Author's Accepted Manuscript

Influence of the Nazar Canyon, centralPortuguese margin, on late winter coccolitho-phore assemblages

Catarina Guerreiro, Carolina S, Henko deStigter, Anabela Oliveira, Mrio Cacho, LlusaCros, Carlos Borges, Luis Quaresma, Ana I.Santos, Jos-Manuel Fortuo, Aurora Rodrigues

PII: S0967-0645(13)00342-1DOI: http://dx.doi.org/10.1016/j.dsr2.2013.09.011Reference: DSRII3498

To appear in: Deep-Sea Research II

Cite this article as: Catarina Guerreiro, Carolina S, Henko de Stigter, AnabelaOliveira, Mrio Cacho, Llusa Cros, Carlos Borges, Luis Quaresma, Ana I.Santos, Jos-Manuel Fortuo, Aurora Rodrigues, Influence of the NazarCanyon, central Portuguese margin, on late winter coccolithophoreassemblages, Deep-Sea Research II, http://dx.doi.org/10.1016/j.dsr2.2013.09.011

This is a PDF file of an unedited manuscript that has been accepted forpublication. As a service to our customers we are providing this early version ofthe manuscript. The manuscript will undergo copyediting, typesetting, andreview of the resulting galley proof before it is published in its final citable form.Please note that during the production process errors may be discovered whichcould affect the content, and all legal disclaimers that apply to the journalpertain.

www.elsevier.com/locate/dsr2

1

Influence of the Nazar Canyon, central Portuguese margin,

on late winter coccolithophore assemblages

Catarina Guerreiroa,b,c*,

Carolina Sd, Henko de Stigter

b, Anabela Oliveira

a, Mrio Cacho

c,e,

Llusa Crosf, Carlos Borges

a, Luis Quaresma

a, Ana I. Santos

a, Jos-Manuel Fortuo

f, Aurora

Rodriguesa

a Portuguese Hydrographic Institute (IH), Rua das Trinas 49, 1249-093 Lisbon, Portugal

b Royal Netherlands Institute for Sea Research (NIOZ), Marine Geology Dep., Texel, The

Netherlands

c Geology Centre of the University of Lisbon, 1749-016 Lisbon, Portugal

d Oceanography Centre Fac. Sciences of the University of Lisbon, 1749-016 Lisbon, Portugal

e Department of Geology, Fac. Sciences, University of Lisbon, 1749-016 Lisbon, Portugal

f Institut de Ciencies del Mar (CSIC), Passeig Martim de la Barceloneta, 37-49. E-08003

Barcelona, Spain

* Corresponding author Fax: +351 217500119, E-mail: cataguerreiro@gmail.com

Key words: Living coccolithophores; Chl-a; ENACWst; Submarine canyon

Abstract

This paper presents a first attempt to characterize coccolithophore assemblages occurring

in the context of an active submarine canyon. Coccolithophores from the upper-middle sections

2

of the Nazar Canyon (central Portuguese margin) - one of the largest canyons of the European

continental margin - were investigated during a late winter period (9 12 March 2010). Species

distributions were analyzed in a multiparameter environmental context (temperature, salinity,

turbidity, Chl-a and nutrient concentrations). Monthly averaged surface water Chl-a

concentrations between 2006 and 2011 assessed from satellite data are also presented, as a

framework for interpreting spatial and temporal distribution of phytoplanktonin the Nazar

Canyon. The Nazar Canyon was observed to act as a conduit for advection of relatively

nutrient-poor oceanic waters of ENACWst origin into nearshore areas of the continental shelf

(less than 10 km off the coast), whilst at the surface a nutrient-rich buoyant plume resulting from

intensive coastal runoff prior and during the beginning of the cruise was spreading in oceanward

direction. Two distinct coccolithophore assemblages appear representative for the coast to open-

ocean gradient: (1) Emiliania huxleyi together with Gephyrocapsa ericsonii and Coronosphaera

mediterranea dominated the more productive assemblage present within coastal-neritic surface

waters; and (2) Syracosphaera spp. and Ophiaster spp. displayed a higher affinity with open-

ocean conditions, and also generally a broader vertical distribution. Local hotspots of

coccolithophore and phytoplankton biomass potentially associated with perturbations of surface

water circulation by the canyon are discussed.

1. Introduction

Submarine canyons incising the continental margins are prominent topographic features that

modify the coastal circulation. By intensifying shelf-slope exchange of water and

organic/inorganic matter they play a key-role in global biogeochemical cycling (e.g. Durrieu de

Madron, 1994; Gardner, 1989; Hickey et al., 1986; Monaco et al., 1999; Puig et al., 2003).

3

Narrow canyons tend to have a stronger effect on low-frequency circulation, whereas wider

canyons mainly cause bottom flow adjustment along isobaths (Klinck, 1988). Stratification of the

water column reduces the canyons topographic effect on the coastal flow (Hickey, 1997; She

and Klinck, 2000).

In the upper water layers (above 100 m), the influence of the canyon is only gentle, with

the along-shelf flow turning slightly onshore upstream of the canyon and turning offshore

downstream. Closer to the canyon rims (100-200 m) the along-shelf flow is more strongly

deflected in onshore direction, turning back on the downstream side of the canyon, with

upwelling or downwelling occurring above the rims, depending on the wind direction (She and

Klinck, 2000). In the Northern Hemisphere right-bounded flows (i.e. coast to the right, looking

downstream) induce downwelling- conditions within the canyon, whereas left-bounded flows

favor the occurrence of upwelling (Klinck, 1996; She and Klinck, 2000). Upwelling occurs

mostly at the canyon head and downstream rim and adjacent shelf (Allen, 1996; Klinck, 1996;

Mendes et al., 2011; She and Klinck, 2000). Under downwelling conditions, the canyon acts as a

trap for converging shelf water (Skliris and Djenidi, 2006).

The intensification of both coast to ocean and vertical water transport within submarine

canyons is expected to affect the dynamics of plankton ecosystems in the vicinity of canyons

(see Bosley et al., 2004; Hickey, 1995; Kampf, 2006; Ryan et al., 2005; 2010; Skliris et al.,

2002; Skliris and Djenidi, 2006). Indeed a strong response of phytoplankton production to

canyon flows, and concentration of marine organisms by physical processes within and around

canyons were reported from several studies (e.g. Bosley et al. 2004; Macquart-Moulin and

Patriti, 1996; Skliris and Djenidi, 2006).

The Nazar Canyon, located at the central Portuguese margin and one of the largest

4

submarine canyons of Europe, has been relatively intensely explored with regards to its geology,

geomorphology, oceanography and benthic biology (e.g. Tyler et al., 2009). Little is known,

however, about the plankton communities thriving in this region, and about the canyons effect

on their ecology.

Guerreiro et al. (submitted) observed a relatively higher diversity of coccolith species,

including both oceanic and coastal-neritic taxa but with a relative dominance of the latter, in the

Nazar Canyon in comparison to the adjacent shelf/slope regions. This was interpreted as

reflecting the exchange of water masses between coastal and oceanic regions through the canyon,

as well as the dynamic and nutrient-rich conditions where the coastal species are better adapted

to survive. Locally enhanced productivity in the surroundings of the canyon may be related to

persistent physical phenomena associated with the canyon such as vertical mixing by solitary

internal waves (Quaresma et al. 2007), and/or upwelling in the canyon head (Guerreiro et al.,

2009). Evidence for local enhancement of phytoplankton productivity is also provided by

observations on phytoplankton pigments reported by Mendes et al. (2011), with maximum values

of Chl-a (indicative of phytoplankton in general) near the canyon head and maximum values of

19 hexanoyloxyfucoxantine pigment (indicative of coccolithophores) found in the area north of

the canyon.

Here we report the results obtained from a plankton survey on living coccolithophores from

the upper-middle Nazar Canyon, during late winter (9 12 March 2010) (Figure 1). On the

basis of a detailed characterization of the coccolithophore assemblages together with a general

characterization of environmental conditions prevailing during the sampling period, the impact

of this major submarine canyon on coccolithophores and phytoplankton biomass is discussed.

2. Regional setting

5

2.1. Oceanography

The central Portuguese continental margin is characterized by a relatively narrow shelf of

a few tens of km width, with a maximum of ~70 km where it projects oceanward in the

Estremadura promontory, but cut back to very close to shore where it is incised by the Nazar

and Lisbon-Setbal Canyons. The Douro and Tagus are the most important rivers debouching on

the shelf, with relatively minor contribution of continental runoff from other rivers. From the

shelf edge located at 160-200 m, a steep upper slope and more gently inclined lower slope

incised by numerous gullies and canyons, lead down to the Iberia and Tagus abyssal plains.

Surface water circulation along the Portuguese margin is directly dependent on two main current

systems transporting water eastwards across the North Atlantic: the North Atlantic Current

extending to the north of the Iberian Peninsula, and the Azores Current south of Iberia (Barton,

2001; Peliz et al., 2005; Pollard and Pu, 1985; Saunders, 1982). As the Azores Current extends

eastwards, branches of this current loop smoothly into the Portugal Current and further south into

the Canary Current. The Portugal Current slowly flows southwards, west of Portugal, carrying

about 2106 m

3/s in the upper 200 m of the water column. It partially continues further south into

the Canary Current, while another part apparently enters the Mediterranean within a shallow

surface layer (Barton, 2001; Saunders, 1982).

The upper 500 m of water column off Portugal, including the surface mixed layer and the

first thermocline, is constituted by the Eastern North Atlantic Central Water (ENACW). This

water mass, representing the main source of the nutrient-rich upwelled waters on the Portuguese

coast, shows considerable variation in its hydrological features as it travels along the coast

(Fiza, 1984; McCave and Hall, 2002). The ENACW has two main components of different

6

origin that converge to this region: a lighter, relatively warm and salty subtropical branch

(ENACWst) formed along the Azores Front, which gradually loses its characteristics as it travels

further northwards along the Iberian margin; a less saline colder water mass of subpolar origin

(ENACWsp) slowly flowing southwards below the poleward subtropical branch, related with the

Subpolar Mode Water formed in the eastern North Atlantic by winter cooling and deep

convection (Fiza et al., 1998).

Beneath the near-surface equatorward flow of the Portugal and Canary currents, the

Iberian Poleward Current (IPC) can be recognized traveling poleward, counter to the general

circulation and closely bound to the continental slope, its core extending about 300-400 m

vertically. This current is mostly restricted to the subsurface layers along most of the eastern

subtropical gyre, but surfaces whenever the Trade Winds weaken or turn northward (Barton,

2001).

Circulation along the Portuguese shelf and upper slope is markedly seasonal, associated

to the annual cycle of two major atmospheric systems: the Azores high and Iceland low pressure

system, respectively (e.g. Barton, 2001; Haynes et al., 1993; Relvas et al., 2007). During

summer, the Azores high pressure system migrates towards the central Atlantic, typically

inducing Trade Winds to become northerly, inducing an equatorward circulation over the upper

150-200 m of the water column off Portugal. During winter, when the Azores high pressure

system is located further south and the Iceland low pressure system intensifies, the dominant

wind regime becomes southerly along the western Portuguese margin. This induces shoaling of

the IPC over the upper slope and shelf, where the poleward flow produces an onshore Ekman

transport, in turn resulting in downwelling conditions over the shelf (Fiza, 1983; Vitorino et al.,

2002).

7

River runoff is an important feature of the winter circulation over the western Portuguese

margin, through which a significant discharge of low salinity water occurs into the coastal ocean.

This results in buoyant plumes that either develop into inshore currents (Relvas et al., 2007;

Otero et al., 2008) or expand further offshore, under the influence of, respectively, southerly or

northerly-winds over the shelf and slope (Otero et al., 2008). The Western Iberian Buoyant

Plume, characterized by low salinity (

8

influencing the hydrodynamics of the Portuguese margin. Particularly where the M2 semi-

diurnal tidal current, the dominant tidal constituent over the Portuguese margin, forces stratified

upper ocean water over the abrupt topography of the slope and shelf-break (e.g. Quaresma and

Pichon, 2011), tidal energy is transferred into baroclinic motions in the form of internal waves

and internal tides. These are very important in mixing the ocean water column, enhancing

vertical nutrient transport and thus phytoplankton productivity (e.g. Guerreiro et al., 2009), as

well as in increasing bottom turbulence over the continental shelf and slope, triggering bottom

sediment resuspension and transport (Huthnance et al., 2002). Hotspots of internal tide

generation on the Portuguese margin appear associated with submarine canyons cutting across

the shelf and slope (e.g. Portimo canyon, Bruno et al., 2006; Nazar Canyon, Quaresma et al.,

2007; Quaresma and Pichon, 2011) and with promontories of the continental shelf (e.g.

Estremadura spur, Quaresma and Pichon, 2011).

2.1. Nazar Canyon

The Nazar Canyon, the largest submarine canyon of the Portuguese margin, cuts completely

across the shelf and slope, from less than 1 km from the coastline off the village of Nazar at a

water depth of about 50 m to a distance of >210 km from the coast and a water depth of 5000 m.

An upper, middle and lower section can be distinguished on the basis of general morphology and

characteristics of the hydrodynamic and sedimentary environment (Vanney and Mougenot, 1990;

De Stigter et al., 2007; Lastras et al., 2009). The upper canyon section consists of a narrow and

distinctly V-shaped meandering valley that lies deeply entrenched in the shelf. Beyond the shelf

edge, it passes into the much broader and U-shaped middle section incised in the continental

slope. The lower canyon section consists of a broad and flat-floored valley at the base of the

9

slope, opening at 5000 m water depth into the Iberia Abyssal Plain.

The physical oceanography of the Nazar Canyon has been summarised by Tyler et al.

(2009), largely on the basis of CTD and current meter data collected by the Portuguese

Hydrographic Institute and Royal NIOZ (final reports of the EUROSTRATAFORM, HERMES

and HERMIONE European projects).

Inside the Nazar Canyon residual currents are generally aligned along the canyon axis as the

result of strong topographical control. The current alignment extends well above the canyon

edges (~150 m depth) implying substantial disturbance of the predominant north-south

circulation parallel to the general trend of the shelf and slope.

At depths shallower than 300 m, the residual currents inside the canyon show a distinct

coupling to the wind-driven current regime over the continental shelf. During winter, the

occurrence of downwelling conditions over the shelf results in a down-canyon residual flow near

or just above the canyon edge. Under strong upwelling conditions and southward flow across the

shelf, onshore (up-canyon) flow is observed in the upper canyon, with intensification of

upwelling near the canyon head. The enhancement of upwelling and associated bottom

resuspension can be expected to provide a nutrient source supporting enhanced phytoplankton

concentration south of the canyon (e.g. Hickey, 1995; Kampf, 2006). This seems to be confirmed

by observations by Mendes et al. (2011) regarding phytopigment distribution patterns in surficial

waters around the Nazar Canyon, with maximum concentrations of diatoms occurring south of

the canyon.

The interaction of the external (barotropic) tide off the Portuguese coast with the canyon

topography, in the presence of water stratification, leads to the generation of internal (baroclinic)

tides (i.e. internal waves of tidal period), which radiate from the generation point and propagate

10

the tidal energy vertically (Quaresma et al., 2007; Tyler et al., 2009). Strong semi-diurnal bottom

currents occur in all parts of the canyon, particularly in its upper and middle sections (commonly

exceeding 30 cm/s) which, along with the ample supply of fine-grained sediments from the shelf,

result in the permanent haze of suspended matter in the upper canyon (De Stigter et al., 2007).

The generation of non-linear internal waves (NIW) at the canyons northern shelf break and

their refraction towards NE was observed by Quaresma et al. (2007) mainly during summer,

when stratification of the shelf waters supports the waves. Observations indicate that the NIW

most likely result from the interaction of the semidiurnal M2 barotropic tide with the canyon rim,

displaying horizontal and vertical velocities strong enough to resuspend bottom sediments along

the wave propagation path from the middle to the inner shelf. The injection of nutrients from the

lower toward the upper levels of the water column forced by the shoreward propagation of these

NIW has been invoked to explain high concentrations of coccoliths found in the sedimentary

cover in this near shore position (Guerreiro et al., 2009). Although this mechanism occurs mainly

during spring and summer, it seems persistent enough to explain such anomaly in coccolith

distribution.

In autumn and winter, violent westerly storms generating waves with significant height up to

9 m cause widespread sediment resuspension on the shelf and downwelling of turbid waters

towards the canyon. The location of the canyon head at less than 1 km from the shore makes it

particularly prone to trap particulate matter transported as bedload and in suspension along the

shelf (De Stigter et al., 2007; Oliveira et al., 2007).

3. Material and methods

3.1. Sample collection

11

Sampling was conducted between 9th

and 12th

of March 2010, on board of NRP Almirante

Gago Coutinho during the 2nd

HERMIONE (Hotspot Ecosystem Research and Mans Impact

On European Seas) scientific cruise of the Portuguese Hydrographic Institute. Coccolithophore

communities were investigated in 97 water column samples collected at discrete water depth

levels between 5 and 110 m depth from 25 CTD (conductivity, temperature, depth) casts in and

around the Nazar Canyon (Figure 1, Table 1).

Physical oceanographic, biological and chemical data (i.e. temperature, salinity, turbidity,

fluorometry and nutrients) and water column samples were collected using a combined Neil

Brown MKIIIC CTD profiler equipped with an Aquatracka nephelometer, a Seapoint

fluorometer and a rosette sampler (12 Niskin bottles of 8 litres). A total of 192 suspended matter

samples were collected from surface, intermediate and bottom nepheloid layers in order to define

the particulate matter concentration (PMC) and to calibrate the nephelometer response

(turbidity). The PMC (g/m3) was compared to a laboratory calibration of the instrument with a

standard formazine solution (FTU). The turbidity calibration for March 2010, was FTU =

0.112*PMC with r = 0.88.

3.2. Meteorological and hydrological data

Hydrographic conditions during the cruise as determined from CTD profiles are represented

as contour plots using inverse distance to power gridding in Surfer Version 8 software. A WSW-

ENE oriented transect covering the entire length of the upper-middle Nazar Canyon axis (23

CTD casts) was built to represent density, temperature, salinity and turbidity conditions during

the sampling period (casts indicated in Figure 1; CTD profiles in Figures 2a-d). For a more

12

detailed description of the data referring to wind, sea wave, and river discharge and sky

conditions, the reader is referred to Guerreiro et al. (2013).

3.3. Satellite data

Monthly averaged surface water chlorophyll a (Chl-a) concentration between 2006 and 2011

was assessed from satellite data as a framework for interpreting spatial and temporal distribution

of phytoplankton in the Nazar Canyon. Chl-a data acquired by the Moderate-resolution imaging

spectroradiometer (MODIS) on NASAs Aqua satellite and processed by The Ocean Biology

Processing Group (OBPG) were downloaded from the Ocean Color Website

(http://oceancolor.gsfc.nasa.gov/). After quality checking and masking, valid data were

interpolated from a grid of regular latitude-longitude inteval. For each image, with nominal

resolution of 1 km, data corresponding to three defined transects (one transect along the canyon,

two other crossing it) were extracted and averaged per month.

3.4. Laboratory and microscope analysis

3.4.1. Coccolithophores

For the study of coccolithophores, seawater samples of around 2l were filtered over

cellulose acetate filters (47 mm diameter and 0.45 m pore size) using a low pressure vacuum

system. The filters were then rinsed with tap water to remove salt and oven-dried at 40 C for 24

hours. A randomly chosen section (approx. 30 45) of each filter was cut and permanently

13

mounted on a glass slide. Coccospheres (cells) were identified and counted under polarized light

microscope (PLM) (Olympus BX-40) at 1250 magnification. The scanned area per filter varied

between 0.1 and 3.5 mm2, depending on the general cell density. The number of cells per liter of

seawater was estimated from the number of counted coccospheres multiplied with the ratio of

filled filter area to observed area and divided by the volume of filtered water (Cros, 2001).

For the study of the living assemblages (cells) only the water column between 5 and 110

m water depth was considered. To refine the taxonomic differentiation of Alisphaera spp.,

Algirosphaera robusta, Gephyrocapsa spp., Ophiaster spp., Syracolithus dalmaticus and

Syracosphaera spp., 13 samples were investigated using Scanning Electron Microscope (SEM

Hitachi S-3500N, at 5 kV). Samples were selected for containing relatively higher cell densities

and species diversity. A randomly chosen section of the selected filters was fixed with colloidal

Ag on a SEM stub and sputtered with an Au-Pd coating of maximum 20 nm thick; then, a

minimum number of 100 vision fields (VF) were observed and counted using magnifications

between 1000 (observation area of each VF: 126.52 94.84 m) and 2000 (observation area

of each VF: 63.26 47.42 m).

Identification of coccolithophore species followed Jordan et al. (2004) and Young et al.

(2003), whilst the new website on nannoplankton taxonomy http://nannotax.org (Young et al.,

2011) and specific literature on light microscopy (Frada et al. 2009), Mediterranean

coccolithophores (Cros and Fortuo 2002) and Syracosphaera genus (Kleijne and Cros, 2009)

provided useful additional guidance for classification.

3.4.2. Phytoplankton pigments (Chl-a) and nutrients

14

Chl-a concentrations were used as an indicator for phytoplankton biomass. Water samples

of 2l were filtered over Whatman GF/F filters (0.7 m pore size, 25 mm diameter), and the filters

were immediately deep-frozen and stored at 80 C. Phytoplankton pigments were extracted

with 2-3 ml of 95 % cold-buffered methanol (2 % ammonium acetate) and analysed with high-

performance liquid chromatography (HPLC). Chromatographic separation was carried out

following Zapata et al. (2000). Chl-a concentrations obtained from 25 HPLC samples were then

used to calibrate fluorometry measurements obtained from CTD casts (r2= 0.7, with p < 0.01).

Nutrient concentrations (nitrate, nitrite, ammonium, phosphate and silicate) were

determined using a Skalar SANplus Segmented Flow AutoAnalyzer specially developed for the

analysis of saline waters. NNOx and NNO2 were determined according to Strickland and

Parsons (1972), with NNO3 being estimated by the difference between the previous two; N

NH4 and SiSiO2 were determined according to Koroleff (1976); PPO4 was determined

according to Murphy and Riley (1962). All methods were adapted to the methodology of

segmented flow analysis and uncertainties were determined following Mendes et al. (2011).

3.5. Statistical analysis

A statistical multivariate analysis (r-mode Factor Analysis by Statistica 10) was performed

upon the data matrix with coccolithophore concentrations, nutrient concentrations (NOx, PO4,

SiO2), biomass (fluorometry calibrated with Chl-a concentrations measured by HPLC) and

physical parameters (temperature, salinity, turbidity) as columns (variables). Results from the

original data matrices were optimized through Varimax Raw rotation.

4. Results

15

4.1. Environmental conditions during the cruise

The plankton cruise took place under transient environmental conditions in late winter

2010, as discussed in detail in Guerreiro et al. (2013). Sampling was performed at the end of an

unusually cold winter in Europe (2009 2010) under an exceptionally negative phase of the

North Atlantic Oscillation (NAO) (Cattiaux et al., 2010; Troupin and Machin, 2012). Whilst a

northerly wind regime began to settle around the start of the cruise, the winter mixed layer was

still occupying most of the water column over the shelf and upper slope (uppermost ~150200 m

water depth), as normally the case during winter off Portugal (Oliveira et al., 2004). However,

intense river runoff that occurred prior to and continued during the cruise had produced a well-

established colder and less saline surface layer extending from near the coast to more than 50 km

offshore, overlying the warmer and saltier winter mixed layer waters (Figures 2a, b and c). The

lowest TS values within this buoyant plume fed by runoff water were measured at the surface,

approximately between 16 and 30 km off the coast (stations 79 and 122, respectively).

The warmer and saltier winter mixed layer associated with the flow of the IPC along the

Portuguese margin was noticeable below the surface buoyant plume in the entire investigated

region, generally below 15-20 m water depth, appearing continuous in north-south direction

close to the shelf-break, at the upper-middle Nazar Canyon transition. Further offshore it was

mostly noticed along the southern flank of the middle canyon but weakening northwards where

significant mixing apparently occurred with colder water masses from north. The TS contrast

between the superficial BP and the winter mixed layer below was particularly pronounced in the

upper Nazar Canyon where the core of the IPC penetrated up-canyon to less than 10 km off the

coast. TS profiles along the canyon axis show evidence of strong vertical oscillation around

16

Belatina Valley (station 120) possibly driven by internal tides in this part of the canyon

(Quaresma et al., 2007) (Figures 2a, b and c).

Turbidity was generally low, with relatively higher FTU values noticed in the surficial

water layer, as well as at the bottom layer of the upper canyon (i.e. in the canyon head and close

to the intersection with Vitria tributary). Highest turbidity values recorded around 200 300 m

water depth appear to reflect bottom sediment resuspension caused by the canyons internal tide

(Figure 2d).

Highest nutrient concentrations were recorded in the relatively cool and low-saline

surface water of the BP, decreasing to lower concentrations in the winter mixed layer water

underneath. The vertical decreasing trend was particularly noticeable in the case of SiO2 (Figure

3). NOx/PO4 ratio was generally close to the 16:1 Redfield Ratio typical for marine waters

(Redfield et al., 1963). A slight deviation toward lower NOx concentrations relative to PO4 in

most samples suggests that NOx was the major limiting nutrient for phytoplankton growth at that

time.

Phytoplankton biomass inferred from Chl-a concentrations (max.

17

A total of 35 distinct taxa of coccolithophores (coccospheres) were recognized. Nineteen

species and 4 genera were identified using polarizing light microscopy (PLM) whereas additional

Scanning Electron Microscope (SEM) analysis revealed an additional 16 species belonging to the

genera Syracosphaera, Ophiaster, Alisphaera and Acanthoica, and one holococcolithophore,

Syracolithus dalmaticus (see Table 2). The list of observed species is presented in Appendix A.

Coccolithophore cells occurred within the BP and the upper layers of the winter mixed

layer as indicated in Figure 5. Total cell densities ranged between 4.0103 and 6.010

5 cells/l

(Table 2). The highest cell densities along a transect covering the upper-middle Nazar Canyon

axis were noticed close to Belatina Valley, associated to minimum TS values within the BP

(stations 118 and 120) (Figure 6). High cell densities were also noticed closer to the coast, at the

canyons head (station 87), less than 2 km off the coast, and above the southern canyon rim

(station 89) (Fig. 7a). Further offshore toward the open ocean (station 132) lower cell densities

were observed, distributed more homogeneously over the water column (Fig. 7b-c).

Of the 35 identified taxa, only ten reached significant cell densities of more than 2000

coccospheres per litre: Emiliania huxleyi, Syracosphaera spp., Gephyrocapsa ericsonii, G.

oceanica, G. muellerae, Coronosphaera mediterranea, Ophiaster spp., Helicosphaera carteri,

Syracolithus dalmaticus and Algirosphaera robusta. E. huxleyi was the dominant species during

the cruise, particularly at the surface close to the shelf-coastal region (Figure 8, Table 2). Below

the surface and further offshore, other species gained in relative importance within the total

assemblage, generally displaying a broader vertical distribution (Figure 9; Guerreiro al., 2013).

G. ericsonii, A. robusta, Acanthoica spp., Syracosphaera pulchra, S. dalmaticus, Coccolithus

pelagicus, Michaelsarsia elegans and, to a lesser extent G. oceanica, displayed a downward

18

decreasing trend in cell density, similar to that of E. huxleyi. Other groups of species such as

Syracosphaera spp, Ophiaster spp. and Gephyrocapsa muellerae revealed a more uniform

vertical distribution. The remaining taxa did not reveal a specific vertical distribution pattern

(Figure 8).

A coast to open ocean ecological and hydrological dichotomy is well illustrated in Figure

9: E. huxleyi dominated at the surface in coastal waters (stations 87 and 120, Figures 9c,b),

whereas Syracosphaera spp. and Ophiaster spp. were dominant further offshore in more open-

ocean conditions, and showing a broader vertical distribution (station 132, Figure 9a). Closer to

Belatina Valley, the three taxa co-existed, with E. huxleyi largely dominating at the surface, and

the latter taxa relatively increasing in the subsurface water mass (Figure 9b). G. muellerae, G.

oceanica and S. dalmaticus were also more abundant near the coast, whereas G. ericsonii and C.

mediterranea revealed a broader lateral distribution.

4.2.2. Multivariate analysis

Results from factor analysis revealed four distinct factor assemblages explaining 46 % of

the total variance in the data (Table 2, Figure 10). Factor 1 (F1) explains 22 % of total

variability, with NOx, SiO2, Acha and Eh recording the highest (positive) factor loadings, in

opposition to S, T (and Syraco and Ophi) (negative loadings). Factor 2 (F2) explains 10 % of

total variance, being represented by Ge, Biom and Cm (and Eh) (positive loadings). Factor 3 (F3)

explains 8 % of total variability and is represented by Dtub, Alisph (and PO4) (negative

loadings). Factor 4 (F4) explains 7 % of total variability and it is represented by the Go (and

Turb) (positive loadings) in opposition to Meleg (negative loadings).

19

Samples influenced by factor assemblage NOx, SiO2, Acanthoica spp. and E. huxleyi (F1

positive scores) were better represented at the surface, particularly close to Belatina Valley

(stations 118 and 120) but also around the uppermost reaches of Nazar Canyon (stations 112,

111, 102) and the canyon head (stations 85, 87) (Figure 10a). Below the surface this assemblage

was practically inexistent or weakly represented. Samples influenced by salinity, temperature,

Syracosphaera spp. and Ophiaster spp. (F1 negative scores) were preferentially represented

further offshore and showed a relatively broader lateral distribution, and at Belatina Valley

region below the surface (Figure 10a).

Samples influenced by G. ericsonii, phytoplankton biomass (Chl-a), C. mediterranea

(and to a lesser extent, E. huxleyi) (F2 positive scores) revealed a rather broad lateral distribution,

preferentially at the uppermost 25 m in the Nazar Canyon head and at Belatina Valley, whereas

further offshore a broader vertical distribution is noticed (Figure 10b).

Samples influenced by Discosphaera tubifera, Alisphaera spp. and PO4 (F3 negative

scores) recorded their strongest signal at 50 m water depth, at the Nazar Canyon head (station

87) (Figure 10c).

Samples influenced by G. oceanica and turbidity (F4 positive scores) were consistently

distributed in more neritic-coastal regions, particularly at the canyon head and surroundings

(stations 87, 93), at all water depths. In the intersection between the canyon axis and Vitria

tributary (station 80) and at Belatina Valley, this assemblage was well represented at the

uppermost 25 m (Figure 10d).

The relatively low percentage of variance explained by F1-F4 (< 50%) reflects the highly

transient meteorological and hydrological conditions during the cruise, where water masses (both

oceanic and continental) were still adjusting to the circulation imposed by the shifting wind

20

regime (see Guerreiro et al., 2013). Nevertheless, factor analysis helped to reveal and understand

the most important ecological signals during the cruise:

(a) coccolithophore cell density and diversity hotspot at the Nazar Canyon head, despite of

abundant detritic material (i.e. terrigenous particles, reworked coccoliths). Significant amounts of

perfectly preserved cells, particularly of E. huxleyi, together with several other species, testify of

the high diversity found in this part of the canyon (see Appendix B). Gephyrocapsa muellerae,

Syracolithus dalmaticus, Acanthoica spp. and Michaelsarsia elegans had their maxima in this

area (Table 2). Additional SEM observations confirmed the relative increase of Calcidiscus

leptoporus, Coccolithus pelagicus and Helicosphaera carteri in the canyon head, together with

the single occurrence of Syracosphaera amoena (formerly S. bannockii, see Dimiza et al., 2008),

Syracosphaera molischii, Palusphaera vandelii and Syracosphaera anthos. G. oceanica was also

systematically better represented in the canyon head at all water depths, associated to turbidity;

(b) Stations close to Belatina Valley seemed to represent a nutrient, Chl-a and coccolithophore

hotspot, with E. huxleyi, G. ericsonii, C. mediterranea (and G. oceanica) dominating the

assemblages at the uppermost 25 m water depth, and Syracosphaera spp. and Ophiaster spp.

dominating underneath; (c) E. huxleyi was clearly displaced towards the neritic/coastal zone, and

G. ericsonii and C. mediterranea more towards the neritic-oceanic zone. Syracosphaera spp. and

Ophiaster spp. were consistently better represented below the surface and further offshore.

4.3. Monthly averaged Chl-a from satellite imagery

Time-series of monthly averaged Chl-a between 2006 and 2011 calculated from satellite

data are shown for three transects: transect A, WSW ENE oriented, covering the whole upper-

21

middle canyon axis (Figure 11a); transect B, N S oriented, cutting across the canyon axis at

Belatina Valley (station 120) (Figure 11b); and transect C oriented at a low angle to the coastline

and cutting across the canyon head (station 87).

The along-canyon time series (Figure 11a) illustrates the recurrent maximum of Chl-a in

offshore waters occurring around March and April of all years, and a more persistent presence of

high Chl-a concentrations in the coastal zone during spring and summer months. There is no

evidence of persistent or particularly high Chl-a at Belatina Valley, although the transition zone

between Chl-a enriched waters extending from the coast and Chl-a poorer offshore waters is

often located approximately in this region. A map of average Chl-a concentration for March

2010 (Figure 12) illustrates the broad spatial spread of this Chl-a enrichment, occupying a

significant portion of the continental shelf and extending approximately up to the middle shelf

region, apparently coming from north. Slightly higher Chl-a concentrations are noticed along the

canyon axis in comparison to the shelf immediately north of it, particularly at Belatina Valley,

where the highest coccolithophore cell densities and Chl-a were recorded in situ during the

cruise. Similar offshore outbreaks of Chl-a enrichment were also observed in March 2006 and

2009, extending almost to the shelf-break in 2006, and even beyond in 2009 (data not shown).

The Chl-a time series for the transect across the canyon at Belatina Valley (Figure 11b)

shows higher concentrations in the canyon meander and adjacent northern and southern shelf in

March of 2006, 2009 and 2010, reflecting the seasonal offshore spread of Chl-a enrichment. Chl-

a concentrations are consistently higher south of 39.4N where the transect is located in the more

productive near shore area, whereas concentration is much lower along the northern part of the

transect located in the less productive offshore area.

Persistently high Chl-a concentration is observed close to the coast, particularly in spring

22

and summer months (between March and October), reaching the highest concentrations in

August-October 2007, and June-September 2010. The time series for the NNE-SSW near-shore

transect cutting across the canyon head (Figure 11c) shows maximum Chl-a concentrations in the

canyon head and immediate vicinity in these time-intervals, exceeding concentrations on the

surrounding shelf. The timing of Chl-a peaks in the canyon head, between mid-August and mid-

September 2007; between mid-May and mid-June 2009; in March and between mid-June and

mid-August 2010, is conspicuously different from that of the widespread Chl-a enrichment in

early spring extending across the shelf.

5. Discussion

5.1. Late winter coccolithophore assemblages off Portugal

Moderately low coccolithophore cell densities (between 3.6103 and 610

5 cells/l) and

low phytoplankton biomass (Chl-a) (max.

23

this period of intense runoff, sub-optimal light conditions due to cloud cover and initial relatively

high turbidity within the superficial BP (discussed in Guerreiro et al., 2013).

Four distinct ecological signatures (factors) were extracted from multivariate statistical

analysis applied to the present dataset, explaining 46 % of the variability within the data and

revealing the most important environmental and ecological signals during the cruise (Figure 10,

Table 3).

Factor 1 (positive loadings) is interpreted as representing the gradient between the runoff-

influenced coastal-neritic zone, where relatively high nutrient concentrations were retained in the

superficial BP, and the oceanic mixed water that characterizes the Portuguese margin during

winter, present below the BP closer to the coast and surfacing further offshore. Acanthoica spp.

and Emiliania huxleyi appear positively correlated with nutrients at the surface within more

coastal-neritic conditions. F1 was strongly expressed close to Belatina Valley and around the

Nazar Canyon head and surroundings, but nearly absent below the surface, highlighting the

strong vertical density gradient of the BP and the clear preference of these taxa to develop at the

sunlit nutrient-rich surface water layer (Figure 9b,c and 10a).

The large dominance of E. huxleyi at the less saline sunlit surface layer and its preference

for more coastal/neritic conditions is in good agreement with several authors describing this

species as having a highly cosmopolitan distribution independent of sea surface temperature, and

attaining high cell densities in both oligotrophic and eutrophic environments (Andruleit, 2007;

Baumann et al., 2000; Winter et al., 1994). This species was considered to be a possible indicator

for more stable regions regarding with nutrient availability (Andruleit and Rogalla, 2002), and is

often found associated with nutrient-rich and productive coastal regions (e.g. Andruleit, 2007;

Giraudeau and Bailey, 1995; Sprengel et al., 2002; Silva et al., 2008). From various locations it

24

has been reported as responsible for major blooms (e.g. Garcia et al., 2011; Knappertsbush and

Brummer, 1995).

E. huxleyi was also weakly positively correlated to Gephyrocapsa ericsonii,

Coronosphaera mediterranea and Chl-a in Factor 2 (positive loadings), particularly in what

revealed to be the most productive station monitored during the cruise, located around Belatina

Valley (Figure 10b). Further offshore where E. huxleyi was not dominating the coccolithophore

community, the two taxa were also important. G. ericsonii was the second most abundant species

during the cruise, next to E. huxleyi, which is in good agreement with several studies indicating

its preference for nutrient-enriched coastal-neritic regions (Giraudeau and Bailey, 1995; Silva et

al., 2009; Winter et al., 1979). C. mediterranea was also significantly present during the cruise,

supporting previous observations reporting high cell densities of this species off the Nazar

region (Moita et al., 2010; Silva et al., 2008), and fast response to nutrient availability in this area

during winter (Guerreiro et al., 2013).

On the contrary, Syracosphaera spp. and Ophiaster spp. (negative loadings of Factor 1)

showed a higher affinity for warmer and saltier open ocean waters, and these species appeared

more broadly distributed along the water column (Figures 9a and 10a). Closer to the coast, these

species were generally less frequent, although higher cell densities were observed below the

surface, where they were apparently able to compete with E. huxleyi. This suggests that the lower

light and nutrient level within neritic subsurface waters were less limiting for these taxa than for

E. huxleyi. Results are consistent with Andruleit (2007) in terms of the broad depth range of

Syracosphaera spp. but not concerning the affinity of this group for nutrient availability in

coastal regions as reported in earlier studies (e.g. Andruleit, 2007; Andruleit and Rogalla, 2002;

Giraudeau and Bailey, 1995). Whereas SEM observations indicated that Syracosphaera

25

marginoporata was the dominant species within the group (max.1.4105 cells/l), the low level of

taxonomical differentiation of Syracosphaera spp. from the above mentioned studies may

explain the discrepancy between its reportedly association with relatively eutrophic conditions

and its preferential distribution in the relatively oligotrophic oceanic waters of the Nazar

Canyon region.

The same applies to Ophiaster spp. of which little is known yet in terms of both

ecological preferences and biogeographic distribution. Whereas our late winter observations

seem to indicate an association of this genus with oceanic-oligotrophic conditions, other studies

describe it as associated to nutrient-rich environments such as subtropical frontal zones and

upwelling areas (e.g. Boeckel and Baumann, 2008; Kleijne, 1993).

Discosphaera tubifera and Alisphaera spp. were not abundant during the cruise (

26

relatively oligotrophic signature of coccolithophore assemblages observed in subsurface waters

along the Nazar Canyon axis seems in favour of the hypothesis that the canyon acts as a

preferential pathway for advection of oceanic waters derived from ENACWst from offshore onto

more nearshore areas during winter (see section 5.2).

Gephyrocapsa oceanica appears to be related to turbidity, although the correlation is

somewhat weak (positive loadings of Factor 4). This species was consistently distributed closer

to the coast (< 10 km) at all water depths, particularly at the canyon head and adjacent shelf

(Figure 10d). The broad depth range of G. oceanica was also recognized by Andruleit (2007) and

Houghton and Guptha (1991), as well as its tolerance for lithogenic particles, which would be in

accordance with the occurrence of G. oceanica in the dynamic canyon head area; water samples

collected from this area displayed a highly content in terrigenous particles and reworked

coccoliths; see Appendix B). The coastal preference of G. oceanica is also in good agreement

with Silva et al. (2008) and Guerreiro et al. (2013; submitted), who described this species as a

typical coastal coccolithophore, well adapted to the nutrient-rich and productive environment off

Portugal. The species seems able to quickly respond to nutrient input (Andruleit and Rogalla,

2002; Andruleit et al., 2003; Broerse et al., 2000; Giraudeau and Bailey, 1995; Sprengel et al.,

2002; Winter et al., 1994). The relatively low cell densities of this species confirms the generally

low-productive conditions during the cruise.

5.2. Influence of the submarine canyon and hydrological conditions

Although phytoplankton production apparently had not yet responded to higher nutrient

availability provided by runoff, as revealed by generally low coccolithophore cell and Chl-a

27

concentrations (see section 5.1, Guerreiro et al., 2013), local abundance and diversity hotspots

were noticed in the upper Nazar Canyon axis close to Belatina Valley (stations 120 and 118)

and in the canyon head (station 87).

Of particular interest for the canyon head dynamics are the sporadic occurrences of

typical subtropical-oligotrophic species, such as Discosphaera tubifera and Palusphaera

vandelii. These species were only observed in this proximal part of the canyon and may be

interpreted as tracers for the preferential onflow of ENACWst through the upper canyon during

winter, as revealed by TS profiles along the Nazar Canyon axis (Figures 2a,b). Shoreward

deflection of circulation in the upper water column is expected to be stronger when the water

column above the shelf and upper slope is relatively unstratified (see Allen, 1996; She and

Klinck, 2000), as typically the case off Portugal during this time of the year (Oliveira et al.,

2004).

Along with these subtropical species, a diverse assemblage dominated by the productive

Emiliania huxleyi, Gephyrocapsa ericsonii and Coronosphaera mediterranea was observed in

the canyon head. Maxima of other species, both neritic-coastal (i.e. Gephyrocapsa oceanica,

Acanthoica spp.) and neritic-oceanic (i.e. Gephyrocapsa muellerae, Syracolithus dalmaticus and

Alisphaera spp.) were also observed in this area. Whereas during the low productive winter

season the shoreward advection of oceanic waters through the canyon can be traced by relatively

diverse coccolithophore assemblages with oligotrophic subtropical affinity, satellite data clearly

show a maximum in Chl-a concentration at the canyon head between March and October

suggesting that upwelling of oceanic waters in the canyon head enhances phytoplankton

productivity making the canyon head the most persistently productive part of the inner shelf zone

(Figures 11a,c). Also during the years of lower productivity a relative increase of Chl-a is

28

noticed at the canyon head. Previous observations from Mendes et al. (2011) had already

indicated that the highest Chl-a concentrations during an upwelling event occurred at the canyon

head (> 4 g/l).

Enhanced Chl-a concentrations observed in satellite imagery south of the Nazar Canyon

and close to Cape Carvoeiro supports previous observations of Mendes et al. (2011) of

persistently high concentrations of diatoms in this area, interpreted as reflecting the occurrence

of intensified upwelling along the southern canyon rim extending its influence over the southern

shelf, and persisting even during relaxation of upwelling-favourable winds. Enhancement of

upwelling in the canyon head and nearby shelf is in accordance with studiesof Bosley et al.

(2004), Hickey (1995) and Skliris and Djenidi (2006). However, the recurrent generation of

upwelling filaments off Cape Carvoeiro during spring-summer should also be considered when

explaining high production of phytoplankton in this area (e.g. Fiza, 1983; Haynes et al., 1993;

Peliz et al., 2002).

The region close to Belatina Valley, where the upper canyon axis makes a tight turn

(stations 120 and 118), also stood out for particular hydrological and ecological characteristics.

The highest phytoplankton biomass and coccolithophore cell densities during the cruise were

observed in this area, with E. huxleyi, G. ericsonii and C. mediterranea dominating the

assemblage in the uppermost 25 m of the water column. The lowest TS values and the highest

nutrient concentrations within the superficial BP were also measured here, whereas indications

of enhanced vertical baroclinic oscillation were noticed underneath the BP (Figures 2a,b),

interpreted as resulting from the interaction of internal waves with the canyon topography. The

conversion of barotropic to baroclinic tidal motion occurs in the presence of water stratification

and leads to the generation of internal (baroclinic) tides (i.e. internal waves of tidal period),

29

which radiate from the generation point and propagate the tidal energy vertically (Quaresma et

al., 2007; Tyler et al., 2009). The vertical density gradient existing between the BP (above) and

the ENACWst (below) within the confined topography of the upper canyon will likely promote

the baroclinic oscillation of the water masses involved. In addition, the presence of a meander in

this part of the canyon axis appears to block the flow of the internal wave, leading to local

amplification of the vertical oscillation. One could speculate that this represents a typical

hydrological feature of the canyon during wintertime, given that it is during this time of the year

that the IPC usually surfaces and reaches particularly nearshore areas within the canyon. During

summer, when the IPC retreats down to slope water depths, baroclinic activity near the surface is

mainly associated to water column thermo-haline stratification typical of this season (e.g.

Quaresma et al., 2007).

The highest cell and Chl-a concentrations measured in situ close to Belatina Valley may

be interpreted to merely represent a local expression of shelf-wide high phytoplankton

production recurrently occurring during the month of March (Figures 11a and 12b). Although

slightly higher monthly Chl-a concentrations appear to be roughly aligned with the canyon axis

in comparison to the northern shelf, in particular close to the meander (Figure 12b), it is very

hard to decipher whether this reflects a recurrent physical phenomenon related to the canyon or

merely an artefact produced by the satellite acquisition. Given that the regional Chl-a outbreak

observed in satellite imagery consistently occurs in late winter/early spring of most years,

occasionally also in early autumn, but never in full winter or full summer time, it is likely

representing the early spring and autumn phytoplankton bloom, controlled primarily by the

increase in light availability in spring and replenishment of nutrients in autumn (see Figure 12a).

The more intense offshore blooms recorded in March of 2006, 2009 and 2010 may result from

30

late-winter and early-spring runoff in combination with short-term northerly winds over the

shelf, a condition described by several authors (i.e. Guerreiro et al., 2013; Peliz and Fiza., 1999;

Ribeiro et al., 2005; Santos et al., 2004).

In situ measurements indicating enhanced productivity in the surroundings of Belatina

Valley should, therefore, primarily reveal the presence of a front generated between the BP and

the shelf-slope waters during a hydrologically and meteorologically highly transient period in

this region (Guerreiro et al., 2013). Nevertheless, in view of the particular location, other

phenomena could be invoked to explain the local phytoplankton increase, which may be too

short-lived and localized to be identified within monthly averaged Chl-a distribution maps.

As suggested above, the abrupt seabed topography of the Nazar Canyon is likely to

induce perturbations in the flow of water masses on the shelf. Fronts between relatively

productive coastal water masses and less-productive open ocean water masses will tend to

meander across the canyon, adding complexity to spatial distribution of particulate matter in the

surface water. Since the sampling cruise took place during the winter-spring transition when the

water masses were still adjusting, the canyon topography might be expected to have a noticable

influence on the circulation. In contrast, during typical summer-conditions, wind forcing will

play a more prominent role in determining surface water circulation.

Belatina Valley appears to be a region of significant topographic effect on the front of the

low salinity BP, as indicated by the occurrence of the strongest vertical density gradients in this

area. Quaresma (2012) reported on the existence of a barotropic water mass flux of convergent-

divergent periodic motion between the interior of the canyon and the shelf close to Belatina

Valley, driven by the barotropic onshore-offshore water flow. According to this author, the

canyon axis acts as drain for shelf water at this location during every low tide. This water

31

exchange may result in the concentration of nutrients within the surface water layer, whose time-

integrated effect would result in a local nutrient-enrichment favorable for phytoplankton growth.

Several modeling studies revealed the importance of ocean currents interacting with submarine

canyons, enhancing productivity and influencing phytoplankton distribution by funneling and

trapping plankton within the canyons. These studies highlight the predominant effect of local

primary production on the canyon food web, in comparison to other potential sources (Bosley et

al., 2004; Macquart-Moulin and Patriti, 1996; Skliris and Djenidi, 2006).

In addition, one could speculate that internal tidal pumping driven by intensified vertical

baroclinic oscillation around Belatina Valley could contribute to phytoplankton growth in this

area, similar to what has recently been described from Monterey Canyon (California, USA) by

Ryan et al. ( 2005; 2010). These authors described the upsurge of a wedge-shaped tongue of

cold, dense water from the canyon, flowing up onto the continental shelf. The intruding water

mass was observed to entrain a plume of nutrient-rich turbid water from the seafloor up to the

surface, above which high concentrations of phytoplankton were observed. In the Nazar

Canyon, during a cruise performed in November 2002, a vertical turbid plume was observed at

the Belatina Valley area, extending upward from a level of intense intermediate nepheloid layers

at 800-900 m water depths to about 300 m. This plume was interpreted as reflecting resuspension

by the canyons internal tide, enhanced by the strong density gradient between the ENACW

(above) and the denser Mediterranean Outflow Water (MOW) (below) (Oliveira et al., 2007).

Such baroclinic vertical oscillation, amplified in the canyon meander, may be responsible for

bringing nutrients from below the canyon rim during winter, promoting phytoplankton growth in

the upper part of the water column. However, our water column turbidity profiles and vertical

distribution of coccolithophores and nutrients show no evidence of the occurrence of this process

32

during the investigated late winter period, where enhanced nutrient concentrations appeared

predominantly associated with the BP (see Guerreiro et al., 2013). Baroclinic activity is more

likely to gain in importance during stratified summer conditions.

5.3. Satellite data versus in situ measurements

Our observations, both long-term Chl-a concentrations obtained from satellite data and in

situ quantification, suggest that the Nazar Canyon may locally favor, at least indirectly, the

development of phytoplankton, including coccolithophores. This is the case for the canyon head,

which appears to be the stage of recurrent higher productivity in comparison to the adjacent

shelf. However, in the case of Belatina Valley, where in situ observations revealed local Chl-a

and coccolithophore cell enhancement, monthly averaged productivity obtained from satellite

suggest that enhanced Chl-a production was not confined to that specific area but occurred over a

much wider area including most of the shelf, (transect B, Figure 12b).

On the one hand, lacking in situ observations from outside the canyon, we cannot

ascertain whether higher Chl-a and cell densities obtained from this area are actually confined to

the canyon axis, or are part of a larger pattern not necessarily related to the canyon. On the other

hand, it cannot be expected that monthly Chl-a averages obtained from satellite data will match

exactly the coccolithophore and Chl-a peaks measured in situ and only representing one instant

of the annual productivity. Different spatial and temporal scales are involved: whereas the

satellite data reveal patterns of phytoplankton distribution at the surface at relatively high

resolution, insight of phytoplankton productivity at deeper levels in the water column can only

be obtained from in situ measurements. Differences between the two will expectedly be largest

33

under the highly transient meteorological and oceanographic conditions characteristic of the late

winter period, as prevailing during the cruise.

Intensified baroclinic activity at Belatina Valley might well promote biological

production events that are too deep and short-lived to be detected by monthly Chl-a averages

obtained by satellite. The rapid response of certain species of coccolithophores to regional

meteorological and hydrological variations off central Portugal was recently demonstrated by

Guerreiro et al. (2013). Satellite imagery has a tremendous potential to describe larger-scale

phenomena prevailing on the Portuguese margin, but it may not be the best approach to

investigate smaller-scale processes, for which higher temporal and spatial resolution are probably

required

Validation of hypotheses presented here requires additional sampling surveys integrated

with meteorological and hydrological monitoring in order to address the seasonal and interannual

variability of phytoplankton (in general) and coccolithophores (in particular), in relation with

physical processes in the Nazar Canyon.

6. Conclusions

This study is the first attempt to characterize coccolithophore assemblages occurring in

the context of an active submarine canyon. A late winter low-productive period was investigated

in the Nazar Canyon (off central Portugal) during which warm and saline waters fed by the IPC

were still strongly influencing the hydrology of the shelf and slope, and the winter mixed layer

occupied the entire water column of the shelf-upper slope. The canyon was clearly acting as a

conduit for the onshore advection of relatively nutrient-poor oceanic waters to very nearshore

34

areas (less than 10 km off the coast).

Runoff prior and during the cruise was an important source of nutrients into the system,

as indicated by high nutrient concentrations that were measured in the relatively low saline

buoyant plume overlying the winter mixed layer in the coastal zone. Nevertheless, the weak

correlation of nutrients with biomass suggests that phytoplankton production had not yet

responded to higher nutrient availability, probably resulting from important advective mixing

promoted by the BP during this period of intense runoff, sub-optimal light conditions due to

cloud cover and initial relatively high suspended sediment load within the surface water layer

(discussed in Guerreiro et al., submitted).

Two main coccolithophore assemblages were distinguished, representing the gradient

between the runoff-influenced coastal-neritic zone and the oceanic mixed water conditions that

characterize the Portuguese margin during winter: (1) Emiliania huxleyi was the dominant taxon

at the surface within more coastal-neritic conditions and, together with Gephyrocapsa ericsonii

and Coronosphaera mediterranea, represent the more productive assemblage during the

sampling period. (2) Syracosphaera spp. and Ophiaster spp. showed a clearly higher affinity for

open-ocean conditions, displaying a generally broader vertical distribution. Closer to the coast,

these taxa were able to compete well with E. huxleyi in the subsurface layer, suggesting that

lower light and nutrient level within more neritic conditions were less limiting for Syracosphaera

spp. and Ophiaster spp. as it was for E. huxleyi.

Chl-a time series obtained from satellite data suggest that the Nazar Canyon head is

often the stage of high productivity between March and October, which makes the canyon head

the most persistently productive part of the upper-middle canyon. In situ observations also

revealed a coccolithophore diversity hotspot in this area, including both oligotrophic-oceanic

35

and opportunistic-coastal taxa. The single occurrence of typically subtropical-oligotrophic

species (i.e. Discosphaera tubifera, Palusphaera vandelii, Calcidiscus leptoporus) is interpreted

as indicative for the shoreward flow of ENACWst intensified along the upper canyon during

winter. In addition to these species, a diversified assemblage dominated by the productive E.

huxleyi, G. ericsonii and C. mediterranea, together with other species which have their

maximum occurrence in the canyon head area including both neritic/coastal (i.e. Gephyrocapsa

oceanica, Acanthoica spp.) and neritic/oceanic species (i.e. Gephyrocapsa muellerae,

Syracolithus dalmaticus, Alisphaera spp. and Michaelsarsia elegans) may also reflect exchange

of water masses between neritic-coastal and oceanic regions through the canyon during winter.

Local enhancement of nutrient concentration and coccolithophore cell concentration was

observed near the Belatina Valley, with E. huxleyi, G. ericsonii and C. mediterranea dominating

the assemblage at the uppermost 25 m of the water column. In addition, monthly averaged

satellite data reveal slightly higher Chl-a concentrations apparently roughly aligned with the

canyon axis, close to Belatina Valley. We hypothesize that this imprint may be tracing the time-

integrated effect of barotropic water mass flux into Belatina Valley and the meandering of the

low-salinity front into this location. Based on our in situ observations and on recent studies

identifying this narrower part of the canyon axis as an area of intensified vertical water

movement, we suggest that Belatina Valley may potentially be a favourable region for

phytoplankton local enhancement.

Results presented here provide some valuable indications with regards to the important

and persistet influence of the Nazar Canyon on the ecology and distribution of coccolithophores

and phytoplankton biomass at the central Portuguese margin. The results highlight the need of

long-term multi-proxy investigations in order to address the seasonal and interannual variability

36

in phytoplankton in relation with the seasonal- and/or topographically driven physical

phenomena associated with the Nazar Canyon.

Acknowledgements

This research was supported by the HERMIONE project (EC contract 226354) funded by

the European Commission and the Cd Tox-CoN project (FCT-PTDC/MAR/102800/2008)

funded by the Portuguese Science Foundation FCT. The first author benefits from an FCT PhD

grant (FRH/BD/41330/2007). Filter samples were collected during the 2nd

HERMIONE cruise of

the Portuguese Hydrographic Institute (IH) on board of NRP Almirante Gago Coutinho. The

authors are grateful to all the crew of the NRP Almirante Gago Coutinho and several researchers

participating in the cruise for their valuable help during the collection of samples. A special

thanks to the OC-IH CTD data acquisition team, Joo Vitorino, Manuel Marreiros, Ins Martins,

Vnia Carvalho and Nuno Zacarias, and to Manuela Valena (QP-IH) for performing the

compilation of nutrient data. All the samples were prepared and analyzed at NANOLAB,

Geology Centre of Lisbon University (CEGUL). SEM observations were performed at the

Institut de Cincies del Mar (ICM CSIC, Barcelona, Spain). Constructive criticism and helpful

suggestions from two anonymous reviewers are most gratefully acknowledged by the authors.

References

Allen, S. E., 1996. Topographically generated, subinertial flows within a finite length canyon.

Journal of Physical Oceanography 26, 1608-1632.

37

Alvarez, I., Gomez-Gesteira, M., de Castro, M., Lorenzo, M. N., Crespo, A. J. C., Dias, J.M.,

2011. Comparative analysis of upwelling influence between the western and northern coast of

the Iberian. Continental Shelf Research 31(5), 388-399.

Andruleit, H., 2007. Status of the Java upwelling area (Indian Ocean) during the oligothrophic

northern hemisphere winter monsoon season as revealed by coccolithophores. Marine

Micropaleontology 64, 36-51.

Andruleit, H., Rogalla, U., 2002. Coccolithophores in surface sediments of the Arabian Sea in

relation to environmental gradients in surface waters. Marine Geology 186, 505-526.

Andruleit, H., Stager, S., Rogalla, U., Cepek, P., 2003. Living coccolithophores in the northern

Arabian Sea: ecological tolerances and environmental control. Marine Micropaleontology 49,

157- 181.

Barton, E., 2001. Canary and Portugal currents. In: Steele, J., Turekian, K., Thorpe, S. (Eds.), In:

Encyclopedia of Ocean Sciences, vol. 1. Academic Press, 380-389.

doi:10.1006/rwos.2001.0360.

Baumann, K.-H., Andruleit, H. A., Samtleben, C., 2000. Coccolithophores in the Nordic Seas:

comparison of living communities with surface sediment assemblages. Deep-Sea Research II

47, 1743-1772.

Boeckel, B., Baumann, K.-H., 2008. Vertical and lateral variations in coccolithophore

community structure across the subtropical frontal zone in the South Atlantic Ocean. Marine

Micropaleontology 76, 255-273.

Bosley, K. L., Lavelle, J. W., Brodeur, R. D., Wakefield, W. W., Emmett, R. L., Baker, E. T.,

Rehmke, K. M., 2004. Biological and physical processes in and around Astoria submarine

Canyon, Oregon, USA. Journal of Marine Systems 50, 21-37.

38

Broerse, A. T. C., Ziveri, P., van Hinte, J. E., Honjo, S., 2000. Coccolithophore export

production, species composition and coccolith-CaCO3 fluxes in the NE Atlantic (34N 21W

and 48N 21W). Deep-Sea Research II 47, 1877-1906.

Bruno, M., Vzquez, A., Gmez-Enria, J., Vargas, J. M., Lafuente, J. G., Ruiz-Caavate, A.,

Mariscal, L., Vidal, J., 2006. Observations of internal waves and associated mixing

phenomena in the Portimao Canyon area. Deep Sea Research Part II: Topical Studies in

Oceanography 53 (11-13), 1219-1240.

Cattiaux, J., Masson-Delmotte,V., Vautard, R., Yiou, P., Cassou, C., Codron, F., 2010. Winter

2010 in Europe: A cold extreme in a warming climate. Geophysical Research Letters

10.1029/2010GL044613.

Cros, L., 2001. Planktonic coccolithophores of the NW Mediterranean. PhD Thesis, Universitat

de Barcelona, 181pp.

Cros, L., Fortuo, J.-M. 2002. Atlas of Northwestern Mediterranean coccolithophores. Scientia

Marina 66 (1), 1-186.

De Stigter, H., Boer, W., Mendes, P., Jesus, C., Thomsen, L., van den Bergh, G., van Weering,

T., 2007. Recent sediment transport and deposition in the Nazar Canyon, Portuguese

continental margin. Marine Geology 256, 144-164.

Dimiza, M. D., Triantaphyllou, M. V., Dermitzakis, M. D., 2008. Seasonality and ecology of

living coccolithophores in Eastern Mediterranean coastal environments (Andros Island,

Middle Aegean Sea). Micropaleontology 54 (2), 159-175.

Durrieu de Madron, X., 1994. Hydrology and nepheloid structure in the Grand-Rhne canyon.

Continental Shelf Research 14, 457-477.

39

Fiza, A., 1983. Upwelling patterns off Portugal. In: E. Suess and J. Thie (Eds). Coastal

Upwelling: Its sediment Record. Plenum, New York, 85-98.

Fiza, A. F. G., 1984. Hidrologia e dinmica das guas costeiras de Portugal (Hydrology and

dynamics of the Portuguese coastal waters). PhD. dissertation, Universidade de Lisboa, 294

pp.

Fiza, A. F. G., Hamann, M., Ambar, I., Del Ro, G., Gonzlez, N., Cabanas, J., 1998. Water

masses and their circulation off western Iberia during May 1993. Deep Sea Research Part I:

Oceanographic Research Papers 45 (7), 1127-116.

Frada, M., Young, J., Cacho, M., Lino, S., Martins, A., Probert, I., de Vargas, C. 2010. A guide

to extant coccolithophores (Calcihaptophycidae, Haptophyta) using light microscopy. 2010.

Journal of Nannoplankton Research 31 (2), 58-112.

Garcia, C., Garcia, V., Dogliotti, A., Ferreira, A., Romero, S., Mannino, Souza, M. S., Mata, M.

M., 2011. Environmental conditions and bio-optical signature of a coccolithophore bloom in

the Patagonian shelf. Journal of Geophysical Research, doi:10.1029/2010JC006595.

Gardner, W. D., 1989. Baltimore Canyon as a modern conduit of sediment to the deep sea. Deep-

Sea Research 36, 323-358.

Giraudeau, J., Bayley, G. W., 1995. Spatial dynamics of coccolithophore communities during an

upwelling event in the Southern Benguela system. Continental Shelf Research 15, 1825-1852.

Guerreiro, C., de Stigter, H., Cacho, M., Oliveira, A., Rodrigues, A., submitted. Coccoliths

from recent sediments of the Central Portuguese Margin: taphonomical and ecological

inferences. Marine Micropaleontology.

40

Guerreiro, C., Oliveira, A., Cacho, M., de Stigter, H., S, C., Borges, C., Cros, C., Santos, A.,

Rodrigues, A., 2013. Late winter coccolithophore bloom off central Portugal in response to

river discharge and upwelling. Continental Shelf Research 59, 65-83.

Guerreiro, C., Rosa, F., Oliveira, A., Cacho, M., Fatela, F., Rodrigues, A., 2009. Calcareous

nannoplankton and benthic foraminiferal assemblages from the Nazar Canyon (Portuguese

continental margin): preliminary results. IOP Conference Series: Earth and Environmental

Science 5012004, 11pp.

Haynes, R., Barton, E. D., Pilling, I., 1993. Development, persistence and variability of

upwelling filaments off the Atlantic coast of the Iberian Peninsula. Journal of Geophysical

Research 98, 22681-22692.

Hickey, B. M., 1995. Coastal Submarine Canyons. In: Proceedings Aha Huliko'a Hawaiian

Winter Workshop 1995, Topographic Effects in the Ocean, 95-110.

Hickey, B. M., 1997. The response of a steep-sided, narrow canyon to time-variable wind

forcing. Journal Physical Oceanography 27, 697-726.

Hickey, B.M., Baker, E., Kachel, N., 1986. Suspended particle movement in and around

Quinault Submarine Canyon. Marine Geology 71, 35-83.

Houghton, S. D., Guptha, M. V. S., 1991. Monsoonal and fertility controls on Recent marginal

sea and continental shelf coccolith assemblages from the western Pacific and northern Indian

oceans. Marine Geology 97, 251-259.

Huthnance, J. M., van Aken, H., White, M., Barton, E. D., Le Cann, B., Coelho, E. F., Fanjul, E.

A., Miller, P., Vitorino, J., 2002. Ocean margin exchangewater flux estimates. Journal of

Marine Systems 32, 107-137.

41

Jordan, R., Cros, L., Young, J., 2004. A revised classification scheme for living haptophytes.

Micropaleontology 50 (1), 5579.

Kampf, J., 2006. Transient wind-driven upwelling in a submarine canyon: A process-oriented

modelling study. Journal of Geophysical Research 111 (C11011) doi:10.1029/2006JC003497

Kleijne, A., 1992. Extant Rhabdosphaeraceae (coccolithophorids, class Prymnesiophyceae) from

the Indian Ocean, Red Sea, Mediterranean Sea and North Atlantic Ocean. Scripta Geologica

100, 1-63.

Kleijne, A., 1993. Morphology, Taxonomy and Distribution of extant coccolithophorids

(calcareous nannoplankton). Ph.D. Thesis, Vrije Universiteit, Amsterdam.

Kleijne, A., Cros, L. 2009. Ten new extant species of the coccolithophore Syracosphaera and a

revised classification scheme for the genus. Micropaleontology 55 (5), 425-462.

Klinck, J. M., 1988. The influence of a narrow transverse canyon on initially geostrophic flow.

Journal of Geophysical Research 93, 509-515.

Klinck, J. M., 1996. Circulation near submarine canyons: a modelling study. Journal of

Geophysical Research 101, 1211-1223.

Knappertsbusch, M., Brummer, G.-J. A., 1995. A sediment trap investigation of sinking

coccolithophores in the North Atlantic. Deep-Sea Research Part I 42 (7), 1083-1109.

Koroleff, F., 1976. Determination of ammonia. In: Grasshoff, K. (Ed.), Methods of Seawater

Analysis. Verlag Chemie, New York, 126158.

Lastras, G., Arzola, R., Masson, D., Wynn, R., Huvenne, V., Huhnerbach, V., Canals, M., 2009.

Geomorphology and sedimentary features in the Central Portuguese submarine canyons,

Western Iberian margin. Geomorphology 103, 310-329.

42

Macquart-Moulin, C., Patriti, G., 1996. Accumulation of migratory micronekton crustaceans

over the upper slope and submarine canyons of the northwestern Mediterranean. Deep-Sea

Research 43, 579-601.

McCave, I., Hall, I., 2002. Turbidity of waters over the Northwest Iberian continental margin.

Progress in Oceanography 52, 299-313.

Mendes, R., S, C., Vitorino, J., Borges, C., Garcia, V., Brotas, V., 2011. Distribution of

phytoplankton assemblages in the Nazar submarine canyon region (Portugal): HPLC-

CHEMTAX approach. Journal of Marine Systems 87, 90-101.

doi:10.1016/j.jmarsys.2011.03.005

Moita, M. T., 2001. Estrutura, Variabilidade e Dinmica do Fitoplncton na Costa de Portugal

Continental. PhD Thesis, Faculdade de Cincias da Univ. de Lisboa, 272 pp.

Moita, M. T., Silva, A., Palma, S., Vilarinho, M. G., 2010. The coccolithophore summerautumn

assemblage in the upwelling waters of Portugal: Patterns of mesoscale distribution (1985

2005). Estuarine, Coastal and Shelf Science 87, 411-419.

Monaco, A., Durrieu de Madron, X., Rodacovitch, O., Huessner, S., Carbone, J., 1999. Origin

and variability of downward biogeochemical fluxes on the Rhne continental margin (NW

Mediterranean). Deep Sea Research I 46, 1483-1511.

Murphy, J., Riley, J. P., 1962. A modified single solution method for the determination of

phosphate in natural waters. Analytica Chimica Acta 27, 3136.

Oliveira, A., Santos, A. I., Rodrigues, A., Vitorino, J., 2007. Sedimentary particle distribution

and dynamics on the Nazar canyon system and adjacent shelf (Portugal). Marine Geology

246, 105-122.

43

Oliveira, P. B., Peliz, A., Dubert, J., Rosa, R. T., Santos, A. M. P., 2004. Winter geostrophic

currents and eddies in the western Iberia coastal transition zone. Deep-Sea Research I 51, 36-

381.

Otero, P., Ruiz-Villarreal, M., Peliz, A., 2008. Variability of river plumes off Northwest Iberia in

response to wind events. Journal of Marine Systems 72, 238-255.

Peliz, A., Dubert, J., Santos, A. M. P., Oliveira, P. B., Le Cann, B., 2005. Winter upper ocean

circulation in the Western Iberian Basin Fronts, Eddies and Poleward Flows: an overview.

Deep Sea Research I 52, 621-646.

Peliz, A. J., Fiza, A. F. G., 1999. Temporal and spatial variability of CZCS-derived

phytoplankton pigment concentrations off the western Iberian Peninsula. International Journal

Remote Sensing 20 (7), 1363-1403.

Peliz, A., Rosa, T., Santos, A. M. P., Pissarra, J., 2002. Fronts, jets, and counter-flows in the

Western Iberia Upwelling System. Journal of Marine Systems 35, 6177.

Pollard, R., Pu, S., 1985. Structure and circulation of the upper Atlantic Ocean northeast of the

Azores. Progress in Oceanography 14, 443-462.

Puig, P., Ogston, A. S., Mullenbach, B. L., Nittrouer, C. A., Sternberg, R. W., 2003. Shelf-to-

canyon sediment-transport processes on the Eel continental margin (northern California).

Marine Geology 193, 129-149.

Quaresma, L. S., 2012. Super-Inertial Tides Over Irregular Narrow Shelves, Ph.D thesis,

Universit de Bretagne Occidentale, Brest, France, 172 pp.

Quaresma, L. S., Pichon, A., 2011. Modelling the barotropic tide along the West-Iberian margin.

Journal of Marine Systems, http://dx.doi.org/10.1016/j.jmarsys.2011.09.016

44

Quaresma, L. S., Vitorino, J., Oliveira, A., Silva, J., 2007. Evidence of sediment resuspension by

nonlinear internal waves on the western Portuguese mid shelf. Marine Geology 246, 123-143.

Relvas, P., Barton, E. D., Dubert, J., Oliveira, P. B., Peliz, A., da Silva, J. C. B., Santos, A. M.

P., 2007. Physical oceanography of the western Iberia ecosystem: Latest views and

challenges. Progress in Oceanography 74, 149-173.

Ribeiro, A., Peliz, A., Santos, M. P., 2005. A study of the response of chlorophyll-a biomass to a

winter upwelling event off Western Iberia using SeaWiFS and in situ data. Journal of Marine

Systems 53, 87-107.

Ryan, J. P., Dierssen, H. M., Kudela, R. M., Scholin, C. A., Johnson, K. S., Sullivan, J. M.,

Fischer, A. M., Rienecker, E. V., McEnaney, P. R., Chavez, F. P., 2005. Coastal ocean

physics and red tides: an example from Monterey Bay, California. Oceanography 18, 246-

255.

Ryan, J. P., McManus, M., Sullivan, J. M., 2010. Interacting physical, chemical and biological

forcing of phytoplankton thin-layer variability in Monterey Bay, California. Continental Shelf

Research 30, 7-16.

Santos, A. M. P., Peliz, A., Dubert, J., Oliveira, P. B., Anglico, M. M., R, P., 2004. Impact of a

winter upwelling event on the distribution and transport of sardine (Sardina pilchardus) eggs

and larvae off western Iberia: a retention mechanism. Continental Shelf Research 24, 149-

165.

Saunders, P., 1982. Circulation in the eastern North Atlantic. Journal of Marine Research 40,

641657.

She, J., Klinck, J. M., 2000. Flow near submarine canyons driven by constant winds. Journal

Geophysical Research 105, 28671-28694.

45

Silva, A., Palma, S. , Moita, M. T., 2008. Coccolithophores in the upwelling waters of Portugal:

Four years of weekly distribution in Lisbon bay. Continental Shelf Research 28, 2601-2613.

Silva, A., Palma, S., Oliveira, P. B., Moita, M.T., 2009. Composition and interannual variability

of phytoplankton in a coastal upwelling region (Lisbon Bay, Portugal). Journal Sea Research

62, 238-249.

Skliris, N., Djenidi, S., 2006. Plankton dynamics controlled by hydrodynamic processes near a

submarine canyon off NW corsican coast: A numerical modelling study. Continental Shelf

Research 26, 1336-1358.

Skliris, N., Hecq, J. H., Djenidi, S., 2002. Water fluxes at an ocean margin in the presence of a

submarine canyon. Journal of Marine Systems 32, 239-251.

Skliris, N., Lacroix, G., Djenidi, S., 2004. Effects of extreme meteorological conditions on

coastal dynamics near a submarine canyon. Continental Shelf Research 24, 1033-1045.

Sprengel, C., Baumann, K.-H., Henderiks, J., Henrich, R., Neuer, S., 2002. Modern

coccolithophore and carbonate sedimentation along a productivity gradient in the Canary

Islands region: seasonal export production and surface accumulation rates. Deep-Sea

Research II 49, 3577-3598.

Strickland, J. D. H., Parsons, T. R., 1972. A Practical Handbook of Seawater Analysis. Fisheries

Research Board of Canada, Ottawa.

Troupin, C., Machn, F., 2012. Negative wind anomalies generated a diminution of productivity

in the North Atlantic in 2010. EGU General Assembly, Vienna.

http://hdl.handle.net/2268/123991.

Tyler, P., Amaro, T., Arzola, R., Cunha, M., de Stigter, H., Gooday, A., Huvenne, V., Ingels, J.,

Kiriakoulakis, K., Lastras, G., Masson, D., Oliveira, A., Pattenden, A., Vanreusel, A., van

46

Weering, Vitorino, J., Witte, U., Wolf, G., 2009. Europes Grand Canyon: Nazar submarine

canyon. Oceanography 22 (1), 46-57.

Vanney, J., Mougenot, D., 1990. Un canyon sous-marin du type gouf: le Canho da Nazar

(Portugal). Oceanologica Acta 13, 13-14.

Vitorino, J., Oliveira, A., Jouanneau, J. M., Drago, T., 2002. Winter dynamics on the northern

Portuguese shelf. Part 1: physical processes. Progress in Oceanography 52, 129-153.

Wallace, J. M., 2002. Two faces of the North Atlantic Oscillation (NAO). Luso-American

Foundation, Lisbon, Portugal, 41pp.

Winter, A., Jordan, R., Roth, P., 1994. Biogeography of living coccolithophores in ocean waters.

In: A. Winter and W. Siesser (Eds). Coccolithophores. Cambridge University Press,

Cambridge, 161-177.

Winter, A., Reiss, Z., Luz, B., 1979. Distribution of living coccolithophore assemblages in the

Gulf of Elat (Aqaba). Marine Micropaleontology 4, 197-223.

Young, J., 1994. Functions of coccoliths. In: A. Winter and W. Siesser (Eds). Coccolithophores.

Cambridge University Press, Cambridge, 63-82.

Young, J. R., Bown P. R., Lees J. A. (eds) Nannotax website. International Nannoplankton

Association. 21 Sept 2011. URL: http://nannotax.org

Young, J., Geisen, M., Cros, L., Kleijne, A., Sprengel, C., Probert, I., stergaard, J.B., 2003. A

guide to extant calcareous nannoplankton taxonomy. Journal of Nannoplankton Research,

Special Issue 1, 1-125.

Zapata, M., Rodriguez, F., Garrido, J. L., 2000. Separation of chlorophylls and carotenoids from

marine phytoplankton: a new HPLC method using a reversed phase C8 column and pyridine-

containing mobile phases. Marine Ecology Progress Series 195, 29-45.

47

Appendix A

The taxonomic list includes, in alfabetical order, all taxa identified during the present study.

Acanthoica quattrospina Lohmann 1903

Acanthoica spp. Lohmann 1903; emend. Schiller 1913, Kleijne 1992

Algirosphaera robusta (Lohmann 1902) Norris 1984

Alisphaera extenta Kleijne et al. 2002

Alisphaera ordinata (Kamptner 1941) Heimdal 1973

Alisphaera pinnigera Kleijne et al. 2002

Braarudosphaera bigelowii (Gran et Braarud 1935) Deflandre 1947

Calcidiscus leptoporus (Murray et Blackman, 1898) Loeblich et Tappan, 1978

Coccolithus pelagicus subsp. braarudii (Gaarder, 1962) Geisen et al., 2002

Coronosphaera mediterranea. (Lohmann 1902) Gaarder in Gaarder and Heimdal 1977

Discosphaera tubifera (Murray et Blackman 1898) Ostenfeld 1900

Emiliania huxleyi (Lohmann, 1902) Hay et Mohler in Hay et al.,1967

Gephyrocapsa ericsonii McIntyre et B, 1967

Gephyrocapsa muellerae Brhret, 1978

Gephyrocapsa oceanica Kamptner, 1943

Helicosphaera carteri (Wallich, 1877) Kamptner, 1954

Michaelsarsia elegans Gran 1912; emend. Manton et al. 1984

Ophiaster formosus Gran 1912 emend. Manton et Oates 1983

Ophiaster hydroideus (Lohmann 1903) Lohmann 1913; emend. Manton et Oates 1983