Seasonal and interannual dynamics in diatom production in the Cariaco Basin, Venezuela

ARTICLE IN PRESS Deep-Sea Research I 56 (2009) 571–581

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Seasonal and interannual dynamics in diatom production in the Cariaco Basin, Venezuela Oscar E. Romero a,, Robert C. Thunell b, Yrene Astor c, Ramon Varela c a b c

Instituto Andaluz de Ciencias de la Tierra (IACT-CSIC), Campus Fuentenueva, Facultad de Ciencias, Universidad de Granada, 18002 Granada, Spain Department of Geological Sciences, University of South Carolina, Columbia, SC 29208, USA ´n La Salle de Ciencias Naturales, Estacio ´n de Investigaciones Marinas de Margarita, Porlamar 6318, Venezuela Fundacio

a r t i c l e in fo

abstract

Article history: Received 7 July 2008 Received in revised form 4 December 2008 Accepted 21 December 2008 Available online 25 December 2008

We examine the diatom flux collected between November 1996 and April 1998, and between January and October 1999 at the time-series study site in the Cariaco Basin, off Venezuela. The temporal dynamics of the total diatom flux mainly reflect seasonal, trade wind-driven changes in surface hydrographic conditions, including changes associated ˜ o/Southern Oscillation (ENSO). Highest diatom fluxes (41.8  107 valves with the El Nin m2 d1) coincided with the upwelling season in boreal winters 1997 and 1999. Changes in the composition of the diverse diatom community reflect variations in hydrographic and atmospheric conditions, as well as nutrient availability. Cyclotella litoralis, a neritic diatom typical of nutrient-rich waters, along with resting spores of several Chaetoceros spp., dominate during periods of high diatom flux, following trade wind-driven upwelling. During the boreal summers of 1997 and 1999, nutrient-depleted surface waters resulted in low diatom fluxes (o5.2  106 valves m2 d1). The seasonal pattern of high diatom production was altered from July 1997 through April 1998, when the ENSO affected the Caribbean Sea. The occurrence of ENSO during boreal winter 1997–1998 caused a major change in the qualitative composition of the diatom assemblage: the highly diverse diatom assemblage was composed of a mixture of pelagic (Nitzschia bicapitata, Thalassionema nitzschioides var. inflata, T. nitzschioides var. parva, Azpeitia tabularis) and coastal species (C. litoralis, resting spores of Chaetoceros, T. nitzschioides var. nitzschioides). The simultaneous occurrence of neritic and openocean diatoms during boreal summers reflects the fact that the Cariaco Basin is influenced by both offshore and coastal waters, with considerable short-term variability in hydrographic conditions and nutrient availability. & 2008 Elsevier Ltd. All rights reserved.

Keywords: Cariaco Basin Diatoms Particle fluxes Caribbean Sea Upwelling Intertropical Convergence Zone

1. Introduction Sediment trap-based studies are useful for determining species-specific ecological tolerances of various plankton groups and for assessing the potential of these groups for paleoceanographic reconstructions (Deuser and Ross, 1989; Thunell and Sautter, 1992; Romero et al., 1999,

 Corresponding author. Tel.: +34 95 824 3360; fax: +34 95 824 3384.

E-mail address: [email protected] (O.E. Romero). 0967-0637/$ - see front matter & 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2008.12.005

2002a, b; Ziveri and Thunell, 2000; Tedesco and Thunell, ˜ iga et al., 2007). Since late 2003; Ba´rcena et al., 2004; Zu´n 1995, a time-series study has been underway in the Cariaco Basin, off Venezuela, that has examined seasonal to interannual changes in hydrography, primary production, sediment fluxes, and water column recycling, and how changes in these processes are preserved in seafloor ˜ i et al., 2003). sediments (Muller-Karger et al., 2001; Gon In particular, observations carried out as part of the Cariaco Basin ocean time-series have provided important insights into the temporal variability and composition of

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the particle fluxes and how this relates to local climate ˜ i et al., 2003). forcing (Thunell et al., 2000, 2007; Gon Thunell et al. (2000) measured organic carbon fluxes in the anoxic water column under varying levels of primary productivity and concluded that 1–2% of the organic carbon produced at the surface of the Cariaco Basin ˜ i et al. (2003) showed reaches the underlying seafloor. Gon the close temporal correlation between the export of biogenic sediment components with the upwelling regime and primary productivity in the upper water column. More recently, Tedesco et al. (2007) studied the seasonal variability of the stable oxygen isotope signal on six species of sediment-trapped planktonic foraminifera and their usefulness as a proxy for the reconstruction of paleotemperatures in the Cariaco Basin. Martinez et al. (2007) used variations in chemical composition of particle fluxes to unravel how present day seasonal migration of the Intertropical Convergence Zone (ITCZ) influences the contribution of terrigenous material from different source regions. Together, these studies accurately describe the variability in the production and composition of the sediment flux in the Cariaco Basin on both a seasonal and interannual basis. This information provides a basis for using the sedimentary record to better reconstruct past oceanographic conditions in the Caribbean region. A significant part of the ocean’s total primary production is provided by diatoms (Tre´guer et al., 1995; Ragueneau et al., 2000). Regardless of the location, there is a general trend for the relative abundance of diatoms to increase as primary production increases (Ragueneau et al., 2000). Tre´guer et al. (1995) suggested that diatoms may constitute up to 75% of the total standing stock in coastal zones and other nutrient-rich systems. Since diatoms account for a major part of the production and flux of biogenic silica (BSi, opal) (Ragueneau et al., 2000), time-series studies of diatom fluxes can be used to improve models of the biogeochemical cycle of BSi (Romero et al., 1999) and the understanding of the silicate pump model (Dugdale et al., 1995). Sediment trap studies have demonstrated that the production and the sedimentation of diatoms in the surface ocean are markedly seasonal and episodic, and can be related to biological and hydrographic processes in the surface waters (e.g., Ba´rcena et al., 2004; Fischer et al., 2002; Romero et al., 1999, 2000, 2001, 2002a, b). Long-term data on diatom fluxes provide valuable information on potential effects of climate change on diatom production and the changes in the composition and export of their assemblages (Fischer et al., 2002; Romero et al., 2000, 2002b). In this work, we examine the variability in diatom fluxes in the Cariaco Basin from November 1996 through April 1998 and between January and October 1999. A central objective of our study was to determine the seasonal and interannual variability in the timing, magnitude and composition of diatom fluxes. We demonstrate that qualitative and quantitative variations in the diatom assemblage are related to prevailing hydrographic and nutrient conditions in the Cariaco Basin and follow the annual cycle of winter (high)/summer(low) productivity. Our results will help in the interpretation of the diatom

community preserved in the surface and downcore sediments of the Cariaco Basin.

2. Oceanographic setting The Cariaco Basin (Fig. 1A) is a 1400-m deep depression off the Venezuelan central coast composed of two sub-basins that are separated by a saddle that rises up to 900 m. The basin, which acts as natural sediment trap within the continental shelf (Richards, 1975), is connected with the south Caribbean Sea above a shallow (100 m) sill and through two channels, the 135 m deep Canal de la Tortuga located to the northeast and the narrower and deeper (146 m) Canal Centinela. The sill and relatively shallow channels restrict the circulation of deep water in the Cariaco Basin. Because of this restricted circulation, the decomposition of organic material sinking from the surface has led to the complete consumption of dissolved oxygen within the bottom waters, resulting in anoxia below approximately 275 m (Deuser, 1973). Upwelling, induced by E-NE trade winds and western boundary surface currents, drives the annual production cycle in the Cariaco Basin (Herrera and Febres-Ortega, 1975; Muller-Karger and Aparicio-Castro, 1994). As the latitude of the ITCZ migrates from its northern to its southernmost position, strong E-NE trade winds develop from December to April along the northern coast of Venezuela (Fig. 1B). Surface Ekman transport induced by these steady winds causes an upward migration of the thermocline along the east–west-oriented continental margin off the Venezuelan coast, bringing nutrients from deeper waters to the surface. During the summer/fall rainy season, the ITCZ migrates north (Fig. 1B), causing winds to become weaker and upwelling to greatly diminish or cease. This seasonal cycle of upwelling is clearly illustrated in the upper water column temperature record for our study period (Fig. 2). The source of the upwelled water in the Cariaco Basin is Subtropical Underwater (SUW), which in this part of the Caribbean margin lies shallower than 150 m and is characterized by a salinity of 36.85% (Morrison and Smith, 1990). Surface salinity at the CARIACO time-series site changes seasonally, from greater than 36.8 in January–July to less than 36.6 during the rainy season between August and November (Astor et al., 2003). Surface waters in the basin originate in the North Equatorial and Guyana Current systems and enter the eastern Caribbean through the Lesser Antilles (Gordon, 1967). Caribbean Surface Water flows into the Cariaco Basin between Cabo Codera and the Tortuga Bank in the west and between Tortuga, Margarita Island and the Araya Peninsula at the eastern end of the basin (Richards and Vaccaro, 1956). Water from the Amazon and Orinoco Rivers may be transported by the North Equatorial and Guyana currents (Froelich et al., 1978) into the Caribbean but are thought to have little influence on the hydrography of the Cariaco Basin (Muller-Karger et al., 1989). Input from local rivers varies seasonally and has a greater impact on the hydrography of the basin. These rivers are

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120˚W

90˚W

60˚W

North America

30˚S Atlantic Ocean

20˚N

Cariaco Basin Venezuela

0˚

573

ITCZ

30´

Summer

ITCZ Winter

1500 1000 500

South America

Plataformade Margarita

Pacific Ocean

Banco dela Tortuga

20˚S

11˚N

0 I.Cubagua Silla Central

Cabo Codera

arita

25

125 10 0 00

0 75

1350

Islade Marg

135

0 CARIACO 30´

Cumana

Plataforma de Unare

La Ta gun ca ad rig e ua

Pto.LaCruz

Laguna Unare de 66˚W

30´

10˚N 65˚W

30´

64˚W

Fig. 1. (A) Location of the Cariaco Basin sediment trap time-series study site (inverted black triangle). (B) Seasonal latitudinal migration of the Intertropical Convergence Zone (ITCZ; Hastenrath and Greishar, 1993).

Fig. 2. Plot of temperature for the top 200 m of the water column at the Cariaco Basin sediment trap time-series study site. Data based on the monthly ´s. Temperature data were averaged at 1-m intervals from the continuous CTD profiles. hydrocasts performed from the R/V H. Gine

the major source of terrigenous sediment delivery to the basin today (Martinez et al., 2007).

3. Material and methods A single mooring containing four automated sediment traps (Honjo and Doherty, 1988) has been deployed continuously on the eastern side of the Cariaco Basin

(101300 N, 641400 W; Fig. 1A) at a depth of approximately 1400 m (Thunell et al., 2000; Fig. 1A) since November 1995. The traps are positioned at four different depths: trap A at 275 m, just above the oxic/anoxic interface, trap B at 455 m, trap C at 930 m and trap D at 1200 m. For this study, we used samples from traps A and B. We assume that the diatom assemblage did not differ significantly between both traps, since valve dissolution predominantly occurs in the upper 500 m of the water

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column (Tre´guer et al., 1995; Ragueneau et al., 2000). Each sediment trap contains 13 sampling cups and is programmed to collect samples continuously at 2-week intervals. The mooring is recovered and redeployed every 6 months. A buffered formalin solution is placed in each sample cup prior to deployment in order to minimize post-depositional degradation of the organic matter. After collection, samples are stored in sealed containers and kept refrigerated until analyzed. Prior to analyses, samples are thoroughly washed with distilled water to remove excess formalin and carefully examined under the microscope to remove swimmers that are not part of the particle flux (Thunell et al., 2000). For this study either 1/16 or 1/64 splits of the original samples were used. Samples were rinsed with distilled water and prepared according to the methodology described in Romero et al. (1999, 2000). Diatom and silicoflagellate analyses were carried out on permanent slides of acid-cleaned material (Mountex mounting medium). Qualitative and quantitative analyses were done at 1000  magnifications using a Zeiss-Axioscope with phase-contrast illumination. Several traverses across the cover slip were examined, depending on abundance (between 400 and 750 valves per cover slip were counted). Each diatom was identified to the lowest taxonomic level possible. Silicoflagellates were only identified at group level. Counting of two replicate slides indicated that the analytical error for the diatom and silicoflagellate flux estimates is p15%. The resulting counts yielded estimates of relative abundances of individual diatom taxa as well as daily fluxes of diatom valves and silicoflagellate skeletons m2 d1 calculated according to Sancetta and Calvert (1988), as follows: F¼

½N½A=a½V½Split ½days½D

where [N] number of specimens (valves), in an area [a], as a fraction of the total area of Petri dish [A] and the dilution volume [V] in ml. This value is multiplied by the sample split [Split], representing the fraction of total material in the trap, and then divided by the number of [days] of deployment and the trap collection area [D]. 4. Results 4.1. Seasonal and interannual variations in diatom fluxes The BSi flux in the Cariaco Basin is composed of diatoms, silicoflagellates, radiolarians, phytoliths and the dinoflagellate Actiniscus pentasterias, with diatoms dominating the BSi fraction throughout the year. Diatom fluxes were always one to four orders of magnitude higher than that of the other siliceous organisms. The daily flux of diatoms ranged between 1.8  105 and 4.3  107 valves m2 d1 (average ¼ 7.0  106 valves m2 d1) (Fig. 3, Table 1). Diatoms occurred in greatest numbers during late March–mid-April 1997 (1.4–2.6  107 valves m2 d1) and mid January/late February 1999 (3.8–4.3  107 valves m2 d1), and March/April 1999 (3.2–3.7  107 valves m2 d1). Secondary maxima occurred in late May 1997

(8.1 106 valves m2 d1), mid-July 1997 (8.4  106 valves m2 d1), and in June 1999 (1.1–1.7  107 valves m2 d1) (Fig. 3; Table 1). Silicoflagellates were the second most abundant siliceous plankton group and their fluxes were highest between January and June 1999 (total range ¼ 4.6  103 and 2.4  106 skeletons m2 d1; 5 average ¼ 2.3  10 skeletons m2 d1). The flux of opal (biogenic silica) ranges 0.01–0.032 g m2 d1 and peaked in early March, late May–early June, and late November– mid-December 1997. Secondary opal maxima occurred in ˜ i et al., 2003). late April–early May 1999 (Gon 4.2. Qualitative and quantitative changes in the diatom assemblage The highly diverse diatom assemblage in the Cariaco Basin included ca. 160 species and varieties (Table 2). Twelve species or group of species accounted for 75% of the total diatom flux, mainly during periods of moderate to high diatom fluxes. On average, the most important contributor to the diatom flux is the coastal planktonic species Cyclotella litoralis (range of relative contribution ¼ 11–68%, average for the total trapped period ¼ 34%). Other coastal components include resting spores (RS) of Chaetoceros spp. (1.0–48.4%, average for the total trapped period ¼ 17.4%), Thalassionema nitzschioides var. nitzschioides (avg ¼ 8.5%), Skeletonema costatum (1.9%) and Thalassiosira oestrupii var. venrickae (1.5%). Open-ocean, warm-water taxa such as Nitzschia bicapitata (7.7%), Roperia tesselata (2.8%), T. nitzschioides var. inflata (1.2%), and T. nitzschioides var. parva (1.2%) contributed mainly during warmer periods. The temperate, coastal water species C. litoralis is dominant during periods of highest diatom fluxes: highest relative contribution is seen in March–April, late June through October 1997, late February through late March 1998, and February 1999 (Fig. 4). Resting spores of Chaetoceros have their highest relative contribution between May and early June 1997, and January, late March/early April, and late June/early July 1999 (Fig. 4). The highest relative contribution of T. nitzschioides var. nitzschioides occurred between October 1997 and February 1998. S. costatum peaked late January–early February 1998. Amongst the diatoms typical of warm, pelagic waters, N. bicapitata contributed mostly during periods of low surface productivity and high sea-surface temperatures: November–December 1996, early November1997–late January 1998, and mid-June–mid-October 1999 (Fig. 4). T. nitzschioides var. inflata, and T. nitzschioides var. parva also had highest contributions during boreal summers. 5. Discussion Temporal variability in the production and export of diatoms in the Cariaco Basin is primarily controlled by the seasonal cycle of primary production in the surface waters. When the ITCZ reaches its southernmost position during the boreal winter (Hastenrath and Greishar, 1993), strong E-NE trade winds enhance the upwelling of

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Fig. 3. Temporal changes in the flux of opal (g m2 d1), diatoms (valves m2 d1) and silicoflagellates (skeletons m2 d1) at the sediment trap site in the Cariaco Basin from November 1996 through April 1998, and between January and October 1999. Grey shadings highlight main periods of upwelling and ˜ o/Southern Oscillation. the cross-hatched shading highlights the secondary upwelling season. ENSO: El Nin

nutrients into surface waters; this in turn results in increased fluxes of diatoms (Fig. 3) and bulk biogenic ˜i components to the seafloor (Thunell et al., 2000; Gon et al., 2003). The ITCZ moves northward in the boreal summer, resulting in weakened E-NE trades (Astor et al., 2003), decreased input of nutrients to the surface water and reduced primary production (Muller-Karger et al., ˜ i et al., 2003). Diatom and opal fluxes reach 2001; Gon their lowest values during boreal summers off Venezuela. Although the upwelling period during the first half of 1997 was relatively long lasting (Fig. 2), diatom produc-

tion and export flux only peaked in late winter when upwelling was most intense, due to strong E-NE trade winds (Astor et al., 2003) and the rapid shoaling of cool, ˜ i et al., 2003). The diatom subsurface waters (Gon assemblage rapidly responds to the variations of the changes in the hydrographic and atmospheric conditions and nutrient availability in the Cariaco Basin. The centric diatom C. litoralis, the main component of the diatom community, dominated the community during the period of highest total diatom flux in boreal winter 1997, when primary productivity in surface waters exceeded 1 mg C

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Table 1 Summary of the main characteristics of the diatom (valves m2 d1) and silicoflagellate (skeletons m2 d1) fluxes at the study site in the Cariaco Basin, off Venezuela, from November 1996 through April 1998, and between January and October 1999. Sample number

Collection period

Trap depth (m)

Diatom flux (valves m2 d1)

Silicoflagellates (skeletons m2 d1)

3A_1 3A_2 3A_3 3A_7 3A_8 3A_9 3A_10 3A_11 3A_12 4A_1 4A_2 4A_3 4A_4 4A_5 4A_6 4A_7 4A_8 4A_9 4A_10 4A_11 4A_12 4A_13 5B_1 5B_2 5B_3 5B_4 5B_6 5B_7 5B_8 5B_9 5B_10 5B_11 5B_12 5B_13 7B_4 7B_5 7B_6 7B_7 7B_8 7B_9 7B_10 7B_11 7B_12 7B_13 8B_1 8B_2 8B_3 8B_4 8B_5 8B_6 8B_7 B 8B_9 8B_10 8B_11 8B_12 8B_13

08 Nov 1996 22 Nov 1996 06 Dec 1996 31 Jan 1997 14 Feb 1997 28 Feb 1997 14 Mar 1997 28 Mar 1997 11 Apr 1997 15 May 1997 22 May 1997 05 June 1997 19 June 1997 03 July 1997 17 July 1997 31 July 1997 14 Aug 1997 28 Aug 1997 11 Sept 1997 25 Sept 1997 09 Oct 1997 23 Oct 1997 13 Nov 1997 20 Nov 1997 04 Dec 1997 18 Dec 1997 15 Jan 1998 29 Jan 1998 12 Feb 1998 26 Feb 1998 12 Mar 1998 26 Mar 1998 09 Apr 1998 23 Apr 1998 12 Dec 1998 02 Jan 1999 16 Jan 1999 30 Jan 1999 13 Feb 1999 27 Feb 1999 13 Mar 1999 27 Mar 1999 10 Apr 1999 24 Apr 1999 6 May 1999 20 May 1999 3 June 1999 17 June 1999 1 July 1999 15 July 1999 29 July 1999 12 Aug 1999 26 Aug 1999 9 Sept 1999 23 Sept 1999 7 Oct 1999 21 Oct 1999

275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 275 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455 455

1,191,607 1,493,456 189,709 312,511 6,420,452 6,975,718 13,628,212 26,166,409 1,077,278 396,356 8,067,647 2,432,065 486,597 6,201,744 8,399,491 3,499,994 1,582,264 1,278,187 2,689,088 960,411 423,879 513,074 4,895,141 2,553,434 1,219,560 4,573,280 597,282 5,190,795 182,933 355,702 3,743,343 2,218,905 858,760 381,569 2,068,266 12,182,086 10,830,947 43,068,773 38,317,232 8,447,764 7,725,794 37,656,590 17,458,103 32,485,146 17,582,548 8,537,191 17,572,247 11,332,105 3,679,767 1,324,073 3,249,206 2,337,454 1,350,822 1,641,325 1,189,071 369,256 410,397

112,640 304,889 77,069 7622 62,248 19,761 0 0 0 0 44,206 62,628 11,382 12,281 98,240 12,281 40,312 0 21,342 0 20,749 49,044 84,691 25,407 60,978 60,977 7622 68,601 20,326 10,163 16,938 8469 0 0 536,598 497,954 231,193 863,916 609,823 50,814 317,081 762,279 436,999 2,418,727 914,699 711,433 1,638,315 965,516 46,579 4536 21,778 121,954 143,975 264,238 182,934 67,753 54,203

˜ i et al., 2003), and SST ranges between 21 m3 h1 (Gon and 27 1C (Fig. 2). A similar pattern of distribution is seen during the main upwelling period between early January and late April 1999. The weak secondary upwelling event from June through mid-August 1997 caused only a moderate

increase in the flux of diatoms. This secondary upwelling, characterized by colder SST (Fig. 2) and a local maximum of winds (Astor et al., 2003), originates from the shoaling of Cariaco Basin waters rather than being the extension of the regional upwelling that occurs earlier in the season ˜ i et al., 2003). The re-establishment of the thermal (Gon

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Table 2 The following list presents all the species, varieties or formae of diatoms (Bacillariophyceae) found in the Cariaco Basin sediment trap samples from November 1996 through April 1998 and between January and October 1998. Marine diatoms Actinocyclus curvatulus Janisch 1874 A. elongatus Grunow 1881 A. exiguus G.Fryxell & Semina 1981 A. octonarius Ehrenberg 1838 Actinoptychus senarius (Ehrenberg) Ehrenberg 1838 Adoneis pacifica G.W. Andrews & P. Rivera 1987 Alveus marinus (Grunow) Kaczmarska and G.Fryxell 1996 Amphora ostrearia Bre´bisson 1849 Amphora sp. Asteromphalus arachne Bre´bisson 1857 A. cleveanus Grunow 1874 A. flabellatus (Bre´bisson) Greville 1859 A. heptactis (Bre´bisson) Ralfs in Pritchard 1861 Aulacoseira granulata (Ehrenberg) Ralfs in Pritchard 1861 Aulacoseira islandica (O.Mu¨ller) Simonsen 1906 Azpeitia africana (Janisch ex Schmidt) G.Fryxell & T.P.Watkins 1986 A. neocrenulata (VanLandingham) G.Fryxell & T.P.Watkins 1986 A. nodulifera (A.Schmidt) G.Fryxell & T.P.Watkins 1986 A. tabularis (Grunow) G.Fryxell & T.P.Watkins 1986 Bacteriastrum elongatum Cleve 1897 B. furcatum Shadbolt 1854 Biddulphia alternans (J.W.Bailey) Van Heurck 1885 Chaetoceros affinis Lauder 1864 C. bacteriastroides Karsten 1907 C. concavicornis Manguin 1917 C. diadema (Ehrenberg) Gran 1897 C. lorenzianus Grunow 1863 C. messanensis Castracane 1875 C. peruvianus Brightwell 1856 C. radicans Schuett 1895 Resting spore (RS) C. affinis Lauder 1864 RS C. cinctus Gran 1897 RS C. compressus Lauder 1864 RS C. constrictus Gran 1867 RS C. coronatus Gran 1897 RS C. debilis Cleve RS C. diadema (Ehrenberg) Gran 1897 RS C. dydimus Ehrenberg 1845 RS C. lorenzianus Grunow 1863 RS C. radicans Schu¨tt 1895 RS C. pseudobrevis Pavillard 1911 RS C. vanheurckii Gran 1900 RS Chaetoceros spp. Coscinodiscus argus Ehrenberg 1839 C. centralis Ehrenberg 1839 C. concinnus Wm. Smith 1856 C. decrescens Grunow 1874 C. oculus-iridis Ehrenberg 1854 C. radiatus Ehrenberg 1841 Cocconeis dirupta Gregory 1857 C. disculus (Schumann) Cleve 1895 C. pelta Schmidt 1864 C. pseudomarginata Gregory 1857 C. stauroneiformis (Rabenhorst) Okuno 1957 Corethron criophilum Castracane 1886 Cyclotella litoralis Lange and Syvertsen 1989 Cymatopleura solea (Bre´bisson and Godey) Wm. Smith 1851 Cymatosira belgica Grunow 1880 Delphineis surirella (Ehrenberg) Andrews 1981 Detonula pumila (Castracane) Gran 1900 Diploneis bombus Ehrenberg 1844 D. didyma (Ehrenberg) Cleve 1880 D. papula var. constricta Hustedt 1927 Ditylum brightwellii (West) Grunow 1880 Entomoneis alata (Ehrenberg) Ku¨tzing 1884 Gosleriella tropica Schu¨tt 1892 Grammatophora marina (Lyngbye) Ku¨tzing 1884

Table 2. (continued ) Guinardia cylindrus (Cleve) Hasle 1996 Gyrosigma sp. Fallacia nyella (Hustedt ex Simonsen) D.G. Mann 1990 Fragilariopsis doliolus (Wallich) Medlin & Sims 1996 Hantzschia amphyoxis (Ehrenberg) Grunow 1880 Haslea gigantea (Hustedt) Simonsen 1974 H. hyalinissima Simonsen 1974 Hemiaulus hauckii Grunow 1880 H. membranaceus Cleve 1873 Hyalodiscus stelliger J.W. Bailey 1854 Leptocylindrus mediterraneus (H. Peragallo) Hasle 1975 Licmophora sp. Lioloma elongatum (Grunow) Hasle 1996 Mastogloia sp. Navicula distans Wm. Smith 1853 Navicula sp. Neodelphineis indica (F.J.R. Taylor) Hasle 1993 Nitzschia aequatorialis Heiden 1928 N. bicapitata Cleve 1901 N. braarudii Hasle 1960 N. capuluspalae Simonsen 1974 N. dietrichii Simonsen 1974 N. interruptestriata (Heiden) Simonsen 1974 N. sicula (Castracane) Hustedt 1958 N. sicula aff. N. cf. sicula Nitzschia spp. Odontella aurita (Lyngbie) Agardh 1832 O. mobiliensis Bailey 1845 Opephora sp. Paralia sulcata (Ehrenberg) Cleve 1873 Planktoniella sol (Wallich) Schu¨tt 1860 Plagiogrammopsis vanheurckii (Grunow) Hasle, von Stosch and Syvertsen 1983 Pleurosigma directum Grunow 1880 Porosira denticulata Simonsen 1974 Proboscia alata (Brightwell) Sundstro¨m 1986 Proboscia alata f. indica (Peragallo) Sundstro¨m 1986 Psammodiscus nitidus (Gregory) Round & D.G. Mann 1980 Psammodyction panduriformis (Gregor) D.G. Mann 1990 Pseudo-nitzschia delicatissima (Cleve) Heiden 1928 P. fraudulenta (Cleve) Heiden 1928 P. delicatissima (Cleve) Heiden 1928 P. inflatula var. capitata Simonsen 1974 P. pungens (Grunow ex Cleve) Hasle 1965 P. subfraudulenta Hasle 1965 Pseudotriceratium punctatum (Wallich) Simonsen 1974 Pseudosolenia calvar-avis (Schultze) Sundstro¨m 1986 Rhizosolenia acicularis Sundstro¨m 1986 R. acuminata (H. Peragallo) H. Peragallo 1892 R. bergonii H. Peragallo 1892 R. pungens Cleve-Euler 1937 R. imbricata Brightwell 1858 R. robusta Norman 1861 R. setigera Brightwell 1858 R. styliformis Brightwell 1858 Roperia tesselata (Roper) Grunow 1880 Skeletonema costatum (Greville) Cleve 1873 Surirella sp. Tabullaria sp. Thalassionema bacillare (Heiden) Kolbe 1955 Thalassionema aff. T. cf bacillare 1 Thalassionema aff. T. cf bacillare 2 T. Frauenfeldii (Grunow) Hallegraeff 1986 T. nitzschioides var. nitzschioides (Grunow) Van Heurck 1880 T. nitzschioides f. capitulate (Castracane) Moreno-Ruiz 1996 T. nitzschioides var. inflata Kolbe 1928 T. nitzschiodes var. parva (Heiden) Moreno-Ruiz 1996 T. pseudonitzschioides (Schuette and Schrader) Hasle 1996 Thalassiora angulata (Gregory) Hasle 1978 T. bioculata (Grunow) Ostenfeld 1908 T. conferta Hasle 1977 T. delicatula Ostenfeld 1908

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Table 2. (continued ) T. diporocyclus Hasle 1972 T. eccentrica (Ehrenberg) Cleve 1904 T. elsayedii G.Fryxell 1975 T. endoseriata Hasle & G.Fryxell 1977 T. ferelineata Hasle & G.Fryxell 1977 T. leptopus (Grunow) Hasle & G.Fryxell 1977 T. lineata Josue´ 1968 T. nanolineata (Mann) G.Fryxell & Hasle 1977 T. oestrupii var. oestrupii (Ostenfeld) Hasle 1972 T. oestrupii var. venrickae G.Fryxell & Hasle 1972 T. partheneia Schrader 1972 T. punctigera (Castracane) Hasle 1983 T. sacketii f. sacketii G.Fryxell 1977 T. sacketii f. plana G.Fryxell 1977 T. subtilis (Ostenfeld) Gran 1900 T. symmetrica G.Fryxell & Hasle 1972 Thalassiosira sp. Toxarium sp. Trachyneis aspera Cleve 1894

Freshwater diatoms Achnanthes delicatula (Ku¨tzing) Grunow 1880 Cyclotella meneghiniana Ku¨tzing 1884 Cymbella sp. Epithemia sp. Gomphonema sp. Navicula cryptotenella Lange-Bertalot 1985 Pinnularia sp. Sellaphora pupula Ku¨tzing 1844 Each species is followed by the author’s name and year of description. In a few cases we were unable to identify the taxon to the species level. If this taxon was found repeatedly the generic name was used, followed by ‘‘sp.’’

stratification by late August 1997 (Fig. 2) resulted in less optimal hydrographic and temperature conditions for diatom production. A major change in the ‘‘normal’’ seasonal cycle began in boreal fall 1997 (Fig. 2). The occurrence of ENSO conditions from October 1997 through April 1998 (Chavez et al., 1999) appears to have interrupted the winter/ summer pattern of high/low diatom production and sedimentation in Cariaco Basin. During the 1997–1998 ENSO, trade winds weakened (Astor et al., 2003), SST were higher (Fig. 2), and upwelling was less intense in the Cariaco Basin compared to the periods immediately before ˜ i et al., 2003). The average and after this ENSO event (Gon primary production between late 1997 and mid-1998 was about half that measured during the 1996–1997 upwelling period (Astor et al., 2003). In fact, mean annual production during 1998 was lower than that for any other year during the last decade (Varela, unpublished data). The interruption of upwelling in December 1997 due to a pool of ˜ i et al., 2003) favored moderate warmer waters (Gon production of diatoms (Fig. 3). Even with the resumption of the trade wind-driven upwelling season by late February 1998, the total diatom flux remained low and the primary production was about half of the values registered during the 1997 upwelling (Astor et al., 2003), probably as consequence of the weak cooling of the surface ocean (Fig. 2) and the strong stratification off the Venezuelan coast through late March 1998 (Astor et al., 2003).

Oceanographic perturbances associated with the 1997–1998 ENSO event were far reaching in the Cariaco Basin: as well as affecting the magnitude of the diatom production and export, a major shift in the composition of the winter upwelling assemblage was observed (Fig. 4, Table 3). The stronger input of Caribbean Surface Water into the Cariaco Basin and the weakened E-NE trade winds during ENSO periods reduce the intensity of upwelling. However, the diatom assemblage present during midNovember 1997 is not indicative of full cessation of upwelling but rather a weakening. Although the diatom community is dominated by N. bicapitata and T. nitzschioides var. nitzschioides, typical of waters of moderate to poor nutrient content, secondary contributions by C. litoralis and several species of Chaetoceros spores reflect the presence of surface water masses with moderate nutrient contents. By late January 1998, still under enso conditions, the increased contribution of the weakly silicified S. costatum coupled with the reduced contributions of RS Chaetoceros spp. and C. litoralis reflect a strong relaxation of upwelling and the presence of warm surface waters in the Cariaco Basin. A similar effect has also been observed in the Santa Barbara Basin, off California (Lange et al., 1997). An increase in the relative contribution of pelagic diatom from the eastern tropical Pacific and the decrease of coastal upwelling species in 1997–1998 was associated with warm-water incursions into the basin and dimin˜ o conditions (Lange ished upwelling associated with El Nin et al., 1997). In other areas of the world ocean, however, the composition of the diatom community did not show a strong response to ENSO conditions. For example, although total diatom fluxes in the Subarctic Pacific decreased significantly in response to ENSO events, there were only slight changes in the composition of the diatom ˜ o (Takahashi, 1987). community during the 1982–83 El Nin Similarly, coastal upwelling-associated RS Chaetoceros dominate the diatom flora in the coastal upwelling area ˜ o and La Nin ˜ a years, off Northern Chile during both El Nin even though total diatom production decreased under ENSO conditions (Romero et al., 2001). During the 1997–1998 ENSO event, contributions by species typical of warmer waters, such as F. doliolus, Azpeitia spp., and N. interruptestriata, remained of secondary importance off Northern Chile (Romero et al., 2001). Unlike the 1997–1998 cycle, the high diatom flux during the early 1999 upwelling yielded relatively high ˜i rates of primary productivity (42 mg C m3 h1, Gon et al., 2003). The secondary upwelling event between late March and late April 1999 is recognized as a very weak shoaling of the isotherms, with the 22 1C isotherm reaching a depth of only 60 m (Fig. 2). Although the cooling of the water column was less intense during 1999 than in 1997–1998, there was a prolonged period of relatively ˜i high productivity from May through August 1999 (Gon et al., 2003). Diatoms contributed to this high primary productivity only until early June 1999, probably due to the depletion of silica in surface waters. The composition of the diatom community in the Cariaco Basin during the period of low diatom flux in boreal summer 1999 resembles that of the ENSO period

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Fig. 4. Temporal changes in the relative contribution (%) of diatoms Cyclotella litoralis, resting spores of Chaetoceros spp., Thalassionema nitzschioides var. nitzschioides, Skeletonema costatum, Nitzschia bicapitata, T. nitzschioides var. parva, T. nitzschioides var. inflata, and N. interruptestriata at the sediment trap site in the Cariaco Basin from November 1996 through April 1998, and between January and October 1999. Grey shadings highlight main periods of upwelling and the cross-hatched shading highlights the secondary upwelling season. ENSO: El Nin˜o/Southern Oscillation.

1997–1998. Similar relative contributions of pelagic diatoms (N. bicapitata, T. nitzschioides var. inflata, T. nitzschioides var. parva, A. tabularis) and coastal diatoms (C. litoralis, RS Chaetoceros, T. nitzschioides var. nitzschioides; Table 3) are indicative of the relaxation of coastal upwelling. Like the hydrographic conditions present during ENSO, summer conditions in 1999 were marked by downwelling (Astor et al., 2003) and a ˜ i et al., 2003), thermally stratified surface layer (Gon conditions that are not favorable for diatom production. Sediments accumulating under anoxic conditions are especially useful because the absence of bioturbating macro-fauna often results in undisturbed records with an

excellent degree of preservation. The Cariaco Basin is presently anoxic below 275 m and sediments from below this depth are frequently varved and characterized by high accumulation rates (Peterson et al., 2000). Because of their sensitive response to the regular cycle of intra-annual environmental changes as well as unusual climatic changes such as ENSO events, diatoms can serve as important climatic tracers in the Cariaco Basin. Our observations on the taxonomic composition and the temporal changes of the sinking diatom assemblages are of relevance to paleoceanographers who need to identify and calibrate climate-ocean proxies for the downcore sedimentary record off the Venezuelan coast.

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Table 3 Summary of the main productivity and temperature characteristics in the Cariaco Basin during periods of high diatom fluxes (valves m2 d1), and dominant and secondary diatom species (%, relative contribution) for each diatom peak. Year

Month

Regime

Primary productivity (mg C m3 h1)

Temperature (1C)

Diatom flux (valves m2 d1)

Main diatom species (%)

Secondary diatom species (%)

1997

Late March

4–5

21–23

2.6  107

C. litoralis (460)

1997

Mid-July

E-NE trade winds upwelling season Secondary upwelling

1–2

22–25

8.4  106

C. litoralis (460)

1997

Mid-November

E-NE trade winds upwelling season

1

24–26

4.5–4.8  106

T. nitzschioides var. nitzschioides (22.0–38.8), N. bicapitata (14.0–17.0)

1998

Late January–early February

1–2

24–26

5.2  106

S. costatum (45.8)

1999

Late January–early February

Interruption of E-NE trade winds upwelling season E-NE trade winds upwelling season

45

22

3.8–4.3  107

C. litoralis (53.0–68.6)

1999

Late March

E-NE trade winds upwelling season

1–2

22–24

3.8  107

1999

Late April

E-NE trade winds upwelling season

2–3

24–27

1.8  107

RS Chaetoceros spp. (48.4) and C. litoralis (39.7) C. litoralis (48.7)

RS Chaetoceros spp. (16.3), P. glacialis (4.8), R. tesselata (3.0) RS Chaetoceros spp. (8.6), R. tesselata (5.4), T. nitzschioides var. nitzschioides (3.7) C. litoralis (11.4–6.7), RS Chaetoceros spp. (20.0–4.5), T. oestrupii var. venrickae (2.0–3.5), T. nitzschioides var. parva (0.7–3.3), S. costatum (0–4.0) RS Chaetoceros spp. (15.4), T. nitzschioides var. parva (4.6), N. bicapitata (3.5), C. litoralis (3.3) RS Chaetoceros spp. (21.1–25.3), T. nitzschioides var. nitzschioides (3.4–10.1), N. bicapitata (0.8–2.8) T. nitzschioides var. nitzschioides (3.4) RS Chaetoceros spp. (16.9), T. nitzschioides var. nitzschioides (5.7), N. bicapitata (3.3), T. oestrupii var. venrickae (2.4), T. nitzschioides var. inflata (2.3), T. oestrupii var. parva (2.0)

˜i The boldface highlights the periods under ENSO occurrence. Primary productivity and temperature measured in the upper 20 m of the water column (Gon et al., 2003).

5.3. Conclusions The central objective of our study was to document the temporal variability in the export of diatoms in the coastal upwelling area off Venezuela. To examine this issue we studied the year-round dynamics of the diatom assemblage from November 1996 through April 1998 and between January and October 1999. The main conclusions of this study are as follow: (1) Diatoms are the main suppliers of biogenic silica throughout the year in the Cariaco Basin. The good correspondence between the timing in both diatom fluxes and primary production suggests that the production and export of diatoms in the basin is strongly linked to the seasonally varying E-NE trade wind-driven upwelling. Lowest total diatom fluxes occurred during boreal summers in the Cariaco Basin in response to the presence of nutrient-depleted surface waters. Additionally, the total diatom flux decreased by an order of magnitude during the 1997–1998 ENSO. (2) A clear seasonal succession in the occurrence of the main components of the diatom community occurred. The qualitative composition of the diverse diatom community reflects both the seasonal migration of the ITCZ and the changes associated with ENSO. The assemblage corresponding to periods of high diatom

production and export in boreal winters is dominated by C. litoralis, typical of nutrient-rich, coastal waters, accompanied by resting spores of several species of Chaetoceros. (3) A major shift in the composition of the diatom community occurs during boreal winters affected by ENSO events. The highly diverse diatom assemblage during ENSO is composed of a mixture of pelagic (N. bicapitata, T. nitzschioides var. inflata, T. nitzschioides var. parva) and coastal planktonic species (C. litoralis, RS Chaetoceros spp., T. nitzschioides var. nitzschioides). The simultaneous occurrence of coastal and pelagic diatoms with different temperature and nutrient requirements reflects the fact that the Cariaco Basin is influenced by both offshore and coastal waters, with considerable oceanographic variability over short time intervals during boreal summers.

Acknowledgements We thank E. Tappa for organizing the sediment trapping program and sample analysis. OER thanks E. Kwoll for her lab work. This research was supported, in part, by grants to OER by the German Research Foundation and to RCT from the US National Science Foundation.

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