicator species in areas of active upwelling and high concentrations of nutrients (Zonneveld et al., 2013), and their presence confirm the high output of nutrients carried by rivers not only in the Pacific zone but in the Caribbean Sea, where E. aculeatum was also present. B. spongium has been reported in costal upwelling (Zonneveldt et al., 2013). However, in our sample was very well associated with the Pacific current (Fig. 9e) and with a tendency to increase their relative abundances far to the coast, advising there could be again other factors not studied here that could influence their distribution (e.g. ENSO and EPWP). The Aff. L. machaerophorum was abundant taxa in region that usually are associated with river discharge plumes (MARUM, 2013), situation observed only in Pacific samples possibly due the highest nutrient content. On the other hand, despite reports in template environments that E. aculeatum is not observed in the vicinity of upwelling zones were low SSS occur (MARUM, 2013; Zonneveld et al., 2013), we found and strong association between their cysts and Atrato, San Juan and Patía river plumes (Fig. 9g), suggesting that E. aculeatum could have a a synergy of environmental conditions (upwelling + fluvial download + distance to coast) (Fig. 9 h).

Also, is relevant to remark too that O. centrocarpum s.e. concentrations were low

compared with other taxa and their distribution were in all kinds of environments, as is reported in other regions (Zonneveld et al., 2013), however, higher abundances were founded near the Panama Basin (Fig. 10b), where there are a boundaries between the Cocos, Carnegie, Coiba, and Malpelo Ridges, with specific physical properties of the water masses (Patarroyo and Martinez, 2013).

18

Brigantedinium spp. (includes Brigantedinium simplex, Brigantedinium cariacoense and Indeterminate Brigantedinium spp.) was the most generalist dinocyst present in both oceans (Fig. 9f). This again is consistent with previous reports for other places of the world, where this taxon commonly dominates the association across coastal regions to central parts of the oceans. It is also commonly observed in oligotrophic to eutrophic and in low to hypersaline environments (Zonneveld et al., 2013). The maximum concentrations are associated with neritic environments. According to several authors (MARUM, 2013; Rochón et al., 1999; Wall et al., 1977) the distribution of Brigantedinium spp. is global and can form up to 99% of the total association recorded. This suggests that this taxa presents an opportunistic behavior (Rochón et al., 1999) and, hence, constitutes a dinocysts proxy with low resolution for this region.

From our results, we propose B. spongium, S. pachydermus, E. aculeatum, Aff. L. machaerophorum and Cief. Cyst of P. schwartzii–kofoid? as the best proxies to reconstruct oceanographic parameters in the region due their high relations with studied environmental variables as in other tropical regions (Bouimetarhan et al., 2009).

On the other hand, fortunately all reported taxa do not represent toxic species, despite a

worldwide increase in harmful toxic algal blooms (Gilbert et al., 2005) and despite that in other tropical Pacific waters, such as in the Gulf of Mexico there are already reports of toxic species (Limoges et al., 2013) resulting in significant economic losses (Anderson et al., 2005). We propose that constant monitoring should be implemented in the region in order to develop of appropriate mitigation strategies in the case that these toxic species invade the coasts. 5.2 Main relationships between dinoflagellate cyst and environmental conditions

Phosphates– It is one of the mostly limiting element in the marine realm (Prauss, 2000) and their concentrations in the upper colum water have different effects on cell growth, encystment and germination of dinoflagellates (Domingues et al., 2011). Our samples show a linear tendency between phosphates in the upper water column and cyst concentrations (Fig. 8b), altough not between sea surface nitrates and cyst concentrations (Fig. 8c). This contrast with previously published work done on subtropical ocean off west Africa (Bouimetarhan et al., 2009), where variance of nitrate concentrations relates significantly to dinocysts distribution, while phosphate concentrations do not relate significantly to the distribution.

Salinity– The stratification/turbulence of the upper water column can effect the salinity,

which influences cell growth, cell dispersion, cyst formation and encystment and excystment of certain species (Figueroa et al., 2011) with drastic effects for some species (Wefer et al., 1999), however, in general, dinoflagellates are tolerant to low salinity (de

19

Vernal et al., 2007). In this study, we found a correlation between salinity and temperature, with high temperatures tied to high salinity and viceversa (Fig. 8e) whose values show important variation over both localities, and influence the cyst distribution of some useful species allowing to estimate changes in salinity and freshwater discharge (e.g. the relation of Brigantedinium spp., O. centrocarpun sensu Wall et Dale and S. achomosphaera with high SSS content and Echinidinium aculeatum and Bitetactodinium spongium with low values of SSS.

Fig. 8. Boxplot and smoooth regressions of dinocyst concentrations with

oceanographical sea surface variables. Caribbean and Pacific dinocyst concentrations (a), phosphates (SSP) (b) and salinity (SSS) (c).

5.3 Future perspectives

In future studies, it will be useful to explore other non-linear relations between cyst

concentrations and environmental variables in order to have a better understanding of the effect of each variable on dinocyst concentrations, improve data resolution, and date the sediments to know the exact time period studied and thus establish quantitative relationships between variables and communities dinoflagellates (transfer functions). Furthermore, it will be important to relate cyst abundance with sediment characteristics and compare it in detail with terrestrial palynomorph studies.

The comparison of our results with the analysis of ancient sediments can allow us to

understand allopatric separation in the Pacific Ocean and Caribbean Sea and understand the environmental preference in the region, as well as trace the fossil record of dinocysts in order to contribute to the discussion of the new hypothesis on the closure of the Isthmus of Panama (Montes et al., 2015), track the ecological niche of dinocysts in the past, and reconstruct past currents and climatic changes, among other applications.

6. Conclusions

20

This study provides information on the distribution of organic-walled dinoflagellate cysts

from recent sediments of the Caribbean Sea and eastern tropical Pacific Ocean. Statistical analyses allow a distinction between assemblages from the Caribbean and Pacific regions. The main environmental parameters controlling cyst assemblages are location, phosphates, and SSS. Cyst distribution reflects hydrographic regimens related to river discharge. The present study shows that dinocyst association reflects upper water conditions such as salinity and nutrient content. This indicates that dinocyst assemblages in a region are a tool for establishing reconstructions of past climates. The species reported are not potentially toxic dinoflagellates. The relation of organic-walled dinocyst assemblages with sea parameters is complex, therefore, it is necessary to statistically explore more parameters, such as sediment characteristics, water turbulence, and transport related to currents, as well as human activities near the coast, in order to be more precise on the composition and concentration in the region.

Our work provides information to understanding equatorial dinocyst ecology and

complementing the Atlas of modern dinoflagellate cyst distribution based on 2405 data points (Zonneveld et al., 2013) for the Neotropical region.

Table 5.

21

Relative abundance of phototrophic and heterotrophic specimens (%), dinoflagellate cyst concentrations (cysts/cm3), pollen grain concentrations (grains/cm3), fern spore concentrations (spores/cm3), and foraminiferal organic lining concentrations (linings/cm3).

Sample number

Phototrophic %

Heterotrophic %

Cyst concentration

Pollen concentration

Spore concentration

Linings concentration

1 11.1 88.89 61 421 139 868

2 18.8 81.25 213 533 107 224

3 12.5 87,50 509 632 308 231

4 14.3 85.71 326 465 295 124

5 0 100 51 89 79 135

6 78.6 21.43 639 3566 114 1037

7 20 80 889 3073 473 3227

8 40 60 220 958 142 610

9 34.5 65.52 1039 2688 397 11455

10 25.0 75 1632 3146 505 3650

11 15.6 84.38 493 1980 184 3341

12 0 100 1103 11266 58 3775

13 67 33.03 3206 1625 546 1481

14 52.6 47,.7 2174 1076 399 898

15 19.3 80.8 505 715 255 155

16 66.5 33.46 4230 3320 3257 3257

17 44.7 55.32 1951 2353 1243 2085

18 44,3 55.65 2547 5661 2417 1437

19 45.9 54,10 1465 1198 753 1028

20 30.3 69.74 1656 2786 943 1360

21 32.5 67.52 2069 2977 761 1736

22 19.8 80.23 606 345 268 394

23 62 38.04 1630 5314 4145 1541

24 31.1 68.94 2912 4148 1765 684

25 15 85 2195 5377 2112 1865

26 23.7 76.27 2850 2932 1612 456

27 14.6 85.37 2531 4522 2157 1286

28 21.3 78.72 6036 5608 2397 3938

29 17.8 82.18 2548 8082 2136 849

30 34.6 65.43 4211 5115 723 1550

31 37.9 62.12 5609 4079 935 5439

32 35.5 64.46 3008 2345 1020 7054

33 22.3 77.66 4224 2338 373 3105 34 24.3 75.70 2408 3283 1094 963

22

Acknowledgements

This contribution is part of the MSc studies of the first author. Financial support was provided by Colciencias project 1240–569–34181 and Proyecto Semilla Fac. Ciencias Uniandes. We want to thank the Instituto Colombiano de Petroleo (ICP), Laboratorio Biología Marina (BIOMAR) Uniandes, Lamont–Duherty Earth Observatory (LDEO), Ocean Drilling Program (ODP, OIDP), and EAFIT University for providing samples. We are grateful to Jorge Salgado for his assistance, M. Jimena Giraldo, Julio C. Avila, Simon Quintero, and Andrea González for their support. Special thanks to Manuel Páez for helping us with the dinocyst identifications. We gratefully acknowledge Andres Pardo and Susana Caballero for their useful comments to the manuscript.

23

Fig. 9. The ratio of terrestrial (pollen grains + fern spores) to marine (organic-walled dinocysts

+ organic forams linings) (a), pollen grains (b), fern spores (c), and organic forams linings (d). Relative abundances of Bitetactodinium spongium (e), Brigantedinium spp. (f), Echinidinium aculeatum (g), and Aff. Echinidinium sp. (h). Black circles denote the location of the 34 surface sediment samples studied.

24

Fig. 10. Relative abundances of Aff. Lingulodinium machaerophorum (a), Nematosphaeropsis

labyrintus (b), Opeculodinium centrocarpum–isrraelianum? (c), Opeculodinium centrocarpum senso estricto (d), Cief. Cyst of Polykricos schwartzii–kofoid? (e), Selenopemphix nephroides (f), Spiniferites spp. (g) and Spiniferites pachydermus (h) Black circles denote the location of the 34 surface sediment samples studied.

25

Table 6. Coefficient of correlation between environmental parameters and the scores of the first two axes of the redundancy analysis. Parameter abbreviations are: water depth (WD), distance to coast (DC), sea surface temperature (SST), sea surface salinity (SSS), sea surface oxygen (SSO), sea surface phosphates (SSP), sea surface nitrates (SSN). Bold numbers correspond to the best correlation between parameters and axes.

Table 7. Scores of dinocyst taxa to the first two axes of the redundancy analysis. Bold numbers correspond to taxa best correlated to the axes.

Dinocyst taxa RDA1 RDA2

Bitectatodinim spongium 0,48077501 -0,028087752 Spiniferites pachydermus -0,0516438 -0,323047236 Spiniferites spp. -0,14279932 -0,025741411 Aff. Lingulodinium machaerophorum 0,30117433 -0,095916267 Opeculodinium centrocarpum senso estricto 0,04979888 -0,005027605

Opeculodinium centrocarpum-isrraelianum? -0,15919742 0,026264491 Nematosphaeropsis labyrintus 0,11097117 -0,030447556 Brigantedinium spp. -0,25832422 0,064548294 Selenopemphix nephroides 0,12030055 0,005883029 Echinidinium aculeatum 0,52691539 0,046207506 Cief. Cyst of Polykricos schwartzii-kofoid? 0,15600549 0,111319402

Aff. Echinidinium sp. 0,06378092 0,064209559

Environmental parameters

RDA1 RDA2

WD -0,058182 -0,32929

DC -0,007886 -0,64441

SST -0,444805 -0,38027

SSS -0,733505 -0,07877

SSO 0,355449 -0,35351

SSP 0,895666 0,18467

SSN 0,438071 0,3929

Localiton (Caribbean/Pacific)

0,945186 0,08283

26

References

Anderson, D., Hoagland, P., Kaururu, Y., White, A., 2005. Estimated annual economic impacts from harmful algal blooms (HABs) in the US. Woods Hole Oceanogr. Institute, Woods Hole, MA.

Bouimetarhan, I., Marret, F., Dupont, L., Zonneveld, K., 2009. Dinoflagellate cyst distribution in marine surface sediments off West Africa (17-6ºN) in relation to sea-surface conditions, freshwater input and seasonal coastal upwelling. Mar. Micropaleontol. 71, 113–130.

Bujak, J., Downie, C., Eaton, G.L., Williams, G.L., 1980. Dinoflagellate cysts and acritarchs from the Eocene of southern England. Spec. Pap. Palaeontol. 24, 1–22.

Bütschli, O., 1873. Einiges über Infusorien. Arch. für Mikroskopische Anat. 9, 657–678. Dale, B., 2001. The sedimentary record of dinoflagellate cysts  : looking back into the future

of phytoplankton blooms. Sci. Mar. 65, 257–272. De Vernal, A., Henry, M., Bilodeau, G., 1999. Techniques de préparation et dànalyse en

micropaleontologie. Les Cahiers du GEOTOP, 28. De Vernal, A., Rochon, A., Radi, T., 2007. Dinoflagellates. Paleoceanography 1652–1667. De Vernal, A., Rochon, A., Turon, J.L., Matthiessen, J., 1997. Organic-walled dinoflagelate

cysts: palinological tracers of sea-surface conditions in middle to high latitude marine environments. Geobios 30, 905–920.

Devillers, R., De Vernal, a., 2000. Distribution of dinoflagellate cysts in surface sediments of the northern North Atlantic in relation to nutrient content and productivity in surface waters. Mar. Geol. 166, 103–124. d

DINOFLAG2, 2015. DINOFLAJ2. URL http://dinoflaj.smu.ca/wiki/Main_Page (accessed 1.1.15).

Domingues, R., Anselmo, T., Barbosa, A., Sommer, U., Galvao, H.., 2011. Nutrient limitation of phytoplankton growth in the freshwater tidal zone of a turbid, Mediterranean estuary. Estuarine. Coast. Shelf Sci. 91, 282–297.

Figueroa, R., Vasquez, J., Massanet, A., Murado, M., Bravo, I., 2011. Interactive effects of salinity and temperature on planozygote and cyst formation of Alexandrium minutum (Dinophyceae) in culture. J. Phycol. 47, 13–24.

Furio, E.F, Azanza, R. V., Fukuyo, Y., Matsuoka, K. 2012. Review of geographical distribution of dinoflagellate cysts in Southeast Asian coast. Coast. Mar. Sci 35, 20–33.

Gilbert, P., Anderson, D., Gentien, P., Granéli, E., Sellner, K.., 2005. The global, complex phenomenaof harmful algal blooms. Oceanography 18, 136–147.

González, C., Urrego, L.E., Martínez, J.I., 2006. Late Quaternary vegetation and climate change in the Panama Basin: Palynological evidence from marine cores ODP 677B and TR 163-38. Palaeogeogr. Palaeoclimatol. Palaeoecol. 234, 62–80.

Head, M.J., 2007. Last Interglacial (Eemian) hydrographic conditions in the southwestern Baltic Sea based on dinoflagellate cysts from Ristinge Klint, Denmark. Geol. Mag. 144, 987–1013.

Höll, C., Zonneveld, K. a F., Willems, H., 2000. Organic-walled dinoflagellate cyst assemblages in the tropical Atlantic Ocean and oceanographical changes over the last 140 ka. Palaeogeogr. Palaeoclimatol. Palaeoecol. 160, 69–90.

27

Hooghiemstra, H., Lezine, A.., Leroy, S.A.G., Dupont, L., Marret, F., 2006. Late Quaternary palynology in marine sediments: a synthesis of the understanding of pollen distribution patterns in the NW African setting. Quat. Int. 148, 29–44.

Hu, C., Montgomery, E.T., Schmitt, R.W., Muller-Karger, F.E., 2004. The dispersal of the Amazon and Orinoco River water in the tropical Atlantic and Caribbean Sea: Observation from space and S-PALACE floats. Deep. Res. Part II Top. Stud. Oceanogr. 51, 1151–1171.

Irigoien, X., Irigoien, X., Huisman, J., Huisman, J., Harris, R.P., Harris, R.P., 2004. Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429, 863–867.

Kump, L.R., Kasting, J.F., Crane, R.G., 2004. The earth system, 2 edition. ed. Pearson, Prentice-Hall.

Kunzig, R., 2007. La exploración del mar: La extraordinaria historia de la oceanografía, Laetoli, S. ed. Pamplona, España.

Lentin, J.K., Williams, G.L., 1993. Fossil dinoflagellates: index to genera and species. Am. Assoc. Stratigr. Palynol. Contrib. Ser. 28.

Limoges, A., Kielt, J.F., Radi, T., Ruíz-Fernandez, A.C., de Vernal, A., 2010. Dinoflagellate cyst distribution in surface sediments along the south-western Mexican coast (14.76° N to 24.75°N). Mar. Micropaleontol. 76, 104–123.

Limoges, A., Londeix, L., de Vernal, A., 2013. Organic-walled dinoflagellate cyst distribution in the Gulf of Mexico. Mar. Micropaleontol. 102, 51–68.

Maher, J. L. J. 1981. Statistics for microfossil concentration measurements employing samples spiked with marker grains. Rev. Palaeobot. Palynol. 32, 153–191.

MARUM, 2013. Center for Marine Environmental Sciences [WWW Document]. URL https://www.marum.de (accessed 1.1.15).

Montes, C., Cardona, A., Jaramillo, C., Pardo, A., Silva, J.C., Valencia, V., Ayala, C., Perez-Angel, L., Rodriguez-Parra, L., Ramirez, V., Niño, H., 2015. Middle Miocene closure of the Central American Seaway. Science 80, 348, 226–229.

Narale, D.D., Patil, J.S., Anil, A.C., 2013. Dinoflagellate cyst distribution in recent sediments along the south-east coast of India. Oceanologia 55, 979–1003.

Orlova, T.Y., Morozova, T. V, Gribble, K.E., Kulis, D.M., Anderson, M., 2004. Dinoflagellate cysts in recent marine sediments from the east coast of Russia. Bot. Mar. 47, 184–201.

Patarroyo, G., Martinez, J.I., 2013. Distribution and environmental preferences of deep sea benthic Foraminifera in the Panama basin, eastern Pacific Ocean. Caldasia 35, 311–324.

Poveda, G., Waylen, P.R., Pulwarty, R.S., 2006. Annual and inter-annual variability of the present climate in northern South America and southern Mesoamerica. Palaeogeogr. Palaeoclimatol. Palaeoecol. 234, 3–27.

Prauss, M., 2000. The oceanographic and climatic interpretation of marine palynomorph phytoplancton distribution from Mesozoic, Cenozoic and Recent sections. Geologische Institute, Universitat Gottingen, Gottingen.

R core Team, 2015. R: A language and environment for statistical computing. Reid, P., 1974. Gonyaulacacean dinoflagellate cysts from the British Isles. Nov. Hedwigia

25, 579–637. Restrepo, J., Lopez, 2008. Morphodynamics of the Paci fic and Caribbean deltas of

Colombia, South America. J. South Am. Earth Sci. 25, 1–21.

28

Restrepo, J.C., Ortíz, J.C., Pierini, J., Schrottke, K., Maza, M., Otero, L., Aguirre, J., 2014. Freshwater discharge into the Caribbean Sea from the rivers of Northwestern South America (Colombia): Magnitude, variability and recent changes. J. Hydrol. 509, 266–281.

Rochón, A., de Vernal, A., Turón, J.-L., Matthiessen, J., Head, M.J., 1999. Distribution of recent dinoflagellate cysts in surface sediments from the north Atlantic Ocean and adjacent seas in relation to sea-surface parameters. Fundation, American Association of Stratigraphic Palynologyst, Dallas, Texas.

Sarjeant, W.A., 1970. The genus Spiniferites Mantell. Grana 10, 74–78. Taylor, G., Muller-Karger, F.E., Thunell, R.C., Scranton, M.I., Astor, Y., Varela, R.,

Ghinaglia, L.T., Lorenzoni, L., Fsnning, K.A., Hameed, S., Doherty, O., 2012. Ecosystem responses in the southern Caribbean Sea to global climate change. PNAS 109, 19315–19320.

Vásquez-Bedoya, L.F., Radi, T., Ruiz-Fernández, a. C., de Vernal, a., Machain-Castillo, M.L., Kielt, J.F., Hillaire-Marcel, C., 2008. Organic-walled dinoflagellate cysts and benthic foraminifera in coastal sediments of the last century from the Gulf of Tehuantepec, South Pacific Coast of Mexico. Mar. Micropaleontol. 68, 49–65.

Vernal, A. De, Henry, M., Matthiessen, J., Mudie, P.J., Rochon, A., Boessenkool, K.P., Eynaud, F., Grosfjeld, K., Guiot, J., Hamel, D., Harland, R., Head, M.J., Kunz-Pirrung, M., Levac, E., Loucheur, V., Peyron, O., Pospelova, V., Radi, T., Turon, J.-L., Voronina, E., 2001. Dinoflagellate cyst assemblages as tracers of sea-surface conditions in the northern North Atlantic, Arctic and sub-Arctic seas: the new  ?n = 677? data base and its application for quantitative palaeoceanographic reconstruction. J. Quat. Sci. 16, 681–698.

Wall, D., 1967. Fossil microplankton in deep-sea cores from the Caribbean Sea. Paleontology 10, 95–123.

Wall, D., Dale, B., 1966. “Living fossils” in western Atlantic plankton. Nature 211, 1025–1026.

Wall, D., Dale, B., Lohmann, G., Smith, W.., 1977. The environmental and climatic distribution of dinoflagellate cysts in modern marine sediments from regions in the North and South Atlantic Oceans and adjacent seas. Mar. Micropaleontol. 2, 121–200.

Wefer, G., Berger, W., Bijma, J., Fisher, G., 1999. Use of proxies in paleoceanography. Examples from the South Atlantic. Berlin Heidelberg.

WOA, 2013. World Ocean Atlas. URL https://www.nodc.noaa.gov/OC5/woa13/woa13data.html

Zonneveld, K. a F., Marret, F., Versteegh, G.J.M., Bogus, K., Bonnet, S., Bouimetarhan, I., Crouch, E., de Vernal, A., Elshanawany, R., Edwards, L., Esper, O., Forke, S., Grøsfjeld, K., Henry, M., Holzwarth, U., Kielt, J.F., Kim, S.Y., Ladouceur, S., Ledu, D., Chen, L., Limoges, A., Londeix, L., Lu, S.H., Mahmoud, M.S., Marino, G., Matsouka, K., Matthiessen, J., Mildenhal, D.C., Mudie, P., Neil, H.L., Pospelova, V., Qi, Y., Radi, T., Richerol, T., Rochon, A., Sangiorgi, F., Solignac, S., Turon, J.L., Verleye, T., Wang, Y., Wang, Z., Young, M., 2013. Atlas of modern dinoflagellate cyst distribution based on 2405 data points. Rev. Palaeobot. Palynol. 191, 1–197. doi:10.1016/j.revpalbo.2012.08.003

Zonneveldd, K., 1997. New species of organic-walled dinoflagellate cysts from modern sediments of the Arabian Sea (Indian Ocean). Rev. Paleobotany Palynol. 97, 319–337.

29

Zonneveldd, K.A., Jurkschat, T., 1999. Bitectatodinium spongium (Zonneveld, 1997) Zonneveld et Jurkschat, comb. nov. from modem sediments and sediment trap samples of the Arabian Sea (northwestern Indian Ocean): Taxonomy and ecological affinity. Rev. Palaeobot.Palyno 106, 153–169.

Annex 1. Taxa Descriptions Genus Bitectatodinium Wilson 1973 Bitectatodinium spongium (Zonneveld) Zonneveld et Jurkschat 1998 Figs.3 a–b, 9c Characteristics: Sphaeroidal cysts, medium size, yellow-ligth. Brown. Archeopyle chasmic. Spongious and fibrous Wall. Proxime chorate whit small, thin, rounded ends and dense process. Dimensions: Body diameter: 50–71.4 µm (mean =60 µm, n=15); thickness wall: 1.4–2 µm (mean = 1.5µm, n=5); small process 3–7 µm, (mean = 5µm, n=13). Motile affinity: Unknown Stratigraphic range: Holocene-Recent Geographic distribution: Tropical to subtropical full marine upwelling areas. It is abundant in areas with anoxic and hypoxic bottom waters. Is restricted to equatorial and subtropical areas that are generally characterised by the presence of coastal upwelling. It can form up to 62.5% of the association in the eastern Pacific Ocean. Environmental parameter range: SST: 10.7–29.8 °C, SSS: 31.9–38.3 psu, P: 0.1–1.1 µmol/l, N: 0.04–8.7 µmol/l, bottom water O2: < 6 ml/l. Web References: https://www.marum.de/en/Bitectatodinium_spongium.html http://dinoflaj.smu.ca/wiki/Bitectatodinium_spongium Genus Brigantedinium Reid, 1977ex Lentin and Williams, 1993 Brigantedinium simplex Wall 1965 ex Lentin et Williams 1993 Figs. 3o, 9f Characteristics: Sphaeroidal, proximate, brown cyst, smooth surface. Intercalary Archeopile and simmetrically hexagonal. Cysts often folded Dimensions: body diameter: 48–58 µm (mean = 50 µm, n= 20); thickness wall: 1.3–1.7 µm (mean = 1.3 µm, n=10) Motile affinity: cyst Protoperidinium conicoides (Paulsen 1905) Balech 1974. Stratigraphic range: Upper Miocene-Recent Geographic distribution: species complex can be considered cosmopolitan. It has a global distribution and can form up to 99% of the association. It can dominate the association from coastal regions to the central parts of the Oceans and is observed in oligotrophic to eutrophic and brackish to hypersaline environments. Environmental parameter range: SST: -2.1–29.8 °C, SSS: 6.7–39.4 psu, P: 0.1–2.1 µmol/l, N: 0.01–30.6 µmol/l, bottom water O2: 0.01–8.2 ml/l. Web references: https://www.marum.de/en/Brigantedinium_spp..html https://www.marum.de/en/Cyst_of_Protoperidinium_conicoides.html Brigantedinium cariacoense (Wall1967) ex Lentin et Williams 1993 Figs. 3p, 9f Characteristics: Sphaeroidal, proximate, brown cyst, smooth surface. Intercalary, hexagonal archeopile. Cysts often folded. Dimensions: body diameter: 40–45 µm (mean= 43 µm, n=10); thickness wall: 1–1.2 µm (mean = 1 µm, n=10) Motile affinity: cyst Protoperidinium avellanum (Meunier 1919) Balech 1974. Stratigraphic range: Middle Miocene-Recent

30

Geographic distribution: species complex can be considered cosmopolitan. It has a global distribution and can form up to 99% of the association. It can dominate the association from coastal regions to the central parts of the Oceans and is observed in oligotrophic to eutrophic and brackish to hypersaline environments. Environmental parameter range: SST: -2.1–29.8 °C, SSS: 6.7–39.4 psu, P: 0.1–2.1 µmol/l, N: 0.01–30.6 µmol/l, bottom water O2: 0.01–8.2 ml/l. Web references: https://www.marum.de/en/Brigantedinium_spp..html http://dinoflaj.smu.ca/wiki/Brigantedinium_cariacoense Genus Echinidinium Zonneveld, 1997 ex Head et al., 2001* Echinidinium aculeatum Zonneveld 1997 Figs. 3 s–t, 9g Characteristics: Sphaeroidal, chorate, dark yellow-brown cyst with abundant randomly distributed large spines. Spines are tapering towards their distal ends. Chasmic arqueopile. Dimensions: body diameter: 19–32 µm (mean = 26.2µm, n=10); thickness wall: 1–1.3 µm (mean = 1.2 µm, n=15); process 4.4–6.9 µm, (mean = 5.5 µm, n=14); Motile affinity: Unknown Stratigraphic range: late Pleistocene to Recent. Geographic distribution: mesotrophic/eutrophic temperate to equatorial species occurring only in regions with unstratified upper waters. It is not observed in areas with well-ventilated bottom waters. With the exception of a few sites, E. aculeatum is restricted to the coastal regions of temperate to equatorial regions. Environmental parameter range: SST: 7.8–29.8 °C, SSS: 26.8–38.5 psu, P: 0.1–1.1 µmol/l, N: 0.4–9.6 µmol/l, bottom water O2: 0.3–6.1 ml/l. Web references: http://dinoflaj.smu.ca/wiki/Echinidinium_aculeatum https://www.marum.de/en/Echinidinium_aculeatum.html * This name was not validly published in Zonneveld (1997) due that author did not provide a Latin diagnosis. Type: Zonneveld, 1997. Aff. Echinidinium sp. Figs. 3 u–v, 9h Characteristics: Spheroidal cysts, small size, dark brown color, proximate with numerous hollow acuminate processes. Dimensions: body diameter: 42–46 µm (mean = 44µm, n=7); thickness wall: 1 µm (mean = 1 µm, n=5), process 7–9 µm, (mean = 8 µm, n= 20). Motile affinity: Unknow Stratigraphic range: Unknow Geographic distribution: Unknow Environmental parameter range: Unknow Genus Lingulodinium Wall 1967 emend. Dodge 1989 Aff. Lingulodinium machaerophorum (Deflandre & Cookson 1955) Wall 1967 Figs. 3 g–h, 10a. Characteristics: Spherical, chorate cyst , médium size, transparent with a microgranulate to granulate wall. Thin, large and abundant process with acute ends. Dimensions: Body diameter: 34–87 µm (mean =52,1 µm, n=20); thickness wall: 1.2–1.5µm (mean =1.3 µm, n=10). process 12–18 µm, (mean = 14,6 µm, n=16). Motile affinity: Lingulodinium polyedrum (von Stein 1883) Dodge 1989 Stratigraphic range: Upper Paleocene to Recent. Geographic distribution: Can be found in temperate to equatorial environments with temperatures above 10°C in summer and 0°C in winter. It is observed in regions with a broad salinity range. Is restricted to temperate to equatorial regions of the northern hemisphere and subtropical - equatorial regions of the Southern Hemisphere with the arctic and antarctic subtropical fronts forming its northern and southern distribution boundary, respectively.

31

Environmental parameter range: SST: 0–29.8 °C, SSS: 8.5–39 psu, P: 0.06–1.1 µmol/l, N: 0.04–12.0 µmol/l bottom water O2: 0.3–7.2 ml/l. Web References: https://www.marum.de/en/Lingulodinium_machaerophorum.html http://dinoflaj.smu.ca/wiki/Lingulodinium_machaerophorum Genus Nematosphaeropsis Deflandre &Cookson 1955 Nematosphaeropsis labyrinthus (Ostenfeld 1903) Reid 1974 Figs. 3 m–n, 10a Characteristics: Ovoid, chorate cyst with central body and smooth processes joined, trabeculate, médium size,. Archeopyle is precingular Dimensions: Body diameter: 40–45 µm (mean = 42µm, n= 5); thickness wall: 1µm (mean = 1µm, n=5) process 10–15 µm, (mean = 12µm, n= 10). Motile affinity: Gonyaulax spinifera (Claparède et Lachmann 1859) Diesing 1866. Stratigraphic range: lower Oligocene to Recent. Geographic distribution: Occurs world-wide from the arctic to the equator in full-marine eutrophic to oligotrophic environments. Cosmopolitan species that can be present in high relative abundances in sediments of eutrophic as well as oligotrophic environments. Environmental parameter range: SST: -2.1–29.8 °C, SSS: 25.8–39 psu, P: 0.06–1.9 µmol/l, N: 0.01–26.5 µmol/l, bottom water O2: 0–8.2 ml/l. Web references: https://www.marum.de/en/Nemaosphaeropsis_labyrinthus.html http://dinoflaj.smu.ca/wiki/Nematosphaeropsis_labyrinthus Genus Opeculodinium Wall, 1967 Emend. Matsuoka et al., 1997 Opeculodinium centrocarpum senso estricto Figs. 3 i–j, 10b. Characteristics: Spherical, chorate cysts with fine acute processes, transparent with microgranular wall. Simple process with conical bases and acuminate terminations. Precingular archeopyle. Dimensions: Body diameter: 38–42µm (mean = 40µm, n=13); thickness wall: 1.3–1.6 µm (mean = 1.2 µm, n= 13). process 8.5–9.5 µm, (mean = 9µm, n=25). Motile affinity: Protoceratium reticulatum (Claparède et Lachmann 1859) Bütschli 1885. Stratigraphic range: Eocene to Recent. Geographic distribution: From the polar to equatorial regions and coastal to open oceanic sites. Environmental parameter range: SST: -2.1–29.8 °C, SSS: 9.8–39.4 psu, P: 0.06–1.87 µmol/l, N:, 0.01–25.99 µmol/l, bottom water O2: 0.01–8.2 ml/l. Web references: https://www.marum.de/en/Operculodinium_centrocarpum.html http://dinoflaj.smu.ca/wiki/Operculodinium Opeculodinium centrocarpum-isrraelianum? Figs. 3 k–l, 10c. Characteristics: Spherical, chorate cysts with hollow processes, transparent with microgranular wall. Simple process with conical bases and rounded terminations. Dimensions: Body diameter: 62–70 µm (mean = 63 µm, n=10); thickness wall: 1.2–1.5 µm (mean = 1.2 µm, n= 10). process 12 µm, (mean = 11 µm, n= 30). Motile affinity: Possibly Protoceratium (Claparède et Lachmann 1859) Bütschli 1885. Stratigraphic range: Pleistocene to Recent. Geographic distribution: Restricted to subtropical, tropical and equatorial regions Environmental parameter range: STT: 1.8–29.8 °C, SSS: 30.3–39 psu, P: 0.06–1.67 µmol/l, N: 0.04–20.86 µmol/l, bottom water O2: 0.01–6.6 ml/l. Web references: https://www.marum.de/en/Operculodinium_israelianum.html

32

http://dinoflaj.smu.ca/wiki/Operculodinium_israelianum Genus Polykricos Bütschli, 1873. Cief. Cyst of Polykricos schwartzii-kofoid? Figs. 3 x–y, 10e Characteristics: Oval cysts, médium size, light to dark brown with rugulate surface, proximochorate, hollow proces with varible shapes, apical archeopile. Dimensions: body diameter: 49–65 µm (mean = 54µm, n=8); thickness wall: 1 µm (mean = 1µm, n=12), process 6–8 µm, (mean = 7 µm, n= 20). Motile affinity: Polykrikos schwartzii Stratigraphic range: Polykrikos schwartzii Geographic distribution: In coastal temperate to equatorial environments. Only in the Pacific Ocean is occurs also in high latitudes Environmental parameter range: SST: -1.6–29.4 °C, SSS: 16.7–38.7 psu, P: 0.07–1.63 µmol/l, N: 0.18–18.5 µmol/l, bottom water O2: 0.8–8.2 ml/l. Web references: https://www.marum.de/en/cyst_of_Polykrikos_schwartzii.html http://dinoflaj.smu.ca/wiki/Polykrikos Genus Selenopemphix Benedek, 1972 emend Bujak in Bujak et al., 1980 Selenopemphix nephroides (Benedek 1972) Benedek et Sarjeant, 1981 Figs. 3q–r, 10f Characteristics: Sphaeroidal cysts, médium size, light brown with smooth surface. Dimensions: body diameter: 50–60 µm (mean = 55µm, n= 7); thickness wall: 1–1.5 µm (mean = 1.2 µm, n=6). Motile affinity: Protoperidinium subinerme (Paulsen 1904) Loeblich III 1970. Stratigraphic range: Middle Eocene-Recent. Geographic distribution: Temperate to equatorial regionns. Environmental parameter range: SST: -0.8–29.8 °C, SSS: 27.6–39.4 psu, P: 0.06–1.7 µmol/l, N: 0.4–17.9 µmol/l, bottom water O2: 0–7.2 ml/l. Web references: https://www.marum.de/en/Selenopemphix_nephroides.html http://dinoflaj.smu.ca/wiki/Selenopemphix_nephroides Genus Spiniferites Mantell 1850 emend. Sarjeant 1970 Spiniferites pachydermus (Rossignol 1964) Reid 1974 Figs. 3 c–d, 10h Characteristics: Sphaeroidal, proximochorate, transparent cyst with smooth surface. Cavate, with thin, tuberculate, end rounded process. Gonal process with a microgranulate to reticulate wall Archeopyle is precingular. Reticulate to microgranulate surface Dimensions: Body diameter: 44–51µm (mean = 49 µm, n= 10); thickness wall: 1–1.5 µm (mean = 1.3 µm, n=5). ). Process 9–11 µm, (mean = 11 µm, n= 15). Motile affinity: Probably a cyst of Gonyaulax spp. Stratigraphic range: Pleistocene to Recent. Geographic distribution: Temperate to equatorial mainly coastal distribution restricted to full marine environments with relatively high upper water nitrate concentrations and bottom waters that are well ventilated. Highest relative abundances occur in mesotrophic to eutrophic environments in upwelling regions in the vicinity of upwelling cells. Is restricted to temperate to equatorial coastal regions along the margins of the Atlantic Oceans, Mediterranean Sea, Arabian Sea and northwestern Pacific Environmental parameter range: SST: 0–29.0 °C, SSS: 27.8–39.0 psu, P: 0.06–1.00 µmol/l, N: 0.2–12.0 µmol/l, bottom water O2: 1.1– 6.0 ml/l.

33

Web References: http://dinoflaj.smu.ca/wiki/Spiniferites_pachydermus https://www.marum.de/Page5169.html

Documents

Spatial distribution of organic-walled dinoflagellate