Cold-water coral reefs thriving under hypoxia

Abstract

Reefs formed by scleractinian cold-water corals represent unique biodiversity hot spots in the deep sea, preferring aphotic water depths of 200–1000 m. The distribution of the most prominent reef-building species Lophelia pertusa is controlled by various environmental factors including dissolved oxygen concentrations and temperature. Consequently, the expected ocean deoxygenation and warming triggered by human-induced global change are considered as a serious threat to cold-water coral reefs. Here, we present results on recently discovered reefs in the SE Atlantic, where L. pertusa thrives in hypoxic and rather warm waters. This sheds new light on its capability to adapt to extreme conditions, which is facilitated by high surface ocean productivity, resulting in extensive food supply. Putting our data in an Atlantic-wide perspective clearly demonstrates L. pertusa’s ability to develop population-specific adaptations, which are up to now hardly considered in assessing its present and future distributions.

Full text

NOTE
Cold-water coral reefs thriving under hypoxia
Dierk Hebbeln
1
•Claudia Wienberg
1
•Wolf-Christian Dullo
2
•Andre
´Freiwald
3
•
Furu Mienis
4
•Covadonga Orejas
5
•Ju
¨rgen Titschack
1,3
Received: 12 August 2019 / Accepted: 6 April 2020 / Published online: 21 April 2020
ÓThe Author(s) 2020
Abstract Reefs formed by scleractinian cold-water corals
represent unique biodiversity hot spots in the deep sea,
preferring aphotic water depths of 200–1000 m. The dis-
tribution of the most prominent reef-building species
Lophelia pertusa is controlled by various environmental
factors including dissolved oxygen concentrations and
temperature. Consequently, the expected ocean deoxy-
genation and warming triggered by human-induced global
change are considered as a serious threat to cold-water
coral reefs. Here, we present results on recently discovered
reefs in the SE Atlantic, where L. pertusa thrives in
hypoxic and rather warm waters. This sheds new light on
its capability to adapt to extreme conditions, which is
facilitated by high surface ocean productivity, resulting in
extensive food supply. Putting our data in an Atlantic-wide
perspective clearly demonstrates L. pertusa’s ability to
develop population-specific adaptations, which are up to
now hardly considered in assessing its present and future
distributions.
Keywords Cold-water corals Lophelia pertusa 
Hypoxia Adaptation Global change
Introduction
Being ecosystem engineers, framework-forming sclerac-
tinian cold-water corals (CWCs) provide habitat for thou-
sands of deep-sea species, revealing equally remarkable
levels of biodiversity as found in tropical coral reefs
(Henry and Roberts 2017). Lophelia pertusa is the domi-
nant reef-forming CWC in the Atlantic, and based on its
distribution correlated with ocean conditions, upper and
lower tolerable limits for basic oceanographic parameters
were proposed for this species (e.g., Davies and Guinotte
2011). Among them, dissolved oxygen concentrations
(DO
conc
) can exert control on its biogeographic distribution
(e.g., Tittensor et al. 2009). However, lowest DO
conc
inhabited by this species apparently differs between NE
Atlantic (*3.7 mL L
-1
; Dullo et al. 2008) and NW
Atlantic (*2mLL
-1
; e.g., Brooke and Ross 2014) reef
sites. These observations are corroborated by laboratory
experiments, revealing that L. pertusa individuals collected
from DO
conc
of 6 mL L
-1
at the Scottish margin, NE
Atlantic, were unable to maintain normal aerobic functions
at DO
conc
\3.2 mL L
-1
(Dodds et al. 2007). Moreover,
for L. pertusa specimens collected from DO
conc
of
*2.8 mL L
-1
in the Gulf of Mexico, 7-day exposure to
DO
conc
of *1.5 mL L
-1
proved fatal (Lunden et al.
Topic Editor Mark R Patterson
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s00338-020-01934-6) contains sup-
plementary material, which is available to authorized users.
&Dierk Hebbeln
dhebbeln@marum.de
1
MARUM – Center for Marine Environmental Sciences,
University of Bremen, Leobener Strasse 8, 28359 Bremen,
Germany
2
GEOMAR Helmholtz Centre for Ocean Research,
Wischhofstr. 1-3, 24148 Kiel, Germany
3
Marine Research Department, Senckenberg am Meer (SAM),
Su
¨dstrand 40, 26382 Wilhelmshaven, Germany
4
NIOZ Royal Netherlands Institute for Sea Research and
Utrecht University, 1790 AB Den Burg, Texel, The
Netherlands
5
Group of Ecosystems Oceanography (GRECO), Instituto
Espan
˜ol de Oceanografı
´a, Centro Oceanogra
´fico de Baleares,
Moll de Ponent s/n, 07015 Palma, Spain
123
Coral Reefs (2020) 39:853–859
https://doi.org/10.1007/s00338-020-01934-6
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

2014). Furthermore, discoveries of L. pertusa in the oxygen
minimum zones (OMZ) of the subtropical eastern Atlantic
(Colman et al. 2005; Le Guilloux et al. 2009) hinted to an
even wider tolerance of L. pertusa to low DO
conc
. Never-
theless, the limited capability of L. pertusa to thrive under
DO
conc
(artificially) reduced below those of their natural
environment (Dodds et al. 2007; Lunden et al. 2014),
questions its ability to cope with the global change-induced
ocean deoxygenation expected for the coming century
(e.g., Sweetman et al. 2017).
Although hitherto hypoxic settings were regarded as
unsuitable habitats for CWC (e.g., Tittensor et al. 2009),
here, we present the discovery of L. pertusa-dominated
CWC reefs thriving in the hypoxic OMZ off Angola in the
SE Atlantic. The regional adaptation of the Angolan CWC
to such extreme conditions sheds new light on their
potential capability to cope with expected future environ-
mental changes in the ocean.
Methods
During RV Meteor expedition M122 in January 2016
(Hebbeln et al. 2017), in situ oceanographic parameters
such as DO
conc
and temperature were recorded off Angola
(Fig. 1). Data were collected during eight dives with the
remotely operated vehicle (ROV) MARUM SQUID (On-
line Resource 1), three benthic lander deployments
(2.5–6.8 days; Online Resource 2) and 17 conventional
CTD casts (Online Resource 3). The conventional CTD
was additionally equipped with a non-calibrated fluores-
cence sensor only providing relative values shown as
means per water depth averaged from all CTD casts.
Results and discussion
Discovery of cold-water coral reefs in the oxygen
minimum zone off Angola
ROV video observations revealed the presence of CWC
reefs dominated by L. pertusa, which colonize the slopes
and summits of up to 100-m-high coral mounds (Fig. 1;
Hebbeln et al. 2017). While dispersed CWC colonies were
found in a depth range of 250–500 m, large aggregates of
healthy colonies were restricted to 330-470 m water depth
(Fig. 2). The observation of [50-cm-high colonies
(Fig. 2) clearly evidenced the continuous proliferation of
CWC off Angola for many years.
The available oceanographic data revealed water tem-
peratures of 6.8–14.2 °C around the CWC (250–500 m;
Fig. 3). The corresponding DO
conc
of 0.6–1.5 mL L
-1
are
the lowest ever obtained from waters bathing flourishing L.
pertusa colonies (Fig. 3). The ROV–CTD DO
conc
mea-
surements show the smallest variations. The slightly larger
ranges of the lander and conventional CTD data (Fig. 3)
likely reflect the impacts of internal waves (Hanz et al.
2019) and the larger geographical coverage, respectively.
To gain insight into the seasonal variability of DO
conc
off Angola, as the M122 data only represent an 8.5-day
snapshot from January 2016, we included further 21 CTD
casts obtained within the mapped area off Angola (Fig. 1)
between 1995 and 2013 (Tchipalanga et al. 2018; Online
Resource 4). These data, spanning from March to
September, almost completely correspond to the M122 data
or reveal even lower DO
conc
(Fig. 3). Interestingly, even in
this hypoxic environment, most prolific CWC reefs are
bound to the center of the Angolan OMZ where lowest
DO
conc
prevail (Fig. 3), which coincide with enhanced
water-column fluorescence pointing to an increased avail-
ability of relatively fresh organic matter (Fig. 3).
Oxygen sensitivity of Lophelia pertusa in the Atlantic
Ocean
Based on field observations in the NW and NE Atlantic
(Dullo et al. 2008; Freiwald et al. 2009; Brooke and Ross
2014; Georgian et al. 2016), the assumed lower limit of L.
pertusa’s oxygen tolerance ranges around DO
conc
of
2–3.7 mL L
-1
. This has recently been challenged by very
low DO
conc
of 1.1–1.4 mL L
-1
reported from CWC sites
off Mauritania (Ramos et al. 2017), which, however, are
associated with only sporadic occurrences of small L.
pertusa colonies (Wienberg et al. 2018). The new Angolan
data documented for the first time L. pertusa’s ability to
develop thriving reefs even under DO
conc
of \1mLL
-1
(Fig. 3).
In addition, off Angola L. pertusa lives at temperatures
of up to 14.2 °C (Fig. 3), which are among the highest
temperatures ever observed for this species (13.9–15.2 °C;
854 Coral Reefs (2020) 39:853–859
123
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12°40'E
S'04°9
S'0
5°9
05km
-700
-600
-500
-700
-300
-400
-500
-400
S'05°
9
12°50'E
-600
Namibia
Angola
10°E
S°01
S°
02
Benguela
Namibe
-4000
-3000
-2000
-1000
-500
-200
study
area
CTD Lander
ROV dives CWC reefs
Coral Reefs (2020) 39:853–859 855
123
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e.g., Freiwald et al. 2009; Mienis et al. 2014). Thus, off
Angola, the partly high temperatures could act as a second
stressor since respiration rates of L. pertusa increase with
increasing temperature (Dodds et al. 2007).
Stress induced by low DO
conc
and relatively high tem-
peratures is energetically a challenge for the metabolism of
most marine species, but can be compensated by the
availability of large quantities of high-quality organic
matter (Diaz and Rosenberg 1995). The Angolan and
Mauritanian margins belong to highly productive upwel-
ling systems triggering extensive OMZs. Also at many
other Atlantic reef sites, L. pertusa is most abundant at
depth intervals with highest oxygen depletion (Freiwald
2002; Georgian et al. 2016), most likely linked to highest
concentrations of suspended food particles in this layer
(e.g., Freiwald 2002) which also applies to Angola (Fig. 3).
Comparing ambient DO
conc
and temperature with site-
specific net primary productivity, used as a food supply
indicator, for several Atlantic CWC sites, it appears plau-
sible that the negative effects of hypoxia and high tem-
peratures on L. pertusa seemingly could be compensated
by significantly enhanced food supply (Fig. 4).
With respect to L. pertusa preferring regional oxygen
minima, ambient DO
conc
cannot provide any information
about its capability to also cope with lower DO
conc
.
However, some information is provided by the aforemen-
tioned laboratory experiments. Lophelia pertusa collected
in the NE Atlantic and the Gulf of Mexico could not
withstand DO
conc
of less than 40–50% of the ambient
values (see above, Dodds et al. 2007; Lunden et al. 2014).
Consequently, the range of low DO
conc
tolerable by L.
pertusa—also beyond its natural environment—might
depend on the conditions the corals are acclimated to, thus
pointing to a possible genotypic adaptive capacity of L.
pertusa. Thus, although on a global scale the tolerable
DO
conc
limits for L. pertusa range from \1to
[6mLL
-1
, smaller ranges define these limits on regional
scales.
The future of Lophelia pertusa in a changing ocean
Cold-water coral reefs are vulnerable marine ecosystems
that are partly protected within marine protected areas.
These can safeguard CWC from destructive human impact
(e.g., bottom trawling, hydrocarbon exploration), but offer
no sustainable protection against global change-induced
threats. In concert with ocean acidification (e.g., Turley
et al. 2007) and warming of intermediate waters (e.g.,
Lunden et al. 2014), also deoxygenation is expected to
become a major stressor for CWC (e.g., Sweetman et al.
bFig. 1 Multibeam bathymetry map showing the distribution of cold-
water coral reefs off Angola. Locations of CTD casts, benthic lander
deployments, and ROV dives are indicated
Fig. 2 Thriving cold-water
corals observed in the oxygen
minimum zone (OMZ) off
Angola. a, b Lophelia pertusa
reefs in the center of the OMZ
(350 m water depth).
cTransported but alive L.
pertusa colony in the lower
OMZ (500 m depth). dLophelia
pertusa colony with many living
polyps (439 m depth) (ROV
images ÓMARUM)
856 Coral Reefs (2020) 39:853–859
123
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2017). However, L. pertusa’s general capacity to thrive
under well-oxygenated as well as hypoxic bottom waters
reveals a rather high oxygen tolerance, although individual
L. pertusa populations appear to have limited adaptive
capabilities to cope with reductions of 40–50% of ambient
DO
conc
values (Dodds et al. 2007; Lunden et al. 2014).
Consequently, the expected decrease in oxygenation of
*2% along the Atlantic continental margins until 2100
(Sweetman et al. 2017) by itself might not exert a serious
threat to L. pertusa, except for already hypoxic settings like
the Angolan margin. However, paleo studies revealed that
during the last *20,000 years regional changes in water
column structure caused the collapse of L. pertusa-
dominated ecosystems due to decreasing DO
conc
(Wien-
berg et al. 2018; Tamborrino et al. 2019). Thus, unlike a
small overall decrease in DO
conc
, major regional reductions
in DO
conc
driven by global change-induced changes in
ocean circulation have the potential to eradicate regional L.
pertusa populations.
Even if smaller decreases in DO
conc
alone might not
pose a serious threat to L. pertusa reefs, these have to be
considered in concert with other changing environmental
parameters that might form additional stressors (e.g.,
temperature and pH) with largely unknown consequences
for the coral’s biological functions. Moreover, the flux of
particulate organic carbon from the surface ocean might
WC
depo
leve
d-l
lewC
sfeer
)
m0
7
4
-033
(
Shipboard data (RV Meteor M122)
(January 2016; CTD/ROV-CTD/Lander)
Literature data (Nansen Programme)
(March to September, 12 different years)
WC gn
i
vil de
v
resbo
fo egn
arC
)
m 005-
0
5
2(
centre
of OMZ
005 004 003 002
htped reta
w(m)
Shipboard data (RV Meteor M122)
(January 2016; CTD/ROV-CTD)
012
DO (mL L )
conc
-1
012
DO (mL L )
conc
-1
fluorescence (mg m )
-3
0 0.01 0.02 0.03 0.04
6.8 days 2.6
days
2.5 days
012
DO (mL L )
conc
-1
012
DO (mL L )
conc
-1
691215
temperature (°C)
CTD (17 casts)
ROV-CTD
Lander (3 deployments) March (6 casts)
April/May (4 casts)
June/July (6 casts)
Aug/Sept (5 casts)
CTD (17 casts)
ROV-CTD
temperature fluorescence
calibrated values)
acb
Fig. 3 Hydrographic setting at the Angolan cold-water coral (CWC)
reef site recorded in January 2016. aWater-column temperature (red
symbols) and mean relative fluorescence data (green symbols)
obtained by conventional CTD and ROV-mounted CTD (temperature
only). bDissolved oxygen concentrations (DO
conc
) obtained by
conventional CTD, ROV-mounted CTD and benthic lander systems
(light gray shading indicates entire spread of DO
conc
data obtained
during RV Meteor expedition M122; same in c). cLiterature DO
conc
data spanning from March to September collected between 1995 and
2013 in the same area (Tchipalanga et al. 2018). For all graphs, the
depth intervals of either well-developed CWC reefs and/or single
living CWC colonies are marked in dark and light yellow,
respectively
Coral Reefs (2020) 39:853–859 857
123
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decline by *30% until 2100 along the Atlantic margins
(Sweetman et al. 2017), resulting in a lower food supply to
the CWC and deep-sea organisms in general, thus reducing
their capacity to cope with increasing stress.
Acknowledgements Open Access funding provided by Projekt
DEAL. We like to thank the nautical and scientific crews for on-board
assistance during RV Meteor cruise M122. This research received
support from the Deutsche Forschungsgemeinschaft (DFG) through
providing ship time and access to the ROV and through the DFG
Research Center/Cluster of Excellence ‘‘MARUM—The Ocean in the
Earth System.’’ C.O. received a scholarship by the German Academic
Exchange Service (DAAD, Grant No. 91723955) supporting her
research stay in Bremen, Germany.
Compliance with ethical standards
Conflict of interest On behalf of all authors, the corresponding
author states that there is no conflict of interest.
Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as
long as you give appropriate credit to the original author(s) and the
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use is not permitted by statutory regulation or exceeds the permitted
use, you will need to obtain permission directly from the copyright
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