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OPEN 3 ACCESS Freely available online
ONE
Deep-Sea Bioluminescence Blooms after Dense Water
Formation at the Ocean Surface
Christian Tam burini1'2*, Miquel Canals3, Xavier Durrieu d e M adron4, Loïc H oupert4,
D om inique Lefèvre1'2, S éverin e Martini1'2, Fabrizio D'O rtenzio5, A nne R obert1'2, Pierre T estor6, Juan
A n ton io A guilar7, Imen Al Sam arai8, Arnaud Albert9, Michel A ndré10, Marco A n gh in olfi11, Gisela A n ton 12,
S hebli Anvar13, M iguel Ardid14, Ana Carolina A ssis J esu s15, Tri L. A straatm adja1503, JeanJacq u es A ubert8, Bruny Baret16, S tép h an e B asa17, V incent Bertin8, Sim one Biagi18'19, Arm ando Bigi20,
Ciro B igongiari7, Claudio B ogazzi15, Manuel B ou-C abo14, B outayeb B ouh ou 16, M ieke C. B ouw huis15,
Jurgen Brunner8ab, José B usto8, Francisco Cam arena14, A n ton io C apone21'22, Christina Cârloganu23,
Giada Carminati18'1900, John Carr8, S tefan o C ecchini18'24, Ziad Charif8, Philippe Charvis25,
T om m aso Chiarusi18, Marco Circella26, Rosa C on iglion e27, H eide C ostantini8'11, Paschal C oyle8,
Christian Curtil8, Patrick D ecow sk i15, Ivan D ek eyser1'2, A nne D esch am p s25, Corinne D on zau d 16'28,
Dam ien Dornic7'8, H asankiadeh Q. D orosti29, D oriane Drouhin9, T hom as Eberl12, U m berto E m anuele7,
Jean-Pierre Ernenwein8, S tép h an ie Escoffier8*, P aolo Fermani21'22, M arcelino Ferri14,
V in cen zo Flam inio20'30, Florian F olger12, Ulf Fritsch12, Jean-Luc Fuda1,2Bd, Salvatore G alatà8,
Pascal Gay23, G iorgio G iacom elli18'19, V alentina G iordano27, Juan-Pablo G óm ez-G onzález7, Kay Graf12,
G oulven G uillará23, G aradeb H alladjian8, G regory H allew ell8, Hans van Haren31, Joris Hartm an15,
Aart J. H eijboer15, Yann H ello25, Juan J o se H ernández-R ey7, Bjoern H erold12, Jurgen H ößl12, ChingC heng H su15, M arteen d e J o n g 1503, M atthias Kadler32, O leg Kalekin12, A lexander K appes12, Uii Katz12,
O ksana K avatsyuk29, Paul K ooijm an15'33'34, Claudio K opper12, A n toin e K ouchner16,
Ingo K reykenbohm 32, Vladimir K ulikovskiy11'35, Robert Lahm ann12, Patrick Lamare13,
G iuseppina Larosa14, Dario Lattuada27, G ordon Lim15'34, D om en ico Lo Presti36'37, Herbert Loehner29,
Sotiris L oucatos38, Salvatore M an gan o7, Michel M arcelin17, Annarita M argiotta18'19, Juan
A n ton io M artinez-M ora14, Athina M eli12, Teresa M ontaruli26'39, Luciano M o sco so 16'38t, H olger M otz12,
Max N eff12, Emma nuel Nezri17, Dimitris P alioselitis15, Gabriela E. Pâvâlaç40, Kevin Payet38,
Patrice Payre8, Jelena P etrovic15, Paolo Piattelli27, Nicolas Picot-C lem ente8, Vlad P op a40,
Thierry Pradier41, Eleonora Presani15, Chantai Racca9, Corey R eed15, G iorgio R iccobene27,
Carsten Richardt12, Roland Richter12, Colas Rivière8, Kathrin R oensch 12, Andrei R ostovtsev42,
Joaquin Ruiz-Rivas7, Marius Rujoiu40, Valerio G. Russo36'37, Francisco S alesa7, A ugustin Sánchez-L osa7,
Piera S ap ien za27, Friederike S ch ock 12, Jean-Pierre Schuller38, Fabian Schussler38, Rezo S h an id ze12,
Francesco S im eon e21'22, A ndreas S p ies12, M aurizio Spurio18'19, Jos J. M. S teijger15, Thierry Stolarczyk38,
Mauro G. F. Taiuti11'43, Sim ona T oscan o7, Bertrand V allage38, V éronique Van Elewyck16,
Giulia V annoni38, M anuela V ecchi8, Pascal Vernin38, Guus Wijnker15, Jorn W ilms32, Eis d e W olf15'34,
Harold Y ep es7, Dmitry Z aborov42, Juan De D ios Z ornoza7, Juan Z úñiga7
1 Aix Marseille Université, CNRS/INSU, IRD, Mediterranean Institute of Oceanography (MIO), UM 110, Marseille, France, 2 Université de Toulon, CNRS/INSU, IRD,
Mediterranean Institute of Oceanography (MIO), UM 110, La Garde, France, 3GRC Geociències Marines, Departament d'Estratigrafia, Paleontología i Geociències Marines,
Facultat de Geología, Universität de Barcelona, Campus de Pedralbes, Barcelona, Spain, 4 Université de Perpignan, CNRS-INSU, CEFREM UMR5110, Perpignan, France,
5 Université Pierre & Marie Curie, CNRS-INSU, LOV UMR7093, Villefranche-sur-mer, France, 6 Université Pierre & Marie Curie, CNRS-INSU, Institut Pierre Simon Laplace,
LOCEAN UMR 7159, Paris, France, 7IFIC - Instituto de Física Corpuscular, Edificios Investigación de Paterna, CSIC - Universität de Valéncia, Apdo. de Correos, Valencia,
Spain, 8 CPPM - Aix-Marseille Université, CNRS/IN2P3, Marseille, France, 9 GRPHE - Institut universitaire de technologie de Colmar, Colmar, France, 1 0 Technical University
of Catalonia, Laboratory of Applied Bioacoustics, Barcelona, Spain, 11 INFN - Sezione di Genova, Genova, Italy, 12 Friedrich-Alexander-Universität Erlangen-Nürnberg,
Erlangen Centre for Astroparticle Physics, Erlangen, Germany, 13 Direction des Sciences de la Matière - Institut de recherche sur les lois fondamentales de l'Univers Service d'Electronique des Détecteurs et d'informatique, CEA Saclay, Gif-sur-Yvette, France, 14 Institut d'Investigació per a la Gestió Integrada de les Zones Costaneres
(IGIC) - Universität Politécnica de Valéncia, Gandia, Spain, 15 Nikhef, Amsterdam, The Netherlands, 16APC, Université Paris Diderot, CNRS/IN2P3, CEA/IRFU, Observatoire
de Paris, Sorbonne Paris Cité, Paris, France, 17 Aix Marseille Université, CNRS, LAM (Laboratoire d'Astrophysique de Marseille) UMR 7326, Marseille, France, 18 INFN Sezione di Bologna, Bologna, Italy, 1 9 Dipartimento di Física d el l'Université, Bologna, Italy, 20 INFN - Sezione di Pisa, Pisa, Italy, 21 INFN -Sezione di Roma, Roma, Italy,
2 2 Dipartimento di Física dell'Università La Sapienza, Roma, Italy, 2 3 Clermont Université, Université Biaise Pascal, CNRS/IN2P3, Laboratoire de Physique Corpusculaire,
IN2P3-CNRS, Clermont-Ferrand, France, 24INAF-IASF, Bologna, Italy, 2 5 Géoazur - Université de Nice Sophia-Antipolis, CNRS/INSU, IRD, Observatoire de la Côte d'Azur
and Université Pierre et Marie Curie, Villefranche-sur-Mer, France, 2 6 INFN - Sezione di Bari, Bari, Italy, 2 7 INFN - Laboratori Nazionali del Sud (LNS), Catania, Italy,
2 8 Université Paris-Sud, Orsay, France, 2 9 Kernfysisch Versneller Instituut (KVI), University of Groningen, Groningen, The Netherlands, 3 0 Dipartimento di Física
dell'Università Pisa, Italy, 31 Royal Netherlands Institute for Sea Research (NIOZ), Texel, The Netherlands, 32 Dr. Remeis Sternwarte & ECAP, Bamberg, Germany,
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July 2013 I V olum e 8 | Issue 7 | e67523
Dense W ater Form ation an d D eep-Sea B iolum inescence
Universiteit Utrecht, Faculteit Bètawetenschappen, Utrecht, The Netherlands, 3 4 Universiteit van Amsterdam, Instituut voor Hoge-Energie Fysika, Amsterdam, The
Netherlands, 3 5 Moscow State University, Skobeltsyn Institute of Nuclear Physics, Moscow, Russia, 3 6 INFN - Sezione di Catania, Catania, Italy, 3 7 Dipartimento di Fisica ed
Astronomía dell'Università, Catania, Italy, 3 8 Direction des Sciences de la Matière - Institut de recherche sur les lois fondamentales de l'Univers - Service de Physique des
Particules, CEA Saclay, Gif-sur-Yvette, France, 3 9 University of Wisconsin - Madison, Madison, Wisconsin, United States of America, 4 0 Institute for Space Sciences,
Bucharest, Romania, 4 1 IPHC-lnstitut Pluridisciplinaire Hubert Curien - Université de Strasbourg et CNRS/IN2P3, Strasbourg, France, 4 2 ITEP - Institute for Theoretical and
Experimental Physics, Moscow, Russia, 4 3 Dipartimento di Fisica dell'Università, Genova, Italy
33
Abstract
The d e e p ocea n is th e largest and least known e co sy stem on Earth. It hosts num erous pelagic organism s, m ost o f w hich are
able to em it light. Here w e present a unique data set consisting o f a 2.5-year long record o f light em ission by d e e p -se a
pelagic organism s, m easured from D ecem ber 2007 to June 2010 at th e ANTARES underw ater neutrino te le sc o p e In the
d e e p NW M editerranean Sea, jointly with syn ch ron ous hydrological records. This Is th e lo n g est con tin u ou s tim e-series o f
d e e p -se a b lolu m ln escen ce ever recorded. Our record reveals several w eek s long, season al b lolu m ln escen ce bloom s with
light Intensity up to tw o orders o f m agnitud e higher than background values, which correlate to ch a n g es In th e properties
o f d e e p waters. Such ch a n g es are triggered by th e w inter coolin g and evaporation experien ced by th e upper ocean layer In
th e Gulf o f Lion that leads to th e form ation and su b seq u e n t sinking o f d e n se w ater through a process known as "op en -sea
convection". It episodically renew s th e d e e p w ater o f th e stu dy area and con veys fresh organic matter that fuels th e d e e p
e co sy stem s. Luminous bacteria m ost likely are th e main contributors to th e ob served d e e p -se a b lolu m ln escen ce bloom s.
Our observations d em on strate a con sisten t and rapid con n ection b e tw e en d e e p o p e n -sea con vection and bathypelaglc
biological activity, as expressed by blolum lnescen ce. In a settin g w h ere d e n se w ater form ation ev en ts are likely to decline
under global warm ing scenarios enhan cin g ocea n stratification, in situ observatories b e c o m e essential as environm ental
sentinels for th e m onitoring and understanding o f d e e p -se a e co sy stem shifts.
C itation : Tamburini C, Canals M, Durrieu de Madron X, Houpert L, Lefèvre D, et al. (2013) Deep-Sea Bioluminescence Blooms after Dense Water Formation at the
Ocean Surface. PLoS ONE 8(7): e67523. doi:10.1371/journal.pone.0067523
Editor: John Murray Roberts, Heriot-Watt University, United Kingdom
Received December 25, 2012; A ccepted May 20, 2013; Published July 10, 2013
C opyrigh t: © 2013 Tamburini et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was partially funded by the ANR-POTES program (ANR-05-BLAN-0161-01), ANTARES-Bioluminescence project (INSU-IN2P3), AAMIS project
(Univ. Méditerranée), EC2CO Biolux project (CNRS INSU), Excellence Research Groups (2009-SGR-1305, Generalität de Catalunya), EuroSITES (FP7-ENV-2007-1202955), MARIN ERA-REDECO (CTM2008-04973-E/MAR), HERMIONE (FP7-ENV-2008-1-226354), KM3NeT-PP (212525), ESONET NoE (FP6- GOCE-036851 ), DOS MARES
(CTM2010-21810-C03-01) and CONSOLIDER-INGENIO GRACCIE (CSD2007-00067) projects. SM was granted a MERNT fellowship (Ministry of Education, Research
and Technology, France). LH acknowledges the support of the Direction Générale de l'Armement (supervisor: Elisabeth Gibert-Brunet). The authors also
acknowledge the financial support of the funding agencies: CNRS, CEA, ANR, FEDER fund and Marie Curie Program, Régions Alsace and Provence-Alpes-Côte
d'Azur, Département du Var and Ville de La Seyne-sur-Mer, France; BMBF, Germany; INFN, Italy; FOM and NWO, the Netherlands; Council of the President of the
Russian Federation for young scientists and leading scientific schools supporting grants, Russia; ANCS, Romania; MICINN (FPA2009-13983-C02-01), PROMETEO
(2009/026) and MultiDark (CSD2009-00064). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the
manuscript.
C om peting Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected] (CT); [email protected] (SE)
aa
ab
ae
ad
Current address: University of Leiden, Leiden, The Netherlands
Current address: DESY, Zeuthen, Germany
Current address: University of California Irvine, Irvine, California, United States of America
Current address: IRD - Centre de Nouméa, Noumea, Nouvelle-Calédonie
t Deceased.
bacteria are unaffected by mechanical stimulation and can glow
continuously for m any days under specific growth conditions [5,6],
Bioluminescent bacteria occur in marine waters as free-living
forms, symbionts in luminous organs of fishes and crustaceans and
attached to m arine snow aggregates sinking through the water
column [5,7]. D uring micro-algae blooms, strong bioluminescence
produced by colonies o f bacteria could even lead to spectacular
marine phenom ena such as “milky seas” in surface waters [6],
Bioluminescence sources have been observed and quantified
over the last three decades using a variety of observational
platforms and instruments such as m anned submersibles [1] and
autonom ous underw ater vehicles [8], in situ high sensitivity
cameras [9,10], underw ater photom eters [7,11,12], and remote
satellite imagery [6], In most cases, deep-sea bioluminescence is
triggered and observed after external mechanical stimulation
using, for instance, pum ped flows through turbulence-generating
grids [13] or downward moving grids that collide with the
Introduction
T he deep-sea ecosystem is unique because of its perm anent
darkness, coldness, high pressure and scarcity of carbon and
energy to sustain life. Most of its biological activity relies on the
arrival of carbon in the form of organic m atter from surface
waters. Ninety percent o f the numerous pelagic organisms that
inhabit the deep ocean are capable of emitting light [1] through
the chemical process of bioluminescence, which appears to be the
most comm on form o f com m unication in this remote realm
[1,2,3]. Deep-sea bioluminescence is also viewed as an expression
of abundance and adaptation of organisms to their environment
[4]. M arine bioluminescent organisms include a variety of distinct
taxa [4]. W hen stimulated mechanically or electrically, eukaryotic
bioluminescent organisms emit erratic luminous flashes, and also
spontaneous flashes to attract prey and mates for recognition of
congeners or for defence purposes [1,3,4], In contrast, luminescent
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July 2013 I Volume 8 | Issue 7 | e67523
Dense Water Formation and Deep-Sea Bioluminescence
occurs during late winter and early spring due to cold, strong and
persistent northern winds (Mistral and Tram ontane) causing
surface cooling of the Modified Atlantic W ater (MAW) both on
the shelf and over the deep basin. W hen the cooled shallow waters
on the shelf become denser than the am bient waters, they start
sinking, overflow the shelf edge, and cascade downslope until they
reach their density equilibrium depth, which may vary from
150 m to m ore than 2,000 m [20,23]. At the same time,
convection in the adjacent deep basin involves a progressive
deepening of the upper ocean mixed layer, which first reaches the
w arm er and saltier underlying Fevantine Interm ediate W ater
(FIW) and eventually extends all the way down to the basin floor,
should the atmospheric forcing be intense enough [19]. Both
processes and the subsequent renewal of the W estern M editerra­
nean Deep W ater (WMDW) show a high interannual variability
because of their sensitivity to atmospheric conditions [18,24]. The
newly-formed deep w ater (nWMDW) resulting from both dense
shelf water cascading and open-sea convection has been observed
to spread over the deep basin floor within months [22,24,25,26].
Studies about the response of deep ecosystems to such processes
are scarce and focus on the im pact of dense shelf w ater cascading
on benthic and epi-benthic organisms [27,28]. O th er recent works
highlight how deep w ater formation triggers the resuspension of
deep-sea sediments, including organic m atter [21], and the
organisms [10]. While these procedures provide crucial informa­
tion on the nature and distribution of deep-sea bioluminescent
organisms in the w ater column [3 and references therein], they are
not suited to investigate the tem poral variability of naturally
occurring light production (i.e. non artificially triggered) at specific
sites over long periods of time, which requires sustained high
frequency in situ measurements.
An unanticipated application of underw ater neutrino telescopes
is to provide direct measurements of bioluminescence in the deepsea [14,15,16]. A neutrino telescope aims at detecting the faint
Cherenkov light emission radiated by elem entary charged particles
called muons that are produced by neutrino interactions.
Darkness, transparency and w ater shielding against cosmic ray
muons make the deep-sea an ideal setting for a neutrino telescope.
H ere we make use of both the high frequency bioluminescence
and hydrological time-series of the cabled ANTARES neutrino
telescope [17] located 40 km off the French coast (42°48'N,
6°10'E) at 2,475 in the N W M editerranean Sea (Fig. la).
T he N W M editerranean Sea is one of the few regions in the
w orld’s ocean where both dense shelf water cascading and opensea convection take place [18,19,20,21] (Fig. la). This results in
the formation of deep w ater owing to the combination of
atmospheric forcing and regional circulation that lead the water
column to overturn [19,20,22]. Dense deep w ater formation
2008
ANTARES
Z
co
M-
LDC
Z
CM
CM
Z
z
LION
2°E
3°E
4°E
5°E
6°E
7°E
8°E'
9°E
2009
z
co
z
CM
z
Figure 1. M ap o f th e NW M ed iterran ean Sea showing the location o f th e ANTARES, LION and Lacaze-Duthiers Canyon (LDC) sites
(a) as w ell as the extension o f open-sea convection area in the G ulf o f Lion and beyond fro m 2 0 0 8 to 2 0 1 0 (b -d ). The bo u n d aries of
th e convection area in w inter 2008 (red in b), 2009 (blue in c) and 2010 (green in d) are derived from MODIS-Aqua satellite-based surface Chlorophylla co n cen tratio n im ages. The limits of th e convection area for each of th e th re e successive w inters correspond to their m axim um ex ten ts during
p eriods of d e e p w ater form ation m easured a t th e LION site (see Text SI and Fig. S5). Black arrow s indicate th e direction of th e tw o main contin en tal
w inds leading to th e cooling and su b se q u e n t sinking of surface w aters: Mistral (M) an d T ram ontane (T). The grey arrow indicates th e path of th e
cyclonic surface m esoscale N orthern C urrent bordering th e o p en -sea convection region.
doi:10.1371/journal.pone.0067523.g001
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Dense Water Formation and Deep-Sea Bioluminescence
development and spreading o f a thick bottom layer loaded with
resuspended particulate m atter across the NW M editerranean
Basin as a result of dense shelf water cascading [29].
H ere we present compelling evidence of the quick response of
the deep-sea pelagic ecosystem to seasonal atm ospheric forcing
leading to dense water formation and sinking, expressed by
particularly intense bioluminescence events captured by neutrino
telescope photom ultiplier tubes. Observations on bioluminescence
are supported by a two and a half years long unique and consistent
record of hydrological and hydrodynamica! variables obtained at
the ANTARES deep-sea neutrino telescope itself bu t also at two
independent mooring arrays equally located in the deep NW
M editerranean Sea.
box-and-whisker plots) and on the other hand, bioluminescence
rates are always higher for new deep w ater (red boxes, S>38.479)
than for pre-existing deep water (grey boxes, S<38.479). The
Kruskal-Wallis test perform ed on the box-and-whisker plots attests
that the red and grey boxes are significandy different (p<0.001) for
current speeds up to 18 and 24 cm s-1 in 2009 and 2010,
respectively (Fig. 3b-3c), which means th at bioluminescence rates
are dependent on water mass properties too. This is illustrated, for
instance, by the 2010 record (Fig. 3c), which shows that the
median bioluminescence rate for the 0 -3 cm s_ current range is
about 60 kHz for the existing deep water (grey box-plots), while it
reaches 400 kHz within the new deep water (red box-plots).
Bioluminescent bacteria, which are not affected by mechanical
stimulation [5,14] and are able to glow continuously under specific
conditions [5,6], are excellent candidates as m ain contributors to
these bioluminescence blooms.
Results and D iscussion
Biolum inescence b lo o m s a t t h e ANTARES site
W e report time-series measurements of light intensity expressed
in m edian counting rates on photom ultiplier tubes as well as
tem perature, salinity and current speed from D ecem ber 2007 to
Ju n e 2010 (Fig. 2a), collected between 2,190 and 2,375 depth in
the ANTARES IL07 mooring line (see Methods and Fig. SI).
While the light intensity background rate is predom inandy
between 40 and 100 kHz, which mainly includes the 40K rate
(see Methods and Fig. S2), two rem arkable bioluminescence
events reaching up to 9,000 were recorded between M arch and
July in 2009 and 2010 (Fig. 2). Because of their high intensity and
duration we call these events “bioluminescence blooms” , defined
here as periods with P M T median rates higher than 600 kHz, i.e.
higher than the 96th percentile o f the entire PM Ts record.
O ur records show that bioluminescence primarily increases with
current speed, which is due to mechanical stimulation either by
impacts of small-sized organisms and particles on the PM Ts
[16,30] or by the reaction of organisms to enhanced turbulent
motion in the wakes o f the PM Ts [14,15,16]. However, current
speed alone fails to explain the complete record of bioluminescent
activity since, for m oderate current speeds, differences in the
median rates of up to one order of m agnitude are observed in 2009
(Fig. 2b) and 2010 (Fig. 2c). For instance, on M arch 8, M arch 11
and April 8-12, 2010, bioluminescence peaks at 800 to 1300 while
current speeds are rather low, from 10 to 15 cm s_ (Fig. 2c) a
speed range usually associated to m edian rates of around 100.
These bioluminescence bursts clearly correspond to significant
increases in both potential tem perature (A0 = 0.03-0.05°C) and
salinity (AS = 0.005-0.015). As the deep water mass at the
ANTARES site is the W M D W , characterized in 2008 by a
narrow range of tem perature and salinity (0 = 12.89-12.92°C,
S = 38.474—38.479), the increases above the norm al range of
variation observed in 2009 and 2010 are indicative of the intrusion
of a distinct water mass (Fig. 2, see T ext SI and Fig. S3). It is
noteworthy that neither deep-water therm ohaline modification
nor bioluminescence blooms were recorded in 2008 (Fig. 2a).
To illustrate the link between the intrusion of newly formed
deep water and high bioluminescence, we use a salinity threshold
of 38.479 as marker of such intrusions at the ANTARES site. This
value has been defined using a statistical decision tree (Fig. S4) and
also corresponds to the 96th percentile of the entire salinity record.
Bioluminescence data, divided into two groups above and below
this salinity threshold, are presented as box-and-whisker plots
versus current speed classes (Fig. 3). Close examination of Figure 3
shows that bioluminescent activity is enhanced by both increasing
current speed and the renewal of the deep water. Indeed, on the
one hand, the bioluminescence rates increase with current speed
for each of the two bioluminescence data groups (grey and red
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D ee p -w a ter convection in th e NW M e d iterranean Sea
To determine the origin of the newly formed deep water
observed at the ANTARES site in 2009 and 2010, we investigated
w hether dense shelf water cascading a n d /o r open-sea convection
occurred in winter months.
Instrum ented mooring lines located at the center of the deep
convection region (LION site at 42°02'N , 04°41'E; Fig. la) and in
Lacaze-Duthiers Canyon (LDC site at 42°26'N , 03°33'E; Fig. la)
provided tem perature, salinity and current speed time-series from
different w ater depths (Fig. 4) synchronous to the ANTARES
record. W hile no deep (& 1,000 m) dense shelf w ater cascading
took place during the study period (Fig. 4a), bottom -reaching
open-sea convection was observed in the basin down to 2,300 m
depth during wintertime in 2009 and 2010, which led to the
homogenization of the w ater column (Fig. 4b). Increases in deepw ater tem perature (Fig. 4b) and salinity (Fig. 4c) are due to the
mixture of sinking cold surface water with w arm er and saltier
LIW. In winter 2008, open-sea convection only affected the upper
1,000 m of the w ater column and did not alter the deep water
mass. C urrent measurements showed the strong barotropic
character o f horizontal velocities (Fig. 4d) and high vertical
velocities (Fig. 4e) during intense mixing periods. O nce the surface
forcing abates, convection ceases and intense sub-mesoscale eddies
carry discrete volumes of the newly formed deep water away from
the convection area [26]. T he delay between the appearance of
the therm ohaline anomalies at the L IO N site in late winter and
their arrival at the ANTARES site in spring is compatible with the
spreading of the newly-formed deep water in the G ulf of Lion and
subsequent mixing with pre-existing deep w ater [22,24,25,26].
Further mixing could take place at the ANTARES site due to
enhancem ent of vertical motion by the interaction of instabilities
in the surface cyclonic N orthern C urrent with the topography of
the continental slope [31]. T he area of open-sea convection, as
obtained from satellite im agery (see Fig. S5), was much smaller
during winter 2008 than in 2009 and 2010 when it covered most
o f the deep G ulf of Lion (Figs. lb -d ). Furtherm ore, it was larger
and closer to the A N TA RES site in 2010 than in 2009 (Fig. lc-d),
which may explain why the signature o f new deep-water recorded
at the A N TA R ES site is stronger in 2010 than in 2009 (Fig. 2).
Link b e t w e e n biolu m in escen c e b lo o m s a n d d e e p - w a te r
convection
All evidence points to deep-water formation by open-sea
convection in the G ulf of Lion as the cause of the renewal of
deep w ater at the ANTARES site that triggered the biolumines­
cence blooms observed in 2009 and 2010.
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Dense Water Formation and Deep-Sea Bioluminescence
Fig. 2c
Fig. 2b
r Median rates (kHz)
i
l i i
103
10
io2
io1
3 8 .4 9
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10
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0 1 -F e b -1 0 0 1 -M a r-1 0
0 1 -A p r-1 0
0 1 -M ay -1 0
0 1 -Ju n -1 0
0 1 -J u l-1 0
Figure 2. Tim e series m easured a t th e ANTARES IL07 m ooring line, (a) M edian PMT counting rates (log scale), salinity, potential te m p e ra tu re
and cu rren t sp e ed from D ecem ber 2007 to Ju n e 2010. Shading indicates periods (b) from January to Ju n e 2009 and (c) from January to Ju n e 2010, in
which biolum inescence bloom s w ere recorded. The lack of data from Ju n e 24 to S ep tem b er 6, 2008 is d u e to a cable technical failure.
doi:10.1371/journal.pone.0067523.g002
D uring and in the afterm ath of the convection period large
amounts of organic m atter, both in particulate (POC) and
dissolved (DOC) form, are exported from the productive upper
PLOS ONE I www.plosone.org
ocean layer down to the deep [21,32,33]. T he resuspension of soft
sediments covering the deep seafloor by bottom currents during
the reported period could also inject organic m atter into the deep-
5
July 2013 | Volume 8 | Issue 7 | e67523
Dense Water Formation and Deep-Sea Bioluminescence
200
-
i: 100
(0,3]
(3,6]
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— i---------------------1----------------------- 1---------------------- 1----------------------1---------------------- 1----------------------1---------------------- 1----------------------1----------------------1—
(0,3]
(3,6]
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(9,12]
(12,15]
(15,18]
(18,21]
(21,24]
(24,27]
(27,35]
Current speed (cm s 1)
Figure 3. Links betw een biolum inescence, current speed and the m odification o f the properties o f the W estern M ed iterran ean
Deep W ater (W M D W ). Box-and-whisker plot of m edian PMT counting rates (log scale) versus current sp e ed classes for salinities higher (red) or
low er (grey) th an 38.479 for data recorded in (a) 2008, (b) 2009 and (c) b etw een January and Ju n e 2010. The salinity th resh o ld of 38.479 is used as a
m arker of th e intrusion of new ly form ed d e e p w ater at th e ANTARES site. While biolum inescence increases w ith current sp eed , it is also e n h an ce d by
th e m odification o f WMDW (red box-plots). The to p and b o tto m of each box-plot rep re sen t 75% (upper quartile) and 25% (lower quartile) of all
values, respectively. The horizontal line is th e m edian. The en d s of th e w hiskers rep re sen t th e 10th and 90th percentiles. Outliers are n o t rep resen ted .
The statistical com parison b etw een th e tw o box-plots (red and grey) in each current class is given by th e Kruskal-Wallis test: th e observed difference
b etw een th e tw o sam ples is significant beyond th e 0.05 (*), th e 0.01 (**) and th e 0.001 (***) levels. The ab sen ce of an asterisk in som e cu rren t classes
indicates th a t th e difference b etw een th e tw o box-plots is n o t significant. The n u m b er of m easu rem en ts for salinity low er or higher th an 38.479 is
given in black or in red, respectively. Note th e different scales of figures a, b and c.
doi:10.1371/journal.pone.0067523.g003
PLOS ONE I www.plosone.org
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July 2013 | Volume 8 | Issue 7 | e67523
Dense Water Formation and Deep-Sea Bioluminescence
LDC Potential t e m p e r a t u r e
14 .00
(°C)
13 .00
500 m
12
.
1, 000 m
00
11.00
1 - J u l - 08
L I O N P o t ential t e m p e r a t u r e
1-J u l -09
1-J u l -10
(°C)
13 . 3 0
13 . 2 0
170 m
700 m
13 . 1 0
1,500 m
2,300 m
13 . 00
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r
L I O N S a l i n i t y 2,300 m
50
49
2,300 m
48
38
.
l-Jul-08
„n
1-Jul-09
L I O N H o r i z o n t a l c urrent sp e e d
l-Jul-10
(cm s'1)
l-Jul-09
LION Vertical
2
c urrent spe e d
l-Jan-10
l-Jul-10
(cm s"1)
I-
0
-150 m
-500 m
-2
-1,000 m
-4
-6
-2,300 m
I-
j
l-Jul-08
1-Jul-09
i
i
i
i
i
i
l - J an-10
i
i
,
i
i
i
i
i
i
i
l-Jul-10
Figure 4. T im e series o f oceanographic param eters m easured a t th e Lacaze-Duthiers Canyon (LDC) and th e open-sea convection
region in th e G ulf o f Lion (LION) from January 2 0 0 8 to June 2 0 1 0. (a) Potential te m p e ra tu re at 500 and 1,000 m d e p th at th e LDC m ooring
site an d (b) from various w ater d e p th s at th e LION site, jointly w ith (c) salinity at 2,300 m d e p th , (d) horizontal current sp e ed an d (e) vertical current
sp e ed from various w ater d e p th s at th e LION site. The four levels of te m p e ra tu re m easu rem en ts a t LION p resen ted here are a su b -set of
m easu rem en t d e p th s (see Fig. S I). Essentially stable te m p eratu res In th e d e e p e s t layers In 2008 show th a t o p en -sea convection reached only 700 m
an d did n o t m odify th e d e e p w ater In th e stu d y area. In contrast, stro n g convection events, reaching 2,300 m d e p th , occurred during February-M arch
PLOS ONE I www.plosone.org
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July 2013 I Volume 8 | Issue 7 | e67523
Dense Water Formation and Deep-Sea Bioluminescence
2009 and 2010 w ith an a b ru p t cooling of th e u p p e r w ater colum n an d an increase in tem p e ra tu re and salinity in th e d e e p layers. A co n cu rren t
increase in cu rren t sp e ed w as also noticed in w inter 2009 and 2010. The 5-m onth long d a ta g a p in 2009 is d u e to a dam ag in g o f th e m ooring line
during th e April 2009 recovery, which induced a p o stp o n e m e n t o f its red ep lo y m en t to S ep tem b er 2009.
doi:10.1371/jo u rn al.pone.0067523.g004
water mass [21,32]. Changes in D O C concentration at the
ANTARES site are shown by discrete measurements carried out at
2,000 m depth during oceanographic cruises from D ecem ber 2009
to July 2010 (Fig. S6). D O C concentration significandy increased
from 42 ± 1 pM in D ecem ber 2009, prior to the convection period,
to 63 ±1 pM in M arch and M ay 2010 when the new deep water
mass occupied the ANTARES site, concurrently with higher
oxygen contents in bottom waters between M arch and mid-June
2010. Subsequently, D O C concentration decreased to 45 in midJu n e and mid-July 2010 (Fig. S6). Such an injection of organic
m atter into the deep water mass has the potential to fuel the deepsea biological activity, thus stimulating bioluminescence activity.
T he increase in D O C concentration matches with observations
reported by Santinelli et al. [33] for different regions of the
M editerranean Sea where deep convection occurs. These authors
showed a high mineralization rate o f D O C in recently ventilated
deep waters, which is mainly attributed to bacteria. Bioluminescent bacteria were isolated at the ANTARES site during a
previous period of high bioluminescent activity in 2005 [34],
Amongst them, we identified a piezophilic strain, Photobacterium
phosphoreum ANT-2200 [34,35], P. phosphoreum being the dom inant
bioluminescent species in the M editerranean Sea [36]. These
luminous bacteria likely represent the m ain organisms responsible
for the higher level of bioluminescence detected at the A NTARES
site. Such contribution is especially noticed when the current speed
is low within the convection season (Fig. 3b-3c). Finally, the flow
associated with deep convection events might likely carries
significant amounts o f bioluminescent organisms too, which can
also contribute to the bioluminescence blooms observed in 2009
and 2010 due to their collision with PM Ts a n d /o r their
stimulation by turbulent motion in the wakes of PM Ts when
current speed is high.
M ethods
T he ANTARES neutrino telescope comprises a three-dim en­
sional array of 885 Flam am atsu R7081-20 photom ultiplier tubes
(PMTs) distributed on 12 mooring lines [17,41], These PM Ts are
sensitive to the wavelength range of 400-700 nm, which matches
the main bioluminescence emission spectrum (440-540 nm) as
reported in W idder [4], An extra mooring line (named IL07)
equipped with R D I 300 kFIz acoustic Doppler current profilers, a
conductivity-temperature-depth (SBE 37 SM P CTD) probe and
PM Ts was added to m onitor environmental variables (Fig. SI). All
moorings are connected to a shore-station via an electro-optical
cable that provides real-time data transmission [42]. A dedicated
program of bioluminescence monitoring was im plem ented to
measure the total num ber o f single photons detected every 13 ms
for each PM T. To consistently compare P M T counting rates
(bioluminescence) with oceanographic data (temperature, salinity,
current speeds) considering the acquisition interval of the later
(15 minutes), we calculated the m edian rates as a m athematical
estimator of PM T counting rates. T he median was selected instead
of the arithmetic m ean because o f its higher robustness and least
disturbance by extreme values. M edian rates were expressed in
thousands o f photons per second or kFIz (see T ext SI and
Fig. S2a). T he m ain light contributions recorded by PM Ts result
from dark noise, from Cherenkov radiation induced by the beta
decay of K in seawater and from bioluminescence. T he dark
noise is about 3 ± 1 kFIz and remains constant with time [41]. The
Cherenkov radiation induced by the beta decay of K in seawater
produces a background o f about 3 7 ± 3 kFIz [43], found to be
constant within the statistical errors over a period of a few years
[44,45]. Therefore, all light increases over this constant back­
ground (40 ± 3 kFIz) can only be due to bioluminescence. The
records of light intensity at ILO 7 are representative of those
collected by the whole array o f ANTARES PM Ts (see T ext SI
and Fig. S2b).
Potential tem perature, salinity, horizontal and vertical current
speeds (Fig. SI) at the L IO N mooring line were measured with
SBE 37 SM P C TD probes and Nortek Aquadopp Doppler
current-m eters regularly spaced between the subsurface (150 m,)
and the seabed (2350 m). Potential tem peratures and vertical
velocities were corrected for the current-induced tilting and
deepening of the line. H ourly potential tem peratures at the LDC
mooring line were measured with the tem perature sensor of
Nortek A quadopp Doppler current meters at 500 and 1,000 m
depth.
Proper calibrations of the C T D probes were perform ed using
the pre- and post-deployment calibrations m ade by the m anufac­
turer. T he intercom parison of instruments complied with qualitycontrol procedures.
C onclusions
W e present evidence for seasonal episodes of dense water
formation driven by atmospheric forcing being a major vector in
fuelling the deep-sea pelagic ecosystem and inducing biolumines­
cence blooms after a fast transfer of the ocean surface signal. Since
dense water formation occurs in other ocean regions worldwide
[19], we anticipate that an enhancem ent of the deep pelagic
ecosystem activity similar to th at observed in the N W M editer­
ranean Sea occurs there too, challenging our understanding o f the
carbon dynamics in the ocean.
Dense w ater formation is likely to be altered by the on-going
global warming. R ecent models [37,38] based on the A2 IPCC
scenario indicate a strong reduction in the convection intensity in
the M editerranean Sea for the end of the 21st century, which will
induce a massive reduction in organic m atter supply and
ventilation of the deep basin. Flence changes in the deep
M editerranean ecosystem m ore intense than those already
observed in both the Eastern [39,40] and the W estern M editer­
ranean [27] basins are forecasted for the near future, a situation
that could also occur but rem ain unnoticed in other sensitive areas
of the world ocean. O u r results Alústrate the potentially farreaching multidisciplinary scientific and societal benefits of the
installation of cabled deep-sea observatories in critical ocean areas.
PLOS ONE I www.plosone.org
Supporting Information
Figure SI C o n fig u r a tio n o f th e m o o r in g lin e s fr o m
w h ich th e d a ta p r e s e n te d in th is stu d y w e r e o b ta in e d .
They include the cabled ILO 7 ANTARES as well as the
autonom ous L IO N and Lacaze-Duthiers Canyon (LDC) mooring
lines. Location is shown in Fig. 1.
JPG )
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July 2013 I Volume 8 | Issue 7 | e67523
Dense Water Formation and Deep-Sea Bioluminescence
Figure S2 (a) R a w c o u n tin g r a te s fr o m o n e p h o to m u l­
tip lie r (PMT) o n th e IL07 lin e (ANTARES site ). Counts are
expressed in thousands of photons per second (kHz). T he median
rate is com puted for each 15-minute data sample (red horizontal
line). T he dataset shown in the figure was recorded on M arch
28th, 2010 with a median rate of 68 kHz and a current speed of
13 c m s - 1 . (b) M e d ia n r a te s fr o m th e IL07 P M T (red) an d
m e a n o f all m e d ia n r a te s o f th e 885 ANTARES P M T s
(blue) fr o m J a n u a ry to A p ril 2009.
JPG )
Figure S5 Illu str a tiv e o c e a n c o lo u r s a te llite im a g e s u se d
to o u tlin e th e lim its o f w in te r o p e n -s e a c o n v e ctio n a r e a s
in th e G u lf o f L io n , (a) Images plotted with a classical, full
range, linear palette, (b) Images plotted with a simplified four level
palette. T he images shown correspond to days 1, 2, 7 and 18
February 2010, which are also transferred into Fig. lb -d . W hite
pixels are indicative o f lack of data due to cloud coverage.
JPG )
Figure S6 D iss o lv e d o r g a n ic c a r b o n an d o x y g en c o n ­
c e n tr a tio n s a t th e ANTARES s ite in 20 10 . Dissolved
O rganic C arbon (DOC) was measured by high tem perature
combustion on a Shim adzu T O C 5000 analyzer [46]. A four
point-calibration curve was perform ed daily with standards
prepared by diluting a stock solution of potassium hydrogen
phthalate in Milli-Q^ water. Procedural blanks run with acidified
and sparged Milli-Q^ water ranged from 1 to 2 pM C and were
subtracted from the values presented here. Deep seawater
reference samples (provided by D. Hansell; Univ. Miami) were
run daily (43.5 pM C, n = 4) to check the accuracy of the D O C
analysis. Oxygen concentration time-series was obtained using an
oxygen optode Anderaa® fitted on the ILO 7.
(TIF)
Figure S3 P o te n tia l te m p e r a tu r e v e r s u s sa lin ity d ia ­
g r a m o f n e a r -b o tto m C T D tim e -s e r ie s a t th e ANTARES
s ite fr o m th e IL07 lin e (red d o ts) a n d C T D p r o file s
(lines) c o lle c te d c lo s e to th e ANTARES s ite , (a) M ay 2007
to January 2009; (b) Jan u ary to D ecem ber 2009; and (c)
D ecem ber 2009 to Jan u ary 2011. T he data shown are from
depths in excess of 1,000 m. D otted lines correspond to potential
density anomaly isolines in kg m - 3 .
JPG )
Figure S4 R e g r e ssio n tr e e fo r p r e d ic tin g th e in te n sity o f
b io lu m in e s c e n c e u s in g o c e a n o g r a p h ic v a r ia b le s (sa lin i­
ty, te m p e r a tu r e , c u r r e n t sp e ed ) a n d tim e d e p e n d e n c e
fr o m D e c e m b e r 2007 to J u ly 2 0 1 0 . Regression trees are
statistical models that sub-divide or partition a set of explanatory
variables X (salinity, tem perature, current speed) to predict a
targeted response variable Y (bioluminescence rate). T he tree is
draw n using a binary recursive algorithm. It divides Y data into
two non-em pty groups either X < a or X > a. T he split which
maximizes the deviance (or distance) is chosen, the data set split
and the process is repeated. This is done until the term inal nodes
are too small or too few to be split, the last groups decision here
are set up by the user in order to get less than 5 sub-groups. Each
of the term inal nodes are the m ean of the predicted value Y. Using
this method, 3 nodes and 4 classes have been defined from the 3
variables predicting the average bioluminescence intensity. This
classification improves the maximal deviance interclass and
minimal deviance intraclass using sampled time-series. Class 1
(mean 121.1 kHz), 2 (mean 435.0 kHz) and 3 (mean 552.4 kHz)
described low empirical bioluminescence intensity mainly due to
low sea current speed (below 19.04 cm s ’). However class 3 and 4
are firstíy described by high current speed intensity (>19.04 cm
s *) but as a second environmental condition, the tem perature
threshold of 12.922°C divide these two classes between high (mean
1393.0 kHz) and highest (mean 5108.0 kHz) bioluminescence
intensity.
JPG )
T ext SI
(DOCX)
Supplemental text information.
A ck n ow led gm en ts
The authors thank the captains and crews of R.V. Tethys II and L’Europe
for cruise assistance. Technical support by Ifremer, Assistance Ingénierie
Management (AIM) and Foselev Marine during sea operation and CCIN2P3 for providing computing facilities is greatly appreciated.
Author C ontributions
Analyzed the data: CT SE MC XDdM LH DL SM LO AR PT CC. Wrote
the paper: CT SE MC XDdM. Conceived, designed and performed the
ANTARES experiment: JAA IAS AA MA MA GA SA MA ACAJ TLA
JJA BB SB VB SB AB CB CB MCB BB M CM JB JB FC AC CC GC JC
SC ZC PC TC MC RC HC PC CC PD ID AD CD DD H Q D DD TE
UE JPE SE PF MF VF FF U F JL F SG PG GG VG JPG G KG GG GH
GH H vH JH AJH Y H JJH R BH J H CCH MdJ MK O K AK U K O K PK
C K AK IK VK RL PL GL DL GL D LP HL SL SM MM AM JAM M AM
TM LM HM MN EN DP GEP KP PP JP PP NPC VP TP EP C R C R GR
C R RR CR K R AR JR R M R VG R FS ASL PS FS JPS FS RS FS RS FS
AS MS JJMS TS MGFT ST BV W E GV MV PV GW JW EdW HY DZ
JD D Z JZ. Conceived, designed and performed the FI ON and LDC sites:
MC XDdM PT.
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