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On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

May 2023
Biological reviews of the Cambridge Philosophical Society 98(5)

May 2023
98(5)

DOI:10.1111/brv.12976

License
CC BY 4.0

Authors:

Sandra Maier

Greenland Institute of Natural Resources

Sandra Brooke

Florida State University

Laurence De Clippele

University of Glasgow

Evert de Froe

Wageningen Marine Research

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The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating 'feast' conditions, interspersed with 'famine' periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these fluctuations in food availability. Laboratory and in situ measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future.

Reef-forming or structure-forming cold-water corals (CWCs) (see Table 1). (A) Desmophyllum pertusum colony on the wall of Baltimore Canyon, Western Atlantic (434 m). Credit: Deepwater Canyons 2012 Expedition NOAA-OER/BOEM/USGS. (B) Enallopsammia cf. pusilla from the Hawaiian Seamounts (800 m). Credit: NOAA-OER, 2015 Hohonu Moana. (C) Enallopsammia rostrata colony on the deep wall of the West Florida Escarpment (1900 m). Credit: Brooke et al. (2022), NOAA-OER/ROV Global Explorer. (D) Enallopsammia profunda from the coral mounds of the southeastern USA (770 m). Credit: Brooke et al. (2005), NOAA-OE. (E) Madrepora oculata from the coral mounds off Cape Canaveral, Florida (420 m). Credit: Ross & Quattrini (2009); NOAA DSCRTP/CIOERT/USGS. (F) Madrepora oculata colony on exposed rocky habitats of the Florida Straits, USA (400 m). Credit: Brooke et al. (2005), NOAA-OE. (G) Madrepora carolina colony collected from the Rosalind Bank, Nicaragua (162 m). Credit: Stephen Cairns, Smithsonian Institute of Natural History, USA. (H) Solenosmilia variabilis with individual, larger polyps of Desmophyllum dianthus on the wall of Norfolk Canyon, Western Atlantic (1200 m). Credit: Deepwater Canyons 2013 Expedition NOAA-OER/BOEM/USGS. Scale bars, green: 1 cm, blue: 5 cm, white: 10 cm.

…

Cold-water coral (CWC) reefs, hotspots of biodiversity. (A) Reef framework formed by Desmophyllum pertusum and Madrepora oculata on the Oreo CWC Mound (summit: 750 m depth), SE slope of Rockall Bank, NE Atlantic; large crinoids (orange) and stylasterid corals (white) live on the reef framework. Credit: Research cruise 64PE4202F. (B) Large colonies of D. pertusum on the West Florida Slope; these mounds provide habitat for golden crabs (Chaceon fenneri), which are fished commercially in the southeastern USA (567 m). Credit DISCOVRE expedition 2010 USGS/ BOEMRE. (C) Live and dead structure of a D. pertusum colony off Cape Canaveral, Florida (430 m) with a blackbelly rosefish (Helicolenus dactylopterus) on the top of the colony, a galatheid crab (Eumunida picta) and a Chain Catshark (Scyliorhinus cf. retifer). Credit: Ross & Quattrini (2009), NOAA DSCRTP/ CIOERT/USGS. Scale bars (top of images): 10 cm.

…

Paradox of thriving cold-water coral (CWC) reefs in the food-limited deep sea. (A) Organic matter export from the ocean surface to the deep sea, measured by sediment traps, plotted as annual flux of particulate organic carbon (POC) over depth. Green symbols show POC export from the photic zone (data from coastal water, 50 m water depth; export flux data from directly above CWC reefs are lacking); black symbols show off-shelf POC flux through the water column (data from moored sediment traps); blue symbols show POC flux close to cold-water coral (CWC) reefs (data from sediment traps on benthic landers). Dashed line indicates transition from photic zone to deep sea at 200 m water depth. (B) Simplified organic carbon (OC) budget of CWC reefs, illustrating the mismatch between high C turnover, high OC stock in reef biomass, and low POC deposition measured by sediment traps. OM, organic matter. References for (A): Wassmann (1990); Antia et al. (2001); Bermuda Atlantic Time-series Study (BATS), see Steinberg et al. (2001); Smith & Rabouille (2002); Duineveld et al. (2004); Lavaleye et al. (2009); Mienis et al. (2009, 2012); van Oevelen et al. (2009); Khripounoff et al. (2014). Data set summarised in Table S1. References for B: POC deposition as in A; C turnover: Cathalot et al. (2015); De Froe et al. (2019) and references therein; Reef OC stock: De Clippele et al. (2021b).

…

Primary productivity (A: annual mean, B: annual range) and annual mean current velocity (C) at sites with cold-water corals (in grey) in comparison to global values (in blue). Note log-transformed values; for original data and units see Fig. 3 and Table 3. Boxes of boxplots indicate median, first and third quartiles, dotted lines show minimum and maximum values without outliers. Asterisks indicate significant differences between coral sites and global values [P < 0.05; KruskalWallis rank-sum tests with post hoc Dunn tests; R package FSA (Ogle et al., 2018); for detailed statistical results, see Appendix S2.

…

A simplified annual carbon budget for the cold-water coral Desmophyllum pertusum, showing C expenses (right side), leading to estimations of C demand (left side) and corresponding food requirement (phytoplankton, zooplankton). For explanation, references, and calculations see Section III and Appendix S3. DM, dry mass; OC, organic carbon.

…

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On the paradox of thriving cold-water coral

reefs in the food-limited deep sea

Sandra R. Maier

1,2,

*,Sandra Brooke

,Laurence H. De Clippele

,Evert de Froe

5,6

Anna-Selma van der Kaaden

,Tina Kutti

,Furu Mienis

and Dick van Oevelen

Greenland Climate Research Centre, Greenland Institute of Natural Resources, Kivioq 2, PO Box 570, Nuuk 3900, Greenland

Department of Estuarine and Delta Systems, Royal Netherlands Institute for Sea Research (NIOZ), Korringaweg 7, Yerseke 4401 NT,

The Netherlands

Coastal & Marine Laboratory, Florida State University, 3618 Coastal Highway 98, St. Teresa, FL 32327, USA

Changing Oceans Research Group, School of GeoSciences, University of Edinburgh, Grant Institute, King’s Buildings, Edinburgh, EH9 3FE, UK

Centre for Fisheries Ecosystem Research, Fisheries and Marine Institute at Memorial University of Newfoundland, 155 Ridge Rd, St. John’sNL

A1C 5R3, Newfoundland and Labrador, Canada

Department of Ocean Systems, Royal Netherlands Institute for Sea Research (NIOZ), PO Box 59, Den Burg (Texel) 1790 AB, The Netherlands

Institute of Marine Research (IMR), PO box 1870 Nordnes, Bergen NO-5817, Norway

ABSTRACT

The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary

production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity

compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We crit-

ically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access

data on CWC habitats. This review shows ﬁrstly that CWCs typically occur in areas where the food supply is not con-

stantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zoo-

plankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’conditions, interspersed

with ‘famine’periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder

Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these ﬂuctuations in food availability.

Laboratory and in situ measurements revealed their dietary ﬂexibility, tissue reserves, and temporal variation in growth

and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention:

acting as giant ﬁlters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains

over losses. Anthropogenic pressures, including climate change and ocean acidiﬁcation, threaten this fragile equilibrium

through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework.

Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in

the future.

Key words: trophic interaction, carbon, nitrogen, respiration, recycling loop, ecosystem engineer, organic matter,

cold-water coral reef, climate change, food web.

CONTENTS

I. Introduction .........................................................................2

II. Food supply to cold-water coral reefs ......................................................7

(1) Are cold-water coral reefs limited to locations with elevated food supply? ...................... 7

(2) Food pulses created by hydrodynamic processes ......................................... 9

(3) Seasonal variability of food pulses ................................................... 11

(4) The role of live zooplankton ....................................................... 12

*Author for correspondence (Tel.: +299 233 171; E-mail: sama@natur.gl).

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium,

provided the original work is properly cited.

Biol. Rev. (2023), pp. 000–000. 1

doi: 10.1111/brv.12976

III. Adaptations of cold-water corals to the feast–famine environment ...............................12

IV. How do cold-water coral reefs sustain their high food demand? .................................15

(1) The reef ﬁlter ................................................................... 15

(2) Recycling of metabolic ‘waste’products .............................................. 15

V. Perspectives: cold-water coral reefs in the anthropocene .......................................18

(1) Disbalanced energy budget of cold-water corals ........................................ 18

(2) Reduced reef functioning on ‘crumbling’reefs ......................................... 20

(3) Conservation of cold-water coral reefs in the Anthropocene ............................... 20

VI. Conclusions .........................................................................21

VII. Acknowledgements ...................................................................21

VIII. References ..........................................................................21

IX. Supporting information ................................................................28

I. INTRODUCTION

The deep sea is the largest habitat on Earth, located

below the continental shelf break from ca. 200 m water

depth (Ramirez-Llodra et al., 2010,2011). Here, far

below the productive waters at the ocean surface, cold-

water corals (CWCs, Fig. 1) form reefs of surprisingly

high biodiversity, biomass, and metabolic activity

(Fig. 2,Freiwaldet al., 2004; Roberts, Wheeler &

Freiwald, 2006;Cathalotet al., 2015;DeClippele

et al., 2021a).

CWCs encompass different taxonomic groups within the

classes Hexacorallia, Octocorallia (sensu McFadden,

Ofwegen & Quattrini, 2022), and Hydrozoa. In contrast to

their well-known warm-water relatives, CWCs occur at rela-

tively low temperatures (i.e. <14 C for reef-building CWCs;

Freiwald et al., 2004;Gomez et al., 2022), facilitating an

almost global distribution in the deep sea (i.e. >200 m water

depth, Fig. 3A). However, they can also occur at shallower

depths, e.g. at 36 m depth in Norwegian fjords, when ocean-

ographic conditions are suitable. Many CWCs create struc-

turally complex and diverse ‘marine animal forests’

(reviewed by Rossi et al., 2017), including soft coral

(Octocorallia) gardens (e.g. Long et al., 2020; Schejter

et al., 2020), black coral (Antipatharia) gardens (e.g. Rakka

et al., 2017,2020), lace coral (Stylasteridae) gardens

(e.g. Di Camillo et al., 2017), and stony coral (Scleractinia)

reefs. In this review, we focus on scleractinian CWCs that

can form or contribute to large, long-lasting carbonate reefs

in the deep sea (Table 1). Small coral polyps (<1 cm diame-

ter; Filander et al., 2021) secrete an aragonite (calcium car-

bonate) skeleton and together can form 1.5 m-high CWC

colonies (Fig. 1; Wilson, 1979). Live polyps are restricted to

the upper and outer parts of the colonies, as coral polyps in

the inner parts become shaded from food-delivering currents

and die (Fig. 2; Wilson, 1979; Mortensen & Fosså, 2006;

Hennige et al., 2021). The carbonate skeleton becomes

exposed to physical and biological erosion (Beuck &

Freiwald, 2005), which causes fragments to break off and

develop into new colonies around the original colony

(Fig. 2). The extending coral framework traps mobile

(e.g. resuspended) sediment, leading to framework cementa-

tion and formation of elevated, kilometres-long CWC reefs

(Dorschel et al., 2005; Roberts et al., 2006). Over time, CWCs

develop large carbonate structures such as the CWC mounds

at Rockall Bank in the North East Atlantic, which are 300 m

high and thousands to millions of years old (Roberts

et al., 2006).

The topologically complex reef framework, especially

the ‘dead’skeleton, provides habitat, feeding grounds

and spawning/nursery areas for a variety of associated spe-

cies (Fig. 2), including sessile suspension feeders, such as

sponges, other corals, and bivalves (Jonsson et al., 2004;

Mortensen & Fosså, 2006; Henry & Roberts, 2007,2016;

Cordes et al., 2008), mobile invertebrates, and commer-

cially and socio-economically valuable ﬁsh (Costello

et al., 2005;Henryet al., 2013;Kuttiet al., 2014). Further-

more, a diverse microbial community grows on and inside

the reef framework and associated with reef animals

such as sponges and corals (Schöttner et al., 2012,2013;

Cardoso et al., 2013; van Bleijswijk et al., 2015). The biodi-

versity of CWC reefs is on a par with tropical shallow-

water coral reefs (Jonsson et al., 2004;Mortensen&

Fosså, 2006; Henry & Roberts, 2007) and directly beneﬁts

humanity, e.g. through the provision of ﬁsheries species for

food and biotechnological resources for drug development

(Rocha et al., 2011;Armstronget al., 2014). Moreover, the

reefs form hotspots of biomass, metabolic activity, and car-

bon (C) and nitrogen (N) turnover in the deep sea (van

Oevelen et al., 2009;Cathalotet al., 2015;DeFroe

et al., 2019; De Clippele et al., 2021a,b). Due to their high

organic matter retention and biomass, CWC reefs have

the potential to sequester C for decades to centuries

(Dorschel et al., 2007;Titschacket al., 2009; Coppari,

Zanella & Rossi, 2019).

The high biodiversity, biomass and metabolic activity

of CWC reefs appear paradoxical, as the deep

seaﬂoor belongs to the most food-limited habitats on

Earth (Ramirez-Llodra et al., 2010). Due to the absence

of light, CWCs lack zooxanthellae (Freiwald et al., 2004),

i.e. symbiotic dinoﬂagellates that contribute to the

nutrition of most reef-building shallow-water corals

(Goldberg, 2013). Like most deep-sea benthos, CWCs

depend on organic matter produced in the sunlit surface

waters, such as phytodetritus (remains of phytoplankton),

zooplankton, and zooplankton remains (e.g. dead

2Sandra R. Maier and others

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Fig. 1. Reef-forming or structure-forming cold-water corals (CWCs) (see Table 1). (A) Desmophyllum pertusum colony on the wall of

Baltimore Canyon, Western Atlantic (434 m). Credit: Deepwater Canyons 2012 Expedition NOAA-OER/BOEM/USGS.

(B) Enallopsammia cf. pusilla from the Hawaiian Seamounts (800 m). Credit: NOAA-OER, 2015 Hohonu Moana.

2022), NOAA-

OER/ROV Global Explorer. (D) Enallopsammia profunda from the coral mounds of the southeastern USA (770 m). Credit: Brooke

et al.(

2005), NOAA-OE. (E) Madrepora oculata from the coral mounds off Cape Canaveral, Florida (420 m). Credit: Ross &

Quattrini (2009); NOAA DSCRTP/CIOERT/USGS. (F) Madrepora oculata colony on exposed rocky habitats of the Florida

Straits, USA (400 m). Credit: Brooke et al.(

2005), NOAA-OE. (G) Madrepora carolina colony collected from the Rosalind Bank,

Nicaragua (162 m). Credit: Stephen Cairns, Smithsonian Institute of Natural History, USA. (H) Solenosmilia variabilis with

individual, larger polyps of Desmophyllum dianthus on the wall of Norfolk Canyon, Western Atlantic (1200 m). Credit: Deepwater

Canyons 2013 Expedition NOAA-OER/BOEM/USGS. Scale bars, green: 1 cm, blue: 5 cm, white: 10 cm.

Cold-water coral reefs 3

zooplankton, faecal pellets) (Duineveld, Lavaleye &

Berghuis, 2004;Duineveldet al., 2007;Naumann

et al., 2015;vanOevelenet al., 2018). Phytodetritus and zoo-

plankton faecal pellets aggregate and slowly sink from the

photic zone to the deep sea as exported particulate organic

matter (POM) (Turner, 2015). In addition, live zooplankton

perform diurnal and/or seasonal vertical migrations

between shallow and deep waters (Bandara et al., 2021). As

passive suspension feeders, CWCs require currents to

deliver food particles (Hamann & Blanke, 2022), which they

capture with their tentacles or with mucus nets (Zetsche

et al., 2016; Murray et al., 2019).

With increasing depth, the vertical ﬂux of particulate

organic carbon (POC) decreases exponentially (Fig. 4A),

as zooplankton and bacterioplankton consume a substan-

tial fraction of the sinking organic material (Suess, 1980;

Lutz, Dunbar & Caldeira, 2002;Boyd&Trull,2007). In

the North Atlantic, 2.5 to 10 mol POC m

−2

year

−1

exported from the photic zone in coastal areas, but only

around 0.1 mol POC m

−2

year

−1

(1–4%) arrives in the

bathyal deep sea (>200 m; Fig. 4A, see online Supporting

Information, Table S1). On CWC reefs, 0.0003–3.5 mol

POC m

−2

year

−1

are deposited, as measured by sediment

traps deployed at 481–850 m water depth (Fig. 4A).

At the same time, CWC reefs respire 4–45 mol

oxygen m

−2

year

−1

,upto20timesmorethanadjacent

soft-sediment communities [respiration rates extrapolated

from daily measurements of reef-community oxygen con-

sumption on different reefs in the North Atlantic during

spring/summer (Cathalot et al., 2015; De Froe

et al., 2019)]. Assuming a respiratory quotient CO

1 (as estimated for CWCs; Khripounoff et al., 2014), this

leadstoaCturnoverof4–45 mol C m

−2

year

−1

(Fig. 4B;

note that C refers to organic C throughout this review).

To sustain this high C turnover, the reefs require an

amount C that is orders of magnitude higher than the

amount of POC deposited in sediment traps (Fig. 4B).

The reefs even seem to require a substantial part of the

entire primary production at the ocean surface [almost

100% of the local primary production above Mingulay

Reef (De Clippele et al., 2021a); 5% of the primary produc-

tion on the entire Norwegian shelf by all known Norwegian

reefs combined (Cathalot et al., 2015)]. This poses the ques-

tion: how can CWC reefs sustain their high biomass and

metabolic activity in the food-limited deep sea, given this

apparent mismatch in C supply (Fig. 4B)?

To approach this ‘CWC reef paradox’, we review the liter-

ature and open-access data and discuss the following ques-

tions: are CWC reefs limited to locations with elevated food

supply, and what mechanisms increase the food supply to

the reefs (Section II); how are CWCs adapted to their food

environment (Section III); how do CWC reefs function as eco-

system to maintain high metabolic rates (Section IV); and how

do anthropogenic threats impact food supply, coral adapta-

tions and reef functioning and jeopardise the existence of

CWC reefs; from a trophodynamic perspective, how can we

optimally protect CWC reefs? (Section V).

Fig. 2. Cold-water coral (CWC) reefs, hotspots of biodiversity.

(A) Reef framework formed by Desmophyllum pertusum and

Madrepora oculata on the Oreo CWC Mound (summit: 750 m

depth), SE slope of Rockall Bank, NE Atlantic; large crinoids

(orange) and stylasterid corals (white) live on the reef

framework. Credit: Research cruise 64PE4202F. (B) Large

colonies of D. pertusum on the West Florida Slope; these

mounds provide habitat for golden crabs (Chaceon fenneri),

which are ﬁshed commercially in the southeastern USA

(567 m). Credit DISCOVRE expedition 2010 USGS/

BOEMRE. (C) Live and dead structure of a D. pertusum colony

off Cape Canaveral, Florida (430 m) with a blackbelly roseﬁsh

(Helicolenus dactylopterus) on the top of the colony, a galatheid

crab (Eumunida picta) and a Chain Catshark (Scyliorhinus

cf. retifer). Credit: Ross & Quattrini (2009), NOAA DSCRTP/

CIOERT/USGS. Scale bars (top of images): 10 cm.

4Sandra R. Maier and others

Fig. 3. Cold-water coral (CWC) occurrence, surface productivity and benthic current velocity. Data from OBIS (2022) and

Bio_ORACLE (Tyberghein et al., 2012; Assis et al., 2018). (A) Global occurrence of Desmophyllum pertusum,Enallopsammia pusilla,

Enallopsammia profunda,Enallopsammia rostrata,Goniocorella dumosa,Madrepora carolina,Madrepora oculata, and Solenosmilia variabilis.

(B) Annual mean of daily surface primary productivity. (C) Annual range of daily surface primary productivity. (D) Annual mean

of benthic current velocity. A QGIS version of B–D can be found at https://doi.org/10.5281/zenodo.7097065.

Cold-water coral reefs 5

Table 1. Colonial, reef-building and/or structure-forming cold-water coral (CWC) species, their colony morphology, the degree to which they are reef-building, their distri-

bution, depth range (mean ±standard deviation), and the number of publications mentioning each species (Google Scholar, 01 September 2022). All species are cnidarians of the

order Scleractinia. Only species that occur at >200 m water depth were considered. References for presented information: Zibrowius (1980); Cairns (1982,1995); Koslow et al.

(2001); Reed (2002); Freiwald et al. (2004); Hebbeln et al. (2014); De Clippele et al. (2017b); Corbera et al. (2019); Raddatz et al. (2020); Filander et al. (2021); Sanna & Freiwald

(2021); OBIS (2022) and https://doi.org/10.5281/zenodo.7097065.

Species Colony morphology Reef-building Distribution

Depth range

(m water

depth)

Number of publications

mentioning species

Desmophyllum pertusum

(formerly Lophelia

pertusa; Linnaeus,

1758)

Bushy/bush-like to

cauliﬂower-shaped

Dominant reef-building CWC in North

Atlantic

Almost cosmopolitan (not found in

continental Antarctica)

480 ±184 ‘Lophelia pertusa’: 6630;

Desmophyllum pertusum:

270

Goniocorella dumosa

(Alcock, 1902)

Bushy Dominant reef-building CWC around

New Zealand

Only Southern hemisphere 462 ±239 198

Enallopsammia rostrata

(Pourtalès, 1878)

Fan-shaped, uni-planar Mostly secondary framework producer

on reefs formed by other species, but

some can also build reefs (E. profunda,

M. oculata,S. variabilis; the others are

considered ‘structure-forming’)

Almost cosmopolitan (not found in

continental Antarctica)

763 ±338 487

Enallopsammia profunda

(Pourtalès, 1867)

Irregular-fragile 667 ±212 173

Enallopsammia pusilla

(Alcock, 1902)

Bushy 568 ±233 12

Madrepora oculata

(Linnaeus, 1758)

Uniplanar zigzag-shaped

branches

654 ±307 2530

Madrepora carolina

(Pourtalès, 1871)

Fan-shaped, uni-planar 225 ±218 68

Solenosmilia variabilis

(Duncan, 1873)

Bushy Almost cosmopolitan (not found in

continental Antarctica & North

Paciﬁc)

1258 ±276 721

6Sandra R. Maier and others

II. FOOD SUPPLY TO COLD-WATER CORAL

REEFS

(1) Are cold-water coral reefs limited to locations

with elevated food supply?

CWCs are supplied with food through primary production at

the ocean surface (measured as chlorophyll-a concentration

or net primary productivity), export of primary production,

ﬂux of POM to the seaﬂoor and/or currents (horizontal

and/or vertical) that carry food particles (e.g. Duineveld

et al., 2004; Kiriakoulakis et al., 2004,2007; Davies

et al., 2009; De Froe et al., 2022). To evaluate whether

CWC reefs are limited to locations with elevated food supply,

we ﬁrst reviewed modelling studies that predict habitat suit-

ability for reef-building/structure-forming CWCs (Table 1),

based on their environmental requirements including ‘food

supply’(primary production, export, POC ﬂux and/or cur-

rent velocity; Table 2). Currents were identiﬁed as an impor-

tant predictor of CWC habitat suitability in nine out of

13 models that explicitly included currents (Table 2). The

importance of surface primary production and/or POM ﬂux

varied between the habitat suitability studies: 40% of the

30 relevant models (i.e. models that included the relevant

parameters) describe the importance of primary produc-

tion/POC ﬂux as (relatively) high, 27% as moderate, and

33% as (relatively) low.

Secondly, we carried out a global analysis to test speciﬁ-

cally whether surface primary productivity and/or benthic

current velocity were above global average at those sites

where either of the eight reef-building/structure-forming

deep-sea CWC species (Table 1) occur. Publicly available

data on the occurrence of these were obtained from

OBIS (2022; data sets are available at https://doi.org/10.

5281/zenodo.7097065). Raster layers with values for (i) the

annually averaged surface primary productivity; (ii) the

annual range of surface primary productivity as an indicator

of seasonality; and (iii) the annually averaged current velocity

were extracted from Bio-ORACLE (Tyberghein et al., 2012;

Assis et al., 2018; resolution 5 arcmin, i.e. ca. 9.2 km at equa-

tor). Bio-ORACLE compiles a global environmental data set

for species distribution modelling, based on data sets pro-

vided by the E.U. Copernicus Marine Service Information

(Assis et al., 2018). For a detailed description of the methodol-

ogy, see online supporting information Appendix S1; the full

R code for all analyses is available at https://doi.org/10.

5281/zenodo.7097065.

Our global analysis revealed that enhanced food supply

through above-average surface productivity and currents

drive the distribution of most reef-forming CWC species.

Firstly, ﬁve out of eight species (i.e. Desmophyllum pertusum,

Enallopsammia profunda,Goniocorella dumosa,Madrepora oculata,

Solenosmilia variabilis) occur in locations with higher primary

productivity than the global average (Figs 3B and 5A,

Table 3, Appendix S2). Some species, however, occur in

areas of non-enhanced (Enallopsammia pusilla,Enallopsammia

rostrata) or even lower (Madrepora carolina) primary

Fig. 4. Paradox of thriving cold-water coral (CWC) reefs in the food-limited deep sea. (A) Organic matter export from the ocean

surface to the deep sea, measured by sediment traps, plotted as annual ﬂux of particulate organic carbon (POC) over depth. Green

symbols show POC export from the photic zone (data from coastal water, 50 m water depth; export ﬂux data from directly above

CWC reefs are lacking); black symbols show off-shelf POC ﬂux through the water column (data from moored sediment traps);

blue symbols show POC ﬂux close to cold-water coral (CWC) reefs (data from sediment traps on benthic landers). Dashed line

indicates transition from photic zone to deep sea at 200 m water depth. (B) Simpliﬁed organic carbon (OC) budget of CWC reefs,

illustrating the mismatch between high C turnover, high OC stock in reef biomass, and low POC deposition measured by

sediment traps. OM, organic matter. References for (A): Wassmann (1990); Antia et al.(2001); Bermuda Atlantic Time-series

Study (BATS), see Steinberg et al.(

2001); Smith & Rabouille (2002); Duineveld et al.(2004); Lavaleye et al.(2009); Mienis

et al.(

2009,2012); van Oevelen et al.(2009); Khripounoff et al.(2014). Data set summarised in Table S1. References for B: POC

deposition as in A; C turnover: Cathalot et al.(

2015); De Froe et al.(2019) and references therein; Reef OC stock: De Clippele

et al.(

2021b).

Cold-water coral reefs 7

Table 2. Environmental parameters that best predict suitable habitat for deep-sea scleractinian cold-water corals (CWCs). The table includes only studies that explicitly ana-

lysed CWCs or CWC species (not CWC reefs) in relation to food availability (‘food parameter’) and/or currents. From these studies, the most important ‘predictors’are listed,

i.e. those environmental parameters that best predict the habitat suitability of CWCs: arag, aragonite saturation; aspect, easterly & northerly aspect; BPI, bathymetric position-

ing index; DIC, dissolved inorganic carbon concentration; nutrients, concentration of nitrate, phosphate, (silicate); O

, oxygen concentration; rugg, terrain ruggedness; S, salin-

ity; seamount, association with a seamount; shear, bottom shear stress; SST, sea surface temperature; T, temperature; TA, total alkalinity; terrain, combined terrain

parameters; v, current velocity; all parameters refer to bottom-water/seaﬂoor, unless otherwise indicated. Food parameters are: chl-a, chlorophyll-a concentration at ocean

surface; DOM ﬂux, dissolved organic matter ﬂux to the seaﬂoor; export PP, export primary productivity; NPP, net primary productivity; POC ﬂux, particulate organic matter

ﬂux to the seaﬂoor. Studies where food availability and/or current velocity were important predictors are highlighted in grey.

Study Species Region Scale Most important

predictors

Food para-

metre

Importance of

food as predictor

Importance of

currents as predictor

Davies et al.

(2008)

D. pertusum Global Global TA, aspect, arag,

DIC

chl-a Moderate to high High

NE Atlantic Regional Aspect, depth, slope Moderate Relatively high

Tittensor et al.

(2009)

Scleractinia

(pooled)

Global seamounts Global

features

arag, O

, nutrients,

DIC

Export PP,

NPP

Low Low

Davies &

Guinotte

(2011)

D. pertusum Global Global S, T, arag POC ﬂux Moderate NA

E. rostrata Depth, T, arag Moderate

G. dumosa Depth, T, arag Relatively high

M. oculata Depth, T, arag Moderate

S. variabilis Depth, T, arag Moderate

Tracey et al.

(2011)

E. rostrata New Zealand Regional POC ﬂux, DOM,

depth

POC ﬂux,

DOM

ﬂux

High NA

G. dumosa Depth, seamount Relatively low

M. oculata Seamount, DOM High

S. variabilis Depth, seamount Moderate

Rengstorf et al.

(2013)

D. pertusum

reef

Irish continental margin, NE Atlantic Local Slope, T, shear NA High [vertical &

bottom shear

stress]

Georgian et al.

(2014)

D. pertusum Gulf of Mexico Regional Hard substrate,

depth, BPI

POC ﬂux Low NA

Rengstorf et al.

(2014)

D. pertusum

framework

CWC provinces, NE Atlantic Local Shear, BPI, slope,

vertical ﬂow

NA High [bottom shear

stress]

De Clippele

et al.(

2017a)

D. pertusum

reef

Mingulay Reef Complex, NE Atlantic Local Depth, rugosity,

BPI, v

NA Relatively high

Bargain et al.

(2018)

D. pertusum Mediterranean Sea canyons Regional

features

rugg, BPI, v, T NA High

M. oculata

Chu et al.

(2019)

Scleractinia

(pooled)

Canadian NE Paciﬁc Regional O

, SST, arag chl-a Relatively low Moderate [vertical &

horizontal]

Georgian et al.

(2019)

E. rostrata New Zealand +adjacent S Paciﬁc Regional T, rugg, arag POC ﬂux Relatively low NA

G. dumosa T, arag, rugg Relatively high

M. oculata BPI, arag, T moderate

S. variabilis rugg, arag, % gravel Relatively low

Barbosa et al.

(2020)

D. pertusum Brazilian continental margin, W Atlantic Regional Depth, T, arag POC ﬂux Relatively low Relatively high

[vertical]E. rostrata Depth, arag, T Relatively low

M. oculata Depth, T, arag High

S. variabilis S, depth, POC ﬂux High

(Continues on next page)

8Sandra R. Maier and others

productivity compared to global values (Figs 3B and 5A). A

preference for sites with enhanced primary production does

not correlate with species-speciﬁc differences in depth range

(Table 1). Overall, the corals tolerate a broad range of

annual primary productivity (Table 3). Secondly, six out

of eight reef-forming CWC species occur in areas with

above global-average current velocity (Figs 3D and 5C,

Table 3). According to our analysis, reef-forming CWCs

occur under current velocities of 0.11 ±0.07 m s

−1

(mean ±SD; Table 3). With their large, three-dimensional,

branching skeletal framework, the corals locally reduce cur-

rent velocities and create niches with optimal ﬂow for their

prey capture (Hennige et al., 2021; Sanna, Büscher &

Freiwald, 2023), i.e. 0.05 m s

−1

for phytoplankton (phyto-

detritus) capture and 0.02 m s

−1

for zooplankton capture

(Purser et al., 2010;Orejaset al., 2016). Currents further

drive CWC distribution as they facilitate speciﬁc hydrody-

namic processes, which spatially and temporally increase

the food supply (see Section II.2).

In summary, food supply is an important driver of CWC

reef distribution and the combination of enhanced current

velocity and increased primary production (among other

environmental drivers) can act as powerful predictors of

CWC reef presence. However, food supply on and around

CWC reefs varies at small spatial and temporal scales, as

reviewed below. Accordingly, attempts to predict CWC reef

distribution are more or less limited by the resolution of envi-

ronmental data and the lack of true coral-absence data, due

to the high logistic effort and associated costs of surveys

(Davies et al., 2008; Georgian, Morgan & Wagner, 2021).

In the future, increasing resolution of environmental data,

especially of less-common parameters such as POM ﬂux,

high-resolution hydrodynamic models and an increasing

number of benthic deep-sea surveys globally (Ramirez-

Llodra et al., 2010) will likely improve our ability to predict

CWC reef occurrences (Rengstorf et al., 2014).

(2) Food pulses created by hydrodynamic processes

Instead of a constantly low food supply, CWCs live in a

dynamic environment, where hydrodynamic processes cre-

ate periodic food pulses at different temporal scales, from a

few hours for processes linked to internal tidal activity

(e.g. Davies et al., 2009; Duineveld et al., 2012; De Froe

et al., 2022), to seasonal cycles (e.g. Mienis et al., 2009; Navas

et al., 2014; van der Kaaden et al., 2021) and multiyear cycles

such as decadal oscillations (e.g. Guihen, White &

Lundälv, 2012; Kazanidis et al., 2021b; Raddatz et al., 2022)

and millennial-scale oscillations (Portilho-Ramos et al.,

2022). Currents interact with the seaﬂoor, especially with ele-

vated seaﬂoor structures such as oceanic banks [e.g. Galicia

Bank and Rockall Bank in the North Atlantic (Duineveld

et al., 2004,2007; White et al., 2005)], continental margins

[e.g. the shelf edges of the Faroe islands and Norway

(Frederiksen, Jensen & Westerberg, 1992; Thiem

et al., 2006)], seamounts (globally, reviewed by White

et al., 2007), and fjord sills [e.g. in Norway (Rüggeberg

Table 2. (Cont.)

Study Species Region Scale Most important

predictors

Food para-

metre

Importance of

food as predictor

Importance of

currents as predictor

Burgos et al.

(2020)

D. pertusum Nordic Seas (Norway Sea, Greenland Sea,

Icelandic Sea, part of Barents Sea)

Regional T, depth, terrain POC ﬂux,

NPP

Relatively high Relatively low

M. oculata T, terrain, depth Low Relatively low

S. variabilis Depth, T, v Low Relatively high

Kinlan et al.

(2020)

Scleractinia

(pooled)

US continental shelf, NW Atlantic Regional T, depth, chl-a chl-a High NA

Morato et al.

(2020)

D. pertusum N Atlantic Regional T, POC ﬂux, arag POC ﬂux High NA

M. oculata T, POC ﬂux, arag High

Sundahl et al.

(2020)

D. pertusum Norwegian continental shelf Regional BPI, sediment, T, v chl-a Relatively high High

Georgian et al.

(2021)

Scleractinia

(pooled)

S Paciﬁc off Peru Regional Arag, BPI, rugg,

nutrients, POC

ﬂux

POC ﬂux Relatively high NA

Cold-water coral reefs 9

et al., 2011; Wagner et al., 2011)]. Similar current–seaﬂoor

interactions are caused by large CWC mounds themselves,

e.g. in the Logachev mound CWC province at the slope of

Rockall Bank (Mienis et al., 2007; Cyr et al., 2016;

Soetaert et al., 2016; van der Kaaden et al., 2021).

These current–topography interactions generate periodic

hydrodynamic events like internal tides, trapped waves, and

hydraulic jumps (Mohn et al., 2014; van Haren et al., 2014;

Cyr et al., 2016). For instance, if an elevated structure par-

tially blocks (tidal) currents, the isopycnals are depressed

downstream of this structure, resulting in so-called ‘hydraulic

jumps’(Mohn et al., 2014). Isopycnal depressions and

hydraulic jumps accelerate the downward transport of

organic matter, from typical particle sinking speeds of a few

to hundreds of metres per day (Riley et al., 2012) to vertical

transport at 10 cm s

−1

, corresponding to >8.5 km day

−1

(Davies et al., 2009; Juva et al., 2020). As a result, fresh organic

matter is transported from surface waters to CWC reefs in

less than 1 h [at the 140 m deep Mingulay reef (Davies

et al., 2009; Findlay et al., 2013)]. As the tide reverses, this

food pulse moves over the reef and supplies the entire reef

community (Davies et al., 2009). Accordingly, fresh, lipid-rich

(high-quality) suspended POM has been documented in the

bottom water above several CWC reefs/mounds in the

North Atlantic (Kiriakoulakis et al., 2007; Mienis

et al., 2007; Davies et al., 2009; De Froe et al., 2022).

Enhanced concentrations of fresh POM can occur in diurnal

or semi-diurnal pulses, linked to the site-speciﬁc internal tidal

cycle (Duineveld et al., 2007; Mienis et al., 2007; Davies

et al., 2009; De Froe et al., 2022). The downward transport

of surface organic matter is most pronounced on or close to

the reef crest or mound summit (Cyr et al., 2016); accord-

ingly, live CWCs are most abundant here (De Haas

et al., 2009; Lim, Wheeler & Arnaubec, 2017; Conti, Lim &

Wheeler, 2019; Maier et al., 2021). The fact that large

CWC mounds can induce a downward transport of surface

organic matter with their own structure (Mienis et al., 2007;

Mohn et al., 2014; Soetaert et al., 2016) represents a positive

feedback of these mounds on coral growth (van der Kaaden

et al., 2020), a remarkable form of ecosystem engineering

(sensu Jones, Lawton & Shachak, 1994).

Next to accelerating vertical particle transport, tidal cur-

rents and internal waves resuspend deposited organic

material into bottom or intermediate nepheloid layers,

providing another temporal food source for the reefs

(Frederiksen et al., 1992;Whiteet al., 2005; Mienis

et al., 2007). Besides tidally induced vertical transport,

Ekman drainage was proposed as yet another mechanism

D. pertusum

–10

–8

–6

–4

–2

log(primary productivity annual mean)

–10

–8

–6

–4

–2

log(primary productivity annual range)

–8

–6

–4

–2

log(current velocity annual mean)

E. profunda

E. pusilla

E. rostrata

G. dumosa

M. carolina

M. oculata

S. variabilis

D. pertusum

E. profunda

E. pusilla

E. rostrata

G. dumosa

M. carolina

M. oculata

S. variabilis

D. pertusum

E. profunda

E. pusilla

E. rostrata

G. dumosa

M. carolina

M. oculata

S. variabilis

******

Fig. 5. Primary productivity (A: annual mean, B: annual range)

and annual mean current velocity (C) at sites with cold-water

corals (in grey) in comparison to global values (in blue). Note

log-transformed values; for original data and units see Fig. 3

and Table 3. Boxes of boxplots indicate median, ﬁrst and third

quartiles, dotted lines show minimum and maximum values

without outliers. Asterisks indicate signiﬁcant differences

between coral sites and global values [P<0.05; Kruskal–

Wallis rank-sum tests with post hoc Dunn tests; R package FSA

(Ogle et al., 2018); for detailed statistical results, see

Appendix S2.

10 Sandra R. Maier and others

of food supply to CWC reefs at shelf break regions in the

North Atlantic (White et al., 2005;Thiemet al., 2006;Simp-

son & McCandliss, 2013). Here, an along-slope surface

current is deﬂected at depth, at an angle of 90, due to

the Coriolis force (Ekman, 1905). As a result, organic

matter-rich bottom water from shallower areas above the

continental shelf is transported downwards across the slope

at velocities of ca.2cms

−1

(White et al., 2005;Thiem

et al., 2006; Simpson & McCandliss, 2013). Due to lower

velocities and longer distances cross-slope, particle trans-

port from shallow to deep water by Ekman drainage is

slower compared to tidally induced processes, but faster

than passive settling (White et al., 2005; Davies

et al., 2009;Rileyet al., 2012;Juvaet al., 2020).

In summary, depending on the prevailing hydrodynamic

regime, food availability on CWC reefs can change drasti-

cally within a couple of hours, creating a ‘feast–famine’

environment. The relative contribution of different hydrody-

namic regimes to food supply is likely reef/region-speciﬁc,

but this remains to be studied.

(3) Seasonal variability of food pulses

Most reef-forming CWC species (six out of eight) occur in

areas where primary productivity shows higher than average

annual variation (Figs 3C and 5B, Table 3,AppendixS2).In

temperate regions, such as the North Atlantic and the South

Paciﬁc, the seasonal cycle of light, temperature and nutrient

replenishment gives rise to a pronounced spring phytoplank-

ton bloom, followed by a peak in zooplankton abundance

(Lalli & Parsons, 1997). In the Gulf of Mexico, seasonal

upwelling, variations of mixed layer depth and riverine nutri-

ent discharge cause a strong variation in primary productivity

(Müller-Karger et al., 1991; Zavala-Hidalgo et al., 2006). Sea-

sonal variations in upwelling are also responsible for primary

productivity ﬂuctuations on the Mauritanian continental mar-

gin (Eisele et al., 2011) and in the North East Paciﬁc California

Current System (Gruber et al., 2012;Gomez et al., 2018). Peri-

odic peaks of surface primary production create important

food peaks for deep-sea benthos (Billett et al., 1983). During

the seasonal phytoplankton bloom, POC ﬂux, POC concen-

tration and zooplankton abundance on Tisler reef (North East

Skagerrak, depth <200 m) and Nakken reef (Norwegian fjord,

depth 200 m) increase by a factor of two or more (Lavaleye

et al., 2009;Maieret al., 2020a). Similarly, one/several annual

peaks of ﬂuorescence (ca. 30% increase) above the CWC reefs

in the Cape Lookout area (NW Atlantic) and the Gulf of

Mexico indicate seasonal pulses of fresh organic matter

(Mienis et al., 2012,2014). In between the seasonal food peaks,

the availability of phytodetritus on the reefs is low (Duineveld

et al., 2004,2007; Mienis et al., 2012,2014; van Engeland

et al., 2019). Alternative resources may then be available,

e.g. resuspended, more degraded organic matter (Mienis

et al., 2009;Maieret al., 2020a; van der Kaaden et al., 2021),

bacterioplankton, and dissolved organic matter (DOM)

(Wild et al., 2008,2009).

Today we know that daily, seasonal, annual, and decadal

cycles of primary production shape deep-sea ecosystems, just

like in shallow waters. However, the study of ‘deep-sea sea-

sonality’remains difﬁcult, especially in temperate and sub-

Table 3. Primary productivity (annual average and annual sea-

sonal range) and current velocity (annual average) at sites with

cold-water corals (CWCs) compared to the global mean.

Coordinates of CWC sites were obtained from OBIS (2022),

environmental parameters at CWC sites were provided by

Bio-ORACLE (Tyberghein et al.,2012; Assis et al.,2018), as

described in Appendix S1. For CWCs, values are given

separately for the indicated CWC species and pooled for all

species (CWCs pooled). Temperatures in CWC habitats are

additionally compared to the range of temperatures on tropical

coral reefs (Freiwald et al.,2004) because temperature inﬂuences

physiological processes (Dodds et al.,2007). All given values are

model estimates, given at a resolution of 5 arcmin (ca. 9.2 km

equatorial), not accounting for small-scale variability.

Parameter Mean ±SD at

locations with CWCs

Global

mean ±SD

Primary

productivity:

annual average

(mg m

−3

day

−1

)

CWC

pooled

7±74±5

D. pertusum 8±10

E. profunda 5±2

E. pusilla 4±2

E. rostrata 4±4

G. dumosa 9±5

M. carolina 2±3

M. oculata 6±8

S. variabilis 8±2

Primary

productivity:

annual range

(mg m

−3

day

−1

)

CWC

pooled

19 ±13 11 ±12

D. pertusum 24 ±14

E. profunda 21 ±9

E. pusilla 11 ±7

E. rostrata 8±6

G. dumosa 17 ±12

M. carolina 11 ±7

M. oculata 16 ±15

S. variabilis 16 ±7

Current

velocity: annual

average (m s

−1

)

CWC

pooled

0.11 ±0.07 0.05 ±0.04

D. pertusum 0.13 ±0.08

E. profunda 0.21 ±0.09

E. pusilla 0.06 ±0.06

E. rostrata 0.06 ±0.03

G. dumosa 0.05 ±0.03

M. carolina 0.14 ±0.1

M. oculata 0.09 ±0.09

S. variabilis 0.09 ±0.03

Temperature:

annual

average (C)

CWC

pooled

5.1 ±3.1 Global:

1.7 ±4.1;

tropical coral

reefs:

20–29 C

D. pertusum 6.5 ±2.4

E. profunda 8.5 ±2

E. pusilla 6.1 ±3.3

E. rostrata 2.5 ±1.8

G. dumosa 6.4 ±2

M. carolina 13.5 ±6.8

M. oculata 6.2 ±3.7

S. variabilis 2.7 ±1.3

Cold-water coral reefs 11

polar areas, due to their difﬁcult year-round accessibility.

Hence, seasonal C ﬂuxes to CWC reefs have only been

measured on few reefs, mostly in the North Atlantic, and

future studies should direct efforts to other CWC reefs

worldwide.

(4) The role of live zooplankton

Vertically migrating zooplankton export substantial amounts

of C, especially lipids, from the ocean surface to the deep sea

(Jonasdottir et al., 2015; Kiko et al., 2017; Bandara

et al., 2021). Most zooplankton spend the night in surface

waters, grazing on phytoplankton, and descend to deeper

waters (>300 m) at dawn to escape visual predators

(Zaret & Suffern, 1976). When passing CWC reefs, they

could create important, lipid-rich food pulses for the corals.

Vertically migrating zooplankton were observed on CWC

reefs over a large depth range, including the relatively shal-

low Tisler reef (Skagerrak, Norway, <200 m depth; Guihen,

White & Lundälv, 2018), Hola reef (Norwegian continental

shelf, 260 m depth; van Engeland et al., 2019), and Mingulay

reef (Outer Hebrides, 150 m depth; Duineveld et al., 2007),

and deeper reefs in the Santa Maria di Leuca CWC Province

(Mediterranean, 300–1100 m depth; Carlier et al., 2009), on

the Campeche mounds and in the Viosca Knoll area [Gulf of

Mexico, ca. 500 m (Mienis et al., 2012; Hebbeln et al., 2014)].

Zooplankton are typically also abundant on and above sea-

mounts, sustaining high CWC abundance (Rogers, 1994;

Duineveld et al., 2004; Rowden et al., 2010). By contrast,

the large CWC reefs on the slope of Rockall Bank (North-

East Atlantic, 800 m depth) showed a low zooplankton abun-

dance (Duineveld et al., 2007; De Froe et al., 2022).

Site-speciﬁc differences in zooplankton abundance in the

deep sea relate to patterns of primary productivity

(Hernandez-Leon et al., 2020). Furthermore, local zooplank-

ton populations have speciﬁc depth ranges, varying from

300 to 600 m, e.g. at the Bermuda-Atlantic-Time-Series sta-

tion (Sargasso Sea; Steinberg et al., 2000), to >1000 m depth,

e.g. in the Gulf of Mexico (Ochoa et al., 2013; Ursella

et al., 2021). Finally, zooplankton overwinter at depth in spe-

ciﬁc areas like the Norwegian Sea at ca. 600 m depth,

whereas other areas like the deep Rockall Trough or shal-

lower Norwegian fjords show low zooplankton abundance

in winter (Heath et al., 2000; Campbell & Dower, 2003;

Maier et al., 2020a). Corresponding to variations in abun-

dance, the importance of live zooplankton in the CWC diet

varies among reefs (Duineveld et al., 2004,2007; Carlier

et al., 2009; van Oevelen et al., 2018) and seasons (Maier

et al., 2020a). However, most information on zooplankton

food for CWCs originates from the North Atlantic, and

future research is required to reveal global patterns.

In conclusion, CWC reefs occur in a highly dynamic

‘feast–famine’environment, where food availability changes

substantially, depending on the season, the prevailing hydro-

dynamic regime, and presence of vertically migrating zoo-

plankton. During feast conditions, food supply likely

sustains reef C demand. For instance, during the productive

season, POC ﬂuxes of 3–67 mmol C m

−2

day

−1

were mea-

sured by sediment traps (Duineveld et al., 2004; Lavaleye

et al., 2009; Mienis et al., 2012; Khripounoff et al., 2014),

which is in the same order of magnitude as the reef C turn-

over of 11–123 mmol C m

−2

day

−1

(4–45 mol C

−2

year

−1

, Fig. 4B). It should be noted that sediment traps

tend to underestimate POC ﬂuxes, especially when they tilt

under high currents (Khripounoff et al., 2014). Furthermore,

additional input of zooplankton and/or dissolved organic

carbon (DOC), which are not measured by sediment traps,

may ﬁll the remaining gap. More precise reef C budgets,

however, require C ﬂux data at higher temporal and spatial

resolution and the inclusion of C ﬂuxes through zooplankton

and DOC. The comparatively low food supply to the reefs in

‘famine’periods (Duineveld et al., 2004,2007; Mienis

et al., 2012,2014; van Engeland et al., 2019)isreﬂected in

the large annual C mismatch (Fig. 4B) and suggests that other

physiological and ecological mechanisms are at play, as out-

lined in the following sections.

III. ADAPTATIONS OF COLD-WATER CORALS

TO THE FEAST–FAMINE ENVIRONMENT

As established in Section II, CWCs live in a feast–famine

environment with strong temporal ﬂuctuations in resource

availability and hydrodynamic conditions. At the same time,

CWCs have a high C demand, as illustrated by the following

simpliﬁed annual C budget for Desmophyllum pertusum (Fig. 6),

the best-studied scleractinian CWC species. Respiration

rates of D. pertusum, measured by ex situ and in situ incubations,

range between 1.1 and 2.8 mmol C (g coral dry mass) year

−1

if CO

=1 (see Section I; Larsson et al., 2013b; Larsson,

Lundälv & van Oevelen, 2013a; Khripounoff et al., 2014;

Maier et al., 2019,2020a; Baussant et al., 2022). C ﬂux (‘loss’)

associated with mucus release has been assessed in

fewer studies by ex situ incubations (Maier et al., 2011,

2016; Naumann, Orejas & Ferrier-Pagès, 2014; Maier

et al., 2019) and amounts to 0.2 mmol POC (g coral dry

mass)

−1

year

−1

(Maier et al., 2019; other studies used differ-

ent units, see Appendix S3). Together, the C demand of

D. pertusum amounts to 1.3–3.0 mmol C

(g dry mass)

−1

year

−1

(Fig. 6, Appendix S3); similar C bud-

gets for other CWC species remain to be investigated. Addi-

tional energetic costs incur for reproduction, but these are

less well established: it is known that D. pertusum,E. rostrata,

G. dumosa, and S. variabilis release a large number of small eggs

and sperm (i.e. ‘organic C’) once per year (broadcast spawn-

ing), while M. oculata produces several smaller cohorts of

larger eggs and sperm (Burgess & Babcock, 2005; Waller &

Tyler, 2005). The related C expenditure is difﬁcult to assess,

but D. pertusum showed a 50% lower organic C content after

than before the spawning season (January–March in

Norway; Brooke & Järnegren, 2013). This difference of

1.5 mmol C (g dry mass)

−1

may correspond to the amount

of spawned C and suggests a relatively high reproductive

12 Sandra R. Maier and others

cost (Maier et al., 2020a). In total, the annual C budget

of D. pertusum (Fig. 6) ranges from 2.8 to 4.5 mmol C (g dry

mass)

−1

year

−1

, or 1.1 to 1.8 mmol C polyp

−1

year

−1

(for

an average-sized D. pertusum polyp of 0.4 g dry mass; Maier

et al., 2019). To maintain this C budget, each polyp has to

capture ca. 170–2000 copepods per year [one copepod

0.9 to 6.5 μmol C (Grønvik & Hopkins, 1984; Orejas

et al., 2016; Höfer et al., 2018)] or 3 ×10

to 5 ×10

live phy-

toplankton cells per year [one phytoplankton cell

0.003 μmol C (Orejas et al., 2016)]; for calculations, see

Appendix S3.

CWCs seem to meet large parts of their annual C demand

by efﬁciently exploiting large food pulses. As passive suspen-

sion feeders, CWCs rely on water ﬂow for their food supply

(Gili & Coma, 1998). The corals are optimally adapted to

site-speciﬁc hydrodynamic conditions and food availability,

through variable colony morphology among and within spe-

cies (De Clippele et al., 2017b; Vad et al., 2017; Hennige

et al., 2021; Sanna & Freiwald, 2021; Sanna et al., 2023).

For example, fan-shaped colonies (M. carolina,E. rostrata)

often grow perpendicular to unidirectional currents, optimis-

ing prey capture (Fricke & Meischner, 1985). D. pertusum

adapts its morphology based on the prevailing hydrodynamic

conditions (Sanna et al., 2023), forming bush-like colonies

with more compact upstream branches under higher, unidi-

rectional ﬂow velocities and symmetrical cauliﬂower-shaped

colonies with thinner, ramiﬁed branches under more shel-

tered conditions with lower, multidirectional ﬂow

(De Clippele et al., 2017b). These adaptations create efﬁcient

suspension feeders. At concentrations of 100 copepods l

−1

D. pertusum can catch around 12–23 copepods polyp

−1

depending on the ﬂow speed (Orejas et al., 2016; highest

capture at 2 cm s

−1

, lowest at 10 cm s

−1

). This corresponds

to a C uptake of 11–150 μmol C polyp

−1

(using the cope-

pod C content range mentioned above; Appendix S3). Prey

capture rates increase further with increasing zooplankton

concentration (Purser et al., 2010). The smaller polyps of

M. oculata show lower capture rates of large zooplankton

compared to D. pertusum, but on the scale of a coral colony,

this effect is outweighed by the higher polyp density

(Tsounis et al., 2010). At high phytoplankton concentrations,

as may occur during rapid downwelling events in the produc-

tive season (Davies et al., 2009), D. pertusum is able to retain up

to 6 ×10

phytoplankton cells polyp

−1

, i.e. ca. 200 μmol

C polyp

−1

(Orejas et al., 2016). Hence, during such zoo-

plankton or phytoplankton food pulses, the corals might be

able to sustain 1–17% of their annual C demand in only

1 hour (for calculation, see Appendix S3). In situ data conﬁrm

the potential of CWCs to exploit food pulses and their ener-

getic value: on the Norwegian shelf, D. pertusum changes its

polyp (feeding) activity in accordance with diurnal changes

in current speed and direction, which likely cause periodic

changes in food availability (Buhl-Mortensen, Tenningen &

Tysseland, 2015; Osterloff et al., 2019). On Nakken reef

(Norwegian fjord), D. pertusum doubled its organic C content

or biomass during the annual spring bloom (Maier

et al., 2020a), showing the importance of seasonal food pulses

for the annual C budget of these corals.

CWCs store excess assimilated resources from food pulses

or periods of high food availability as tissue reserves (Maier

et al., 2019). To store reserves, CWCs contain a substantial

amount of neutral lipids, i.e. triacylglycerols for short-term

storage and wax esters for long-term storage (Dodds

et al., 2009; Larsson et al., 2013a; Galand et al., 2020). The

Fig. 6. A simpliﬁed annual carbon budget for the cold-water coral Desmophyllum pertusum, showing C expenses (right side), leading to

estimations of C demand (left side) and corresponding food requirement (phytoplankton, zooplankton). For explanation, references,

and calculations see Section III and Appendix S3. DM, dry mass; OC, organic carbon.

Cold-water coral reefs 13

build-up of lipid reserves depends on the CWC species and

diet. Experiments showed that D. pertusum prefers a zooplank-

ton diet to build-up storage lipids (Galand et al., 2020). In situ

(Norway), this species formed lipid reserves after the zoo-

plankton bloom in summer, while the earlier spring phyto-

plankton bloom (phytodetritus peak) was mostly invested in

proteins (Maier et al., 2020a). By contrast, M. oculata beneﬁts

more from a phytodetritus or mixed phytodetritus–

zooplankton diet to build up lipid stores (Galand et al., 2020).

The original hypothesis that CWCs draw on their lipid

reserves in food-limited periods was, however, not conﬁrmed

for D. pertusum. When experimentally starved, the corals

showed either no decline in storage lipids (Baussant

et al., 2017), or a decline in storage lipids that was indepen-

dent of their feeding status (high versus low food; Larsson

et al., 2013a). In temperate areas, the lipid content of

D. pertusum did not decrease steadily over winter (Dodds

et al., 2009). Nevertheless, the species did show a seasonal

cycle of build-up and decline in lipids closely related to its

gametogenesis and spawning. Lipid reserves were formed

during summer, in the period of highest oocyte growth,

maintained until late winter (December), following which

>50% were released between December and February, pre-

sumably during a mass-spawning event (Brooke &

Järnegren, 2013; Maier et al., 2020a). Hence, CWCs seem

to use their lipid reserves rather to sustain their high repro-

ductive costs than to overcome low-food periods. It appears

likely that food availability governs the reproductive timing

of broadcast-spawning CWCs for two reasons. Firstly, syn-

chronising cost-intensive spawning with the approaching

spring bloom allows the resource-depleted adult coral colo-

nies to restock (Maier et al., 2020a). Secondly, the coral larvae

start feeding at 3 weeks of age and might proﬁt from abun-

dant phytoplankton (Strömberg & Larsson, 2017). Increased

food availability may also trigger periodic spawners

(e.g. M. oculata) to produce and spawn gametes several times

a year (Waller & Tyler, 2005).

Conservation of tissue reserves, in spite of low food avail-

ability (e.g. in winter), could be facilitated by a switch to alter-

native resources. For example in the Rockall Bank area,

increased internal wave activity in winter resuspends sedi-

ment and resupplies the CWC reefs with more degraded

organic particles (Mienis et al., 2009; van der Kaaden

et al., 2021), which could, in turn, release DOM and attract

bacterioplankton. Feeding experiments demonstrated that

CWCs are able to consume these alternative resources,

i.e. bacterioplankton, detritus (D. pertusum; Mueller

et al., 2014) and DOM [D. pertusum,M. oculata (Gori

et al., 2014; Mueller et al., 2014)]. Their close association

with a species-speciﬁc microbiome (Hansson et al., 2009;

Schöttner et al., 2012) further allows D. pertusum to feed on

inorganic resources, such as inorganic C (coupled to nitriﬁca-

tion), dinitrogen and ammonium. However, these chemoau-

totrophic pathways only contributed 2% to their respiratory

C demand (Middelburg et al., 2015). Two studies underline

consumption of alternative resources in situ. Firstly, the occur-

rence of E. rostrata and M. oculata in the New Zealand region is

driven by DOM concentration (Tracey et al., 2011). Sec-

ondly, D. pertusum in a Norwegian fjord switched from a

zooplankton–phytodetritus diet to more degraded mate-

rial/bacteria in winter, indicated by decreased δ

C and

increased bacteria fatty acid trophic markers (Maier

et al., 2020a). Other studies, however, indicate that

M. oculata is a less-opportunistic feeder than D. pertusum

(Galand et al., 2020) and therefore less adapted to variations

in resource supply (Chapron et al., 2020). Future research

should address variability in resource ﬂexibility among

CWC species.

Finally, CWCs may also conserve tissue reserves and

energy through low metabolic activity and growth. Facili-

tated by lower temperatures (Table 3), the respiration rate

of CWCs is almost 60% lower compared to their tropical

zooxanthellate relatives (Naumann et al., 2011). Correspond-

ingly, CWCs grow about 10 times slower compared to their

tropical, shallow-water relatives, i.e. at rates between

0.02% mass increase per day (D. pertusum) and 0.2% per

day (M. oculata) (Orejas et al., 2011a,b). Nevertheless, growth

rates vary considerably depending on the local environmen-

tal conditions and can reach up to 4 cm year

−1

, rates compa-

rable to some shallow-water corals (Chapron et al., 2020).

While low metabolism and growth may represent general

adaptations of CWCs, their reaction to seasonal food short-

age differs among species. Under long-term (7-month) exper-

imental food deprivation, D. pertusum slowly reduced its

metabolic rate by 40–50% in total, but maintained skeletal

growth rates (Larsson et al., 2013a; Baussant et al., 2017). By

contrast, its close relative Desmophyllum dianthus (a non-reef-

building, solitary CWC) immediately and strongly reduced

skeletal growth and metabolic rate in response to short-term

experimental food deprivation (Naumann et al., 2011). In situ,

D. pertusum maintained skeletal growth and budding in sea-

sons with reduced food supply (Lartaud et al., 2014; Maier

et al., 2020a). However, increased metabolic rates and

decreased skeletal growth during the period of highest oocyte

growth suggested an energetic trade-off between reproduc-

tion and skeletal growth (Maier et al., 2020a). M. oculata

(Mediterranean) showed more pronounced seasonal differ-

ences in budding (reduced in summer) and skeletal growth

(reduced in winter/spring) compared to D. pertusum, possibly

related to its periodic reproduction or a lower dietary ﬂexibil-

ity (Lartaud et al., 2014). M. oculata may be more sensitive to

varying food availability than D. pertusum (Lartaud

et al., 2014; Chapron et al., 2020). Species-speciﬁc differences

in CWC C budgets and adaptations to low-food periods may

explain differences in distribution and resilience; hence,

future research efforts should aim at including a broader

range of different CWC species.

Interannual growth patterns also relate to ﬂuctuating food

supply. In the NW Mediterranean, D. pertusum and M. oculata

grew faster (polyp budding and/or linear growth) in years

with higher seasonal downwelling intensity caused by epi-

sodic dense shelf water events (Chapron et al., 2020). Further-

more, in years with higher sedimentation, the CWCs grew

slower, related to less-efﬁcient feeding and energetic costs of

14 Sandra R. Maier and others

sediment cleaning; in years with particularly strong currents,

the corals formed thicker colonies and allocated energy to

polyp budding over linear growth (Chapron et al., 2020).

In summary, D. pertusum is well adapted to the feast–famine

environment through its high physiological ﬂexibility: (i) phy-

todetritus and zooplankton food pulses are effectively

exploited, but when absent, the corals switch to alternative

resources; (ii) growth rates are low, but can be boosted during

high food availability; (iii) build-up and expenditure of tissue

reserves, mostly for reproduction, are synchronised with the

seasonal changes in resource supply. Additional work is

needed on the physiological ﬂexibility of other CWC species.

By contrast, the accumulated knowledge on D. pertusum pro-

vides the chance to move from simple C budgets (Fig. 6)to

more complex dynamic energy budget (DEB) models

(Kooijman, 2000; van der Meer, 2006). While rarely applied

to deep-sea species due to limited data availability, DEB the-

ory provides a useful model framework to understand, for

example, how species can grow (in size, tissue reserves) and

reproduce under varying food availability in the deep sea

(Gaudron, Lefebvre & Marques, 2021).

IV. HOW DO COLD-WATER CORAL REEFS

SUSTAIN THEIR HIGH FOOD DEMAND?

Reef-building CWCs may be well adapted to their ‘feast–

famine’environment, yet, the entire CWC reef community,

i.e. the corals and reef-associated fauna and microbes require

more food to sustain their high biomass and metabolic activ-

ity than they receive in terms of deposited particulate organic

matter (see Section I). Based on the literature reviewed here,

we suggest two interdependent mechanisms that may explain

this mismatch in the reef (organic) C budget: (i) the reef acts

as a mechanical and biological ﬁlter for phytodetritus

(POM); and (ii) recycling (re-use) of C and N within the reef

community limits material loss.

(1) The reef ﬁlter

A CWC reef represents a giant ﬁlter composed of different

ﬁlter mechanisms (mechanical and biological) and mesh sizes

(Fig. 7; Lavaleye et al., 2009; Soetaert et al., 2016; Maier

et al., 2021). The reef framework (Fig. 2) acts as mechanical

ﬁlter (Fig. 7) that bafﬂes the ﬂow and increases the deposition

of phytodetritus particles (POM; Dorschel et al., 2005; Mienis

et al., 2019). Accordingly, organic matter concentration in the

sediment below the reef framework is higher than in sedi-

ment off-reef (De Froe et al., 2019). Deeper sediment layers

below CWC reefs, however, show extremely low rates of

anaerobic C mineralisation, because most organic matter is

consumed and mineralised in the overlying ‘reef ﬁlter’

(Wehrmann et al., 2009). In addition, suspension-feeding epi-

fauna are highly abundant on CWC reefs (Mortensen &

Fosså, 2006; Henry & Roberts, 2007) and create a biological

ﬁlter for phytodetritus and zooplankton. Reef-forming

CWCs change the environment to optimise (their own) sus-

pension feeding, e.g. by modifying their hydrodynamic envi-

ronment (Hennige et al., 2021) and by reaching into the

upper, current-exposed benthic boundary layer (Buhl-

Mortensen et al., 2010). This beneﬁts other suspension-

feeding epifauna (Buhl-Mortensen et al., 2010). In a ‘habitat

cascade’, different epifauna taxa grow on top of each other

[e.g. bryozoans growing on bivalve shells (Kazanidis

et al., 2016; Kazanidis, Henry & Roberts, 2021a)] to access

fresh phytodetritus (POM; Duineveld et al., 2007). Suspen-

sion feeders have evolved a variety of feeding mechanisms

(e.g. active versus passive) and complex feeding structures spe-

cialised on different particle sizes (Gili & Coma, 1998). For

example, CWCs capture live zooplankton at high rates

(Purser et al., 2010; Orejas et al., 2016) when available (see

Section II.4). The large reef bivalve Acesta excavata

(Fabricius, 1779) shows extraordinarily high clearance rates

for phytoplankton or phytodetritus (Järnegren &

Altin, 2006), but only limited consumption of smaller-sized

bacteria (Maier et al., 2020b). By contrast, sponges such as

Geodia barretti (Bowerbank, 1858) or Mycale lingua

(Bowerbank, 1866) retain bacterioplankton with a near

100% efﬁciency (Pile, Patterson & Witman, 1996; Maier

et al., 2020b). Similarly, suspension feeders have a speciﬁc

hydrographical niche, determined, e.g. by small-scale varia-

tions in ﬂow (Henry, Davies & Roberts, 2010). Active suspen-

sion feeders are typically more reliant on POM

concentration than on POM ﬂux (Lesser, Witman &

Sebnens, 1994). Accordingly, some active suspension feeders,

e.g. the sponge Hymedesmia paupertas (Bowerbank, 1866), pre-

fer current-sheltered reef sites (Henry et al., 2010). Small-

scale spatial segregation (Purser et al., 2013; Robert

et al., 2020) may reduce competition where dietary niches

overlap (van Oevelen et al., 2018). Acting as a mechanical

and biological ﬁlter, CWC reefs deplete phytodetritus

(POM) from the bottom water (Lavaleye et al., 2009; Wagner

et al., 2011).

The branched, porous reef framework brings abundant

suspension-feeding epifauna into close contact with detriti-

vores (Mortensen et al., 1995; Henry & Roberts, 2007) and

a diverse microbial community (van Bleijswijk et al., 2015),

giving rise to a complex food web (van Oevelen

et al., 2009). Particles mechanically intercepted by the reef

framework serve as a food source for detritivores such as

echiuran worms (Kiriakoulakis et al., 2004) or ophiuroids

(Maier et al., 2021). The tube-building polychaete Eunice nor-

vegica (Linnaeus, 1767) forms a symbiosis with D. pertusum: the

polychaete beneﬁts from stealing food particles from the

coral and at the same time it keeps its host clean from

accumulating detritus and stabilises the reef framework

by building tubes between the framework branches

(Mortensen, 2001; Roberts, 2005; Mueller et al., 2013).

(2) Recycling of metabolic ‘waste’products

The high organic matter mineralisation on CWC reefs leads

to an accumulation of faunal waste products, e.g. detrital

Cold-water coral reefs 15

POM, DOM, dissolved inorganic carbon and nitrogen (DIC,

DIN) (Wild et al., 2008; Wagner et al., 2011; Khripounoff

et al., 2014; De Froe et al., 2019). For instance, CWCs release

mucus (Wild et al., 2008), a polysaccharide–protein complex,

for protection against biofouling and sedimentation and as a

feeding aid (Fig. 7; Bythell & Wild, 2011; Zetsche et al., 2016;

Murray et al., 2019). Mucus detaches from the corals (Wild

et al., 2004) and enhances the concentration of labile (high-

quality) POM downstream of the reef (Wagner et al., 2011).

Most of the mucus dissolves rapidly, creating a pool of labile

DOM (Wild et al., 2008). Typically limited in deep-sea water

(Carlson & Hansell, 2015), coral-derived labile DOM pro-

motes the activity and growth of bacterioplankton (Fig. 7;

Wild et al., 2008,2009). Bacterioplankton, in turn, provide

a high-quality substrate for reef sponges, as outlined above

(Pile et al., 1996; Leys et al., 2018; Maier et al., 2020b). The

recycling of ‘waste DOM’by bacterioplankton returns mate-

rial and energy to higher trophic levels (Fig. 7), correspond-

ing to the microbial loop in surface-waters (Azam et al., 1983).

Moreover, suspension feeders can directly consume and

recycle DOM (Fig. 7, Table 4). Deep-sea sponges are well-

known DOM consumers (Table 4), just like their shallow-

water counterparts (reviewed by De Goeij, Lesser &

Pawlik, 2017). Initially, symbiotic microbes were considered

responsible for the high DOM uptake of sponges

(Reiswig, 1981; Yahel et al., 2003; Ribes et al., 2012). Specif-

ically in high-microbial-abundance (HMA) sponges, micro-

organisms contribute 20–35% to the total sponge biomass

(Reiswig, 1981; Hentschel, Usher & Taylor, 2006). Recent

research, however, challenged this paradigm: Firstly, low-

microbial-abundance (LMA) sponges consume and assimi-

late DOM at high rates (Table 4; De Goeij et al., 2017), but

host microorganisms at concentrations only equivalent to

those in the surrounding sea water (Hentschel et al., 2006).

Secondly, stable isotope tracer experiments demonstrated

direct uptake of DOM by sponge cells (Rix et al., 2020) and

incorporation of DOM-derived C into de novo-synthesised

and/or sponge-speciﬁc fatty acids (Rix et al., 2016;

Fig. 7. The cold-water coral (CWC) ‘reef ﬁlter’and recycling of C and N within the reef community. Filtration and subsequent

consumption of phytodetritus, a form of particulate organic matter (POM), are shown in green. Production and recycling of

organic matter are in turquoise, e.g. coral mucus [POM, dissolving to dissolved organic matter (DOM)], sponge detritus, or

bivalve (pseudo-)faeces. Production and recycling of inorganic matter is in light blue, i.e. dissolved inorganic C (DIC) and N (DIN;

ammonium recycling for example).

16 Sandra R. Maier and others

Bart et al., 2020). Thirdly, several other suspension-feeding

taxa on CWC reefs consume and assimilate DOM, including

several scleractinian CWC species (Gori et al., 2014; Mueller

et al., 2014), hydrozoans, stylasterid corals, and bivalves

(Maier et al., 2020b,2021). The faunal and microbial com-

munity growing on and inside the reef framework meets

30% of its respiratory C demand by uptake of natural

DOM (Maier et al., 2021), demonstrating the quantitative

importance of this recycling pathway.

In a recycling pathway termed the ‘sponge loop’, sponges

recycle substantial amounts of assimilated DOM to particu-

late ‘sponge detritus’(POM; Fig. 7), which is consumed by

reef detritivores (De Goeij et al., 2013). Originally described

for tropical coral reefs (De Goeij et al., 2013), the sponge loop

ﬁnds an equivalent on CWC reefs (Rix et al., 2016; Bart

et al., 2021a). Other suspension feeders, such as bivalves, like-

wise recycle substantial amounts of DOM to detrital POM,

in this case bivalve (pseudo-)faeces, which can be consumed

by reef detritivores (Maier et al., 2020b). The prevalence of

DOM consumption by reef invertebrates (Table 4) suggests

that these ‘suspension feeder’loops (Fig. 7; Maier

et al., 2020b; Bart et al., 2021a) are ubiquitous within the

CWC reef community and future research is likely to

reveal more.

Finally, DIC and DIN are recycled by reef microbes that

grow on and inside the porous reef framework and as symbi-

onts in invertebrates (Fig. 7). Nitrifying bacteria and archaea

associated with the reef framework (van Bleijswijk et al., 2015)

subsist on (faunal) ammonium, which they transform to

nitrate (nitriﬁcation; Maier et al., 2021); thereby gaining

energy for chemoautotrophic DIC ﬁxation. Furthermore,

HMA sponges and their diverse microbiome (Hentschel

et al., 2006) perform a variety of nutrient ﬂuxes together,

e.g. aerobic and anaerobic respiration, nitriﬁcation of

sponge-derived ammonium and coupled DIC ﬁxation, deni-

triﬁcation of nitrate to dinitrogen gas, and anaerobic ammo-

nium oxidation (anammox) (Hoffmann et al., 2009;De

Kluijver et al., 2021). Microbially ﬁxed C is transferred to

the sponge hosts (van Duyl et al., 2020), e.g. via the consump-

tion of microbes via phagocytosis (Leys et al., 2018). Mediat-

ing diverse internal and external recycling pathways,

sponges act on and connect several trophic levels and play

Table 4. Consumption of dissolved organic matter (DOM) by benthic invertebrates from cold-water coral reefs and deep-sea sponge

grounds. HMA, high-microbial abundance sponge; LMA, low-microbial abundance sponge. POM, particulate organic matter.

Study DOM substrate Species Phylum, class, (description)

Van Duyl et al.(

2008)

H-leucine (amino acid) Higginsia thielei Porifera, Demospongiae (HMA)

Nodastrella nodastrella

(formerly: Rossella nodastrella)

Porifera, Hexactinellida (massive, HMA)

Gori et al.(

2014) Dissolved free amino acids Desmophyllum pertusum,

Desmophyllum

dianthus,Dendrophyllia cornigera,

Madrepora oculata

Cnidaria, Anthozoa

Mueller et al.(

2014)

C-dissolved free amino acids Desmophyllum pertusum Cnidaria, Anthozoa

Rix et al.(

2016) Coral mucus (POM, DOM) Hymedesmia coricea Porifera, Demospongiae (encrusting,

LMA)

Kazanidis et al.(

2018)

C-glucose Spongosorites coralliophaga Porifera, Demospongiae (massive)

Bart et al.(

2020)

C-DOM (from lysed

diatoms)

Geodia barretti Porifera, Demospongiae (massive, HMA)

Hymedesmia paupertas Porifera, Demospongiae (encrusting,

LMA)

Vazella pourtalesii Porifera, Hexactinellida (massive, LMA)

Maier et al.(

2020b)

C-DOM (from lysed

diatoms)

Geodia barretti Porifera, Demospongiae (massive, HMA)

Acesta excavata Mollusca, Bivalvia

Bart et al.(

2021b) Natural DOM Vazella pourtalesii Porifera, Hexactinellidae (LMA; massive)

Geodia barretti Porifera, Demospongiae (HMA; massive)

Geodia atlantica Porifera, Demospongiae (HMA; massive)

Acantheurypon spinispinosum Porifera, Demospongiae (LMA;

encrusting)

Maier et al.(

2021)

C-DOM (from lysed

diatoms)

Porifera Porifera

Stylasteridae Cnidaria, Hydrozoa

Protanthea simplex Cnidaria, Anthozoa

Alcyonacea Cnidaria, Anthozoa

Asperarca nodulosa Mollusca, Bivalvia

Pectinidae Mollusca, Bivalvia

Lima marioni Mollusca, Bivalvia

Ophiuroidea Echinodermata, Ophiuroidea

Hesionidae Annelida, Polychaeta

Chaetopterus sp. Annelida, Polychaeta

Polynoidae Annelida, Polychaeta

Cold-water coral reefs 17

an ubiquitous role in deep-sea ecosystems (Hanz et al., 2022).

CWCs also host a microbiome, enabling them to perform

similar nutrient ﬂuxes, but these play a minor quantitative

role in the total CWC metabolism (Middelburg et al., 2015).

Altogether, the microbial community contributes substan-

tially to the total organic matter mineralisation of CWC reefs

(van Oevelen et al., 2009; Maier et al., 2021).

In conclusion, the high ecological efﬁciency of CWC reefs

may explain the mismatch in their organic C budget

(Fig. 4B). While the ‘reef ﬁlter’ensures optimal retention

of zooplankton, phytodetritus, and bacterioplankton, sedi-

ment traps only measure the deposition of phytodetritus

(POM). Hence, sediment traps underestimate the actual

food retention by CWC reefs, especially under high current

velocities (Gardner, Biscaye & Richardson, 1997; Mienis

et al., 2009; van Oevelen et al., 2009). Moreover, diverse tro-

phic interactions and material recycling facilitate optimal

utilisation of the retained food and exploitation of additional

resources beyond deposited POM, such as dissolved organic

and inorganic matter. Nevertheless, the quantitative impor-

tance of recycling pathways and their link in the reef food

web remain vague. Modern mapping attempts of reef bio-

mass and metabolic activity detail the importance of CWC

reefs in the regional C cycle (De Clippele et al., 2021a,b). In

a logical next step, reef food web (C cycling) models

(e.g. van Oevelen et al., 2009) could be updated with recy-

cling pathways to estimate how much of the retained and/or

metabolised material is recycled, how ﬁltration and recy-

cling contribute to reef (biomass) growth, and how much

metabolic ‘waste’material is lost from the reef ecosystem.

Another essential question in this context is the importance

of (functional) biodiversity for the ﬁltration and recycling

capacity of the reef, and hence its biomass, metabolic activity

and resilience to changing conditions, which we discuss in

the following section.

V. PERSPECTIVES: COLD-WATER CORAL

REEFS IN THE ANTHROPOCENE

In the Anthropocene, each of the mechanisms discussed

above that sustain CWC reefs in the food-limited deep sea

have become threatened. The ocean, including the deep

sea, is becoming warmer, less well mixed and more acidic,

with pollution, ﬁsheries and mining aggravating global

change (Gruber, 2011; Roberts & Cairns, 2014; Sweetman

et al., 2017). Anthropogenic environmental change disba-

lances the energy budget of reef-building corals (Fig. 8A)

and destabilises the reef framework, resulting in decreased

reef biodiversity and functioning (Fig. 8B).

(1) Disbalanced energy budget of cold-water corals

A disbalanced energy budget of CWCs is the result of

decreasing food supply on the one hand, and increasing ener-

getic costs on the other (Fig. 8A). As the ocean surface is

warming more rapidly than the rest of the water column,

the water column becomes more stratiﬁed (Bopp

et al., 2001; Gruber, 2011; Capotondi et al., 2012). Enhanced

stratiﬁcation decreases the intensity of the hydrodynamic

mixing processes (Bopp et al., 2001;Liet al., 2020) that supply

CWC reefs with important food pulses (see Section II.2). In

addition, reduced upwelling of nutrient-rich bottom water

limits diatom growth, further reducing POM export (Bopp

et al., 2005).

At the same time, bottom-water temperature in the

bathyal is projected to increase by 3–4C by 2100 (Mora

et al., 2013; Sweetman et al., 2017). Increasing temperatures

spur the corals’respiratory activity and metabolic costs

(Dodds et al., 2009; Dorey et al., 2020;Gomez et al., 2022).

Initially, CWCs may beneﬁt from higher temperatures,

through enhanced polyp activity, higher prey capture rates

(Chapron et al., 2021) and growth (Büscher, Form &

Riebesell, 2017; Büscher et al., 2022). Nevertheless, beyond

a certain temperature threshold (+4C), enhanced food

intake is no longer sufﬁcient to offset the metabolic energy

costs (Chapron et al., 2021) or prey capture decreases, leading

to decreased growth, tissue reserves, and eventually death

(Gomez et al., 2022). Furthermore, even small changes in

temperature affect the CWC microbiome, with potential

consequences for microbially assisted nutrient acquisition

and immune responses (Chapron et al., 2021).

Moreover, high atmospheric CO

concentrations lead to

ocean acidiﬁcation (Kleypas et al., 1999; Wolf-Gladrow

et al., 1999) and a projected decrease of 0.3 pH units in the

bathyal by 2100 (Sweetman et al., 2017). More acidic condi-

tions render calciﬁcation, i.e. the formation of calcium car-

bonate (aragonite) skeletons, more energetically costly

(Cohen & Holcomb, 2009). Due to the naturally low carbon-

ate (aragonite) saturation in their deep, cold habitat, CWCs

are particularly vulnerable to ocean acidiﬁcation (Orr

et al., 2005; Guinotte et al., 2006; Lunden, Georgian &

Cordes, 2013;Gomez et al., 2018). Nevertheless, CWCs, par-

ticularly some genotypes, are able to acclimatise and main-

tain skeletal growth under long-term exposure to

experimental acidiﬁcation (Form & Riebesell, 2012; Maier

et al., 2013; Hennige et al., 2014,2015; Movilla et al., 2014;

Büscher et al., 2017; Kurman et al., 2017; Gammon

et al., 2018). The metabolic stimulation by higher tempera-

tures may partially offset the negative impact of acidiﬁcation

on CWC growth up to a certain temperature and pH thresh-

old (Büscher et al., 2022). At several sites, CWCs (D. pertusum,

E. rostrata,G. dumosa,M. oculata,S. variabilis) even grow under

aragonite undersaturation (Thresher et al., 2011; Bostock

et al., 2015; Baco et al., 2017). To calcify under low pH, corals

may upregulate their internal pH through ion transport

(McCulloch et al., 2012a,b; Wall et al., 2015; Glazier

et al., 2020). The involved energetic cost, however, increases

by 10% per 0.1 pH unit decrease in seawater pH

(McCulloch et al., 2012b), hence, the ability of CWCs to

locally acclimatise or adapt to acidiﬁed conditions may

depend greatly on the respective food supply (Georgian

et al., 2016).

18 Sandra R. Maier and others

Other anthropogenic impacts additionally disbalance the

energy budget of CWCs, by increasing their energetic costs

to mitigate stress while at the same time decreasing their

prey-capture rates (Fig. 8A); these impacts include physical

abrasion and increased sedimentation through ﬁsheries and

mineral extraction (Fossa, Mortensen & Furevik, 2002;

Davies, Roberts & Hall-Spencer, 2007; Armstrong & van

den Hove, 2008; Huvenne et al., 2016), oxygen stress through

increasing deoxygenation of bottom waters (Dodds

et al., 2007; Sweetman et al., 2017; Hanz et al., 2019;

ROWTH

Fig. 8. Negative impacts of anthropogenic environmental change (in red) on (A) the energy budget of cold-water corals (CWCs) and

(B) CWC reef ecosystem functioning. OM, organic matter.

Cold-water coral reefs 19

Hebbeln et al., 2020), and pollution by oil spills (Weinnig

et al., 2020) and plastic (Chapron et al., 2018; Mouchi

et al., 2019).

In situ, CWCs already show signs of energetic shortfalls. In

seasonal periods of enhanced metabolic activity, possibly due

to reproductive tissue modiﬁcations, D. pertusum showed on

average ca. 70% lower linear skeletal extension rates com-

pared to other seasons (Maier et al., 2020a). Likewise, in years

of low downwelling/water-column mixing intensity, the spe-

cies showed on average ca. 80% lower linear skeletal exten-

sion rates compared to high-mixing years (Chapron

et al., 2020). Furthermore, corals at heavily trawled sites are

non-reproductive, possibly because their energy reserves

(and colony size) are too low to afford sexual reproduction

(Waller & Tyler, 2005). Altogether, global change is pre-

dicted to reduce the habitat suitable for CWCs by 79%

(Morato et al., 2020) and CWC reef biomass by 38% (Jones

et al., 2014) by 2100.

(2) Reduced reef functioning on ‘crumbling’reefs

On the ecosystem level, decreased coral growth on the one

hand, and increased erosion of the reef framework on the

other hand (Fig. 8B), threaten the reef carbonate budget

(Perry et al., 2013; Büscher et al., 2019). Under low pH,

CWC skeletons are more porous and form a less stable reef

framework (Hennige et al., 2015). Furthermore, ocean acidi-

ﬁcation accelerates chemical dissolution and bioerosion of

the calcium carbonate reef framework (Wisshak et al., 2012,

2014; Hennige et al., 2015). Altogether, this ‘coralporosis’

produces instable, ‘crumbling’reefs of reduced structural

complexity, and in case of aragonite undersaturation,

CWC ‘reefs’consisting primarily of live coral colonies with-

out a dead framework foundation (Hennige et al., 2020).

Reduced structural complexity will likely diminish CWC

reef biodiversity and ecosystem functioning (Fig. 8B), similar

to tropical coral reefs (Nelson, Kuempel & Altieri, 2016;

Sunday et al., 2016; Doo, Edmunds & Carpenter, 2019; Dove

et al., 2020). A ﬂat reef structure does not induce downward

transport of POM-rich surface water, leading to (further)

diminished food supply and retention (White et al., 2005;

Mienis et al., 2007; Soetaert et al., 2016). Reef sessile suspen-

sion feeders cannot attach to strongly degraded reef frame-

work and coral rubble (Mortensen & Fosså, 2006; Maier

et al., 2021). Furthermore, suspension feeders appear partic-

ularly sensitive to temperature increase, indicated by their

reduced abundance under episodic, interannual tempera-

ture highs at the Mingulay Reef (Kazanidis et al., 2021b). Loss

of structural complexity and suspension feeders on CWC

reefs will likely impair the mechanical and biological ‘reef ﬁl-

ter’and concomitantly food particle retention (Fig. 8B; see

Section IV). Reduced food availability and decreased biodi-

versity may restrain recycling pathways. For instance, lower

abundance of CWCs could result in lower production of

mucoid DOM, less recycling of DOM by the reef fauna,

and less production of detrital waste for detritivores –

i.e. an attenuated ‘suspension feeder (sponge) loop’

(Fig. 8B). Reduced resource availability might lead to a

further decrease of biodiversity (Fig. 8B), creating a detrimen-

tal feedback loop that jeopardises the stability of the reef

community (Worm & Duffy, 2003). In conclusion, theAnthro-

pocene climate may substantially damage the functioning of

CWC reef ecosystems, but unlike for tropical coral reefs

(Hughes et al., 2010), virtually nothing is known about their

resilience and potential phase shifts. In a similar way, global

change will likely affect other complex deep-sea ecosystems,

such as coral gardens and sponge grounds (Rossi et al., 2019).

(3) Conservation of cold-water coral reefs in the

Anthropocene

The vulnerability of CWC reefs and their importance as

ecosystem service providers (see Section I) has been recog-

nised by the United Nations (UN) Food and Agriculture

Organisation (FAO, 2009), declaring CWC reefs as vulner-

able marine ecosystems (VMEs), according to the United

Nations General Assembly (UNGA) resolution 61/105

(UNGA, 2007). VMEs require special protection,

e.g. through marine spatial planning with the designation

of marine protected areas (MPAs; United Nations, 2017).

Yet, effective marine spatial planning remains difﬁcult, due

to limited scientiﬁc knowledge on global CWC distribution,

lack of historical baseline data (Duran Muñoz & Sayago-

Gil, 2011; Kazanidis et al., 2020; Lim, Wheeler &

Conti, 2021), and scarce data on MPA effectiveness

(Huvenne et al., 2016). Some stressors are not constrained

by protected area boundaries, including oil, other pollutants

and impacts from global change; however protected areas

can provide resilience to global stressors by maintaining eco-

system function. Continued mapping and characterisation

of CWC habitats is critical, but we argue that our improved

understanding of the ‘cold-water coral reef paradox’should

also be incorporated into ecosystem assessment and conser-

vation efforts. Live coral cover has been used as a proxy

for CWC reef health (Flögel et al., 2014;Juvaet al., 2020),

yet differences in CWC cover may be natural and do not

necessarily provide information on whether a reef is new

or on the verge of disappearing (Hughes et al., 2010). An

integrative approach to assess the environmental status of

CWC reefs was presented by Kazanidis et al.(

2020), includ-

ing biodiversity indices, coral cover, ﬁsh biomass, signs of

anthropogenic impacts, etc., as proxies for reef status. Based

on Sections II–IV, we suggest complementing these ecosys-

tem descriptors by including (i) organic and inorganic C

budgets for (a) CWCs and (b) the reef ecosystem, to evaluate

reef growth versus erosion; and (ii) reef functional diversity

and food-web complexity, to judge ecosystem functioning

and resilience to changing oceanographic conditions. Future

research should create a framework to facilitate the assess-

ment of these ecosystem descriptors. For 1a, the energetic

status (energy budget) of CWCs at different reefs should be

regularly measured, e.g. their metabolic activity and tissue

stores (somatic and reproductive). In addition, these mea-

sures could be introduced into DEB models, to assess coral

20 Sandra R. Maier and others

growth under local and potentially changing environmental

conditions (e.g. temperature, food supply). Regarding 1b,

video transect annotations of CWC reefs can be combined

with predictive modelling to create reef-scale biomass, and

organic and inorganic C maps; newly developed machine-

learning algorithms will accelerate video annotations in the

future (De Clippele et al., 2021a). Regarding 2, future

research could develop a functional traits database for

reef-associated organisms (e.g. their feeding guild) plus

open-source code for simple implementation of food-web

models. This would allow evaluation of the trophodynamic

resilience of different CWC reefs without strong program-

ming skills. Based on these approaches, future research

may help to identify CWC reef ‘refugia’that are likely to

persist during future global change (Morato et al., 2020).

Spatial measures protecting networks of these refugia from,

e.g. bottom-trawling ﬁsheries, appear to be our best chance

to preserve CWC reefs and their function as diversity–

productivity hotspots in the deep sea.

VI. CONCLUSIONS

(1) Recent major advances allow us to approach the paradox

of how CWC reefs sustain high biodiversity, biomass and

metabolic activity in the food-limited deep sea. Suggested

answers to this paradox reveal key drivers of CWC reef distri-

bution that are required to achieve effective conservation

measures.

(2) Most reef-building CWC species occur in areas of

enhanced primary production with high seasonal ﬂuctua-

tions and under elevated current velocity (relative to global

averages), indicating that food production and supply are

important drivers of CWC reef distribution.

(3) Food supply on CWC reefs is not constantly low, but

highly dynamic. Within a couple of hours, food availability

can change from very low to very high, depending on the sea-

son, the prevailing hydrodynamic regime, and presence of

vertically migrating zooplankton.

(4) The best-studied reef-forming CWC species D. pertusum is

well adapted to these extreme temporal ﬂuctuations in food

availability, by (i) high capture rates of phytodetritus and zoo-

plankton, (ii) high resource ﬂexibility (DOM, bacterioplank-

ton, inorganic resources), (iii) investing in large tissue

reserves for reproduction, and (iv) synchronising activity with

(seasonal) ﬂuctuations in food availability.

(5) On the ecosystem level, CWC reefs sustain high meta-

bolic activity and biomass. They achieve this ﬁrstly by efﬁ-

cient retention of phytodetritus, zooplankton and

bacterioplankton in the ‘reef ﬁlter’, a combination of a

mechanical ﬁlter provided by the structurally complex,

porous reef framework and a biological ﬁlter consisting of

diverse, abundant suspension-feeding epifauna. Secondly,

diverse trophic interactions and material recycling facilitate

optimal resource utilisation and exploitation of additional

food sources, such as dissolved organic and inorganic matter.

(6) Climate change, ocean acidiﬁcation, ﬁsheries, mining,

and pollution impact reef functioning in various ways,

e.g. by reducing organic matter supply, increasing the ani-

mals’energy demands, and dissolving the carbonate reef

framework, thereby decreasing structural and biological

diversity and ecosystem functioning. Research has only

started to reveal the vast complexity, drivers and functioning

of CWC reefs, but it is crucial to continue this path to facili-

tate knowledge-based habitat management for sustaining

these diversity–productivity hotspots in the future ocean.

VII. ACKNOWLEDGEMENTS

We would like to acknowledge funding by the Netherlands

Organisation for Scientiﬁc Research (VIDI grant

864.13.007 to D. v. O. and S. R. M., VIDI grant

016.161.360 to F. M.), funding by the European Union’s

Horizon 2020 Research and Innovation Programme

(ATLAS project, grant agreement no. 678760 to D. v. O.

and E. d. F.; iAtlantic project, grant agreement no. 818123

to L. H. d. C.), funding by the Greenland Research Council

and the Greenland Self Rule Governments funding for

science support to S. R. M., and funding by the National

Oceanic and Atmospheric Administration (NOAA), by the

Bureau of Ocean Energy and Management (BOEM), and

by the United States Geological Survey (USGS) to S. B.

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IX. SUPPORTING INFORMATION

Additional supporting information may be found online in

the Supporting Information section at the end of the article.

Appendix S1. Detailed methods.

Appendix S2. Results of statistical analysis of comparisons

of primary productivity annual average and annual range,

and current velocity annual average at cold-water coral sites

with the global mean.

Appendix S3. Respiration, organic matter release, food

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Table S1. Flux of particulate organic carbon (POC_ﬂux)

measured by sediment trap at the indicated sites, depth and

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(Received 21 September 2022; revised 26 April 2023; accepted 1 May 2023 )

28 Sandra R. Maier and others

Resemblance of the global depth distribution of internal-tide generation and cold-water coral occurrences

Article

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Apr 2024
OCEAN SCI

Internal tides are known to be an important source of mixing in the oceans, especially in the bottom boundary layer. The depth of internal-tide generation therefore seems important for benthic life and the formation of cold-water coral mounds, but internal-tide conversion is generally investigated in a depth-integrated sense. Using both idealized and realistic simulations on continental slopes, we found that the depth of internal-tide generation increases with increasing slope steepness and decreases with intensified shallow stratification. The depth of internal-tide generation also shows a typical latitudinal dependency related to Coriolis effects. Using a global database of cold-water corals, we found that, especially in Northern Hemisphere autumn and winter, the global depth pattern of internal-tide generation correlates (rautumn = 0.70, rwinter = 0.65, p < 0.01) with that of cold-water corals: shallowest near the poles and deepest around the Equator, with a decrease in depth around 25° S and N, and shallower north of the Equator than south. We further found that cold-water corals are situated significantly more often on topography that is steeper than the internal-tide beam (i.e. where supercritical reflection of internal tides occurs) than would be expected from a random distribution: in our study, in 66.9 % of all cases, cold-water corals occurred on a topography that is supercritical to the M2 tide whereas globally only 9.4 % of all topography is supercritical. Our findings underline internal-tide generation and the occurrence of supercritical reflection of internal tides as globally important for cold-water coral growth. The energetic dynamics associated with internal-tide generation and the supercritical reflection of internal tides likely increase the food supply towards the reefs in food-limited winter months. With climate change, stratification is expected to increase. Based on our results, this would decrease the depth of internal-tide generation, possibly creating new suitable habitat for cold-water corals shallower on continental slopes.

Quantifying the δ 15 N trophic offset in a cold-water scleractinian coral (CWC): implications for the CWC diet and coral δ 15 N as a marine N cycle proxy

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Mar 2024
BG

The nitrogen (N) isotope composition (δ15N) of cold-water corals is a promising proxy for reconstructing past ocean N cycling, as a strong correlation was found between the δ15N of the organic nitrogen preserved in coral skeletons and the δ15N of particulate organic matter exported from the surface ocean. However, a large offset of 8 ‰–9 ‰ between the δ15N recorded by the coral and that of exported particulate organic matter remains unexplained. The 8 ‰–9 ‰ offset may signal a higher trophic level of coral dietary sources, an unusually large trophic isotope effect or a biosynthetic δ15N offset between the coral's soft tissue and skeletal organic matter, or some combinations of these factors. To understand the origin of the offset and further validate the proxy, we investigated the trophic ecology of the asymbiotic scleractinian cold-water coral Balanophyllia elegans, both in a laboratory setting and in its natural habitat. A long-term incubation experiment of B. elegans fed on an isotopically controlled diet yielded a canonical trophic isotope effect of 3.0 ± 0.1 ‰ between coral soft tissue and the Artemia prey. The trophic isotope effect was not detectably influenced by sustained food limitation. A long N turnover of coral soft tissue, expressed as an e-folding time, of 291 ± 15 d in the well-fed incubations indicates that coral skeleton δ15N is not likely to track subannual (e.g., seasonal) variability in diet δ15N. Specimens of B. elegans from the subtidal zone near San Juan Channel (WA, USA) revealed a modest difference of 1.2 ± 0.6 ‰ between soft tissue and skeletal δ15N. The δ15N of the coral soft tissue was 12.0 ± 0.6 ‰, which was ∼6 ‰ higher than that of suspended organic material that was comprised dominantly of phytoplankton – suggesting that phytoplankton is not the primary component of B. elegans' diet. An analysis of size-fractionated net tow material suggests that B. elegans fed predominantly on a size class of zooplankton ≥500 µm, implicating a two-level trophic transfer between phytoplankton material and coral tissue. These results point to a feeding strategy that may result in an influence of the regional food web structure on the cold-water coral δ15N. This factor should be taken into consideration when applying the proxy to paleo-oceanographic studies of ocean N cycling.

Development and physical characteristics of the Irish shelf-edge Macnas Mounds, Porcupine Seabight, NE Atlantic

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Apr 2024

Modern cold-water corals (CWCs) occur in a wide range of water depths, with Desmophyllum pertusum being one of the most common species. Pleistocene, Holocene, and modern coral mound formation by living CWC reefs have previously been described in the Porcupine Seabight from water depths greater than 700 m in the vicinity of the transitional zone between the Eastern North Atlantic Water and Mediterranean Outflow Water. Here we document occurrence of fossil corals retrieved from two cores at 370 m depth in the Macnas Mounds, a relatively shallow occurrence for mounds on the Irish shelf-edge. Both cores feature D. pertusum restricted to the upper two metres, immediately overlying an erosive surface and a coeval major down-core change in grain size from sand to mud. Radiocarbon dating of coral specimens indicates the CWC mounds initiated 7.82 Cal ky BP. Our study unequivocally documents the existence of Holocene shelf-edge coral mounds in the eastern Porcupine Seabight and highlights the possibility of other occurrences of CWCs in similar settings elsewhere in the northeast Atlantic. Given that no living CWCs were encountered in the study area, we suggest that the area previously experienced more favourable conditions for CWC mound initiation and development along the shelf-edge margin, possibly due to differing conditions in the European Slope Current which flows northward along the continental slope from south of the Porcupine Bank to the Faroe-Shetland Channel. Graphical Abstract

Cold-water coral energy reserves and calcification in contrasting fjord environments

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Mar 2024

The relationship between energy reserves of cold-water corals (CWCs) and their physiological performance remains largely unknown. In addition, it is poorly understood how the energy allocation to different metabolic processes might change with projected decreasing food supply to the deep sea in the future. This study explores the temporal and spatial variations of total energy reserves (proteins, carbohydrates and lipids) of the CWC Desmophyllum dianthus and their correlation with its calcification rate. We took advantage of distinct horizontal and vertical physico-chemical gradients in Comau Fjord (Chile) and examined the changes in energy reserves over one year in an in situ reciprocal transplantation experiment (20 m vs. 300 m and fjord head vs. mouth). Total energy reserves correlated positively with calcification rates. The fast-growing deep corals had higher and less variable energy reserves, while the slower-growing shallow corals showed pronounced seasonal changes in energy reserves. Novel deep corals (transplanted from shallow) were able to quickly increase both their calcification rates and energy reserves to similar levels as native deep corals. Our study shows the importance of energy reserves in sustaining CWC growth in spite of aragonite undersaturated conditions (deep corals) in the present, and potentially also future ocean.

Heterotrophy in marine animal forests in an era of climate change

Article

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BIOL REV

Marine animal forests (MAFs) are benthic ecosystems characterised by biogenic three-dimensional structures formed by suspension feeders such as corals, gorgonians, sponges and bivalves. They comprise highly diversified communities among the most productive in the world's oceans. However, MAFs are in decline due to global and local stressors that threaten the survival and growth of their foundational species and associated biodiversity. Innovative and scal-able interventions are needed to address the degradation of MAFs and increase their resilience under global change. Surprisingly , few studies have considered trophic interactions and heterotrophic feeding of MAF suspension feeders as an integral component of MAF conservation. Yet, trophic interactions are important for nutrient cycling, energy flow within the food web, biodiversity, carbon sequestration, and MAF stability. This comprehensive review describes trophic interactions at all levels of ecological organisation in tropical, temperate, and cold-water MAFs. It examines the strengths and weaknesses of available tools for estimating the heterotrophic capacities of the foundational species in MAFs. It then discusses the threats that climate change poses to heterotrophic processes. Finally, it presents strategies for improving trophic interactions and heterotrophy, which can help to maintain the health and resilience of MAFs.

Tiger reefs: Self‐organized regular patterns in deep‐sea cold‐water coral reefs

Article

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Oct 2023

Complexity theory predicts that self‐organized, regularly patterned ecosystems store more biomass and are more resilient than spatially uniform systems. Self‐organized ecosystems are well‐known from the terrestrial realm, with “tiger bushes” being the archetypical example and mussel beds and tropical coral reefs the marine examples. We here identify regular spatial patterns in cold‐water coral reefs (nicknamed “tiger reefs”) from video transects and argue that these are likely the result of self‐organization. We used variograms and Lomb–Scargle analysis of seven annotated video transects to analyze spatial patterns in live coral and dead coral (i.e., skeletal remains) cover at the Logachev coral mound province (NE Atlantic Ocean) and found regular spatial patterns with length scales between 62 and 523 m in live and dead coral distribution along these transects that point to self‐organization of cold‐water coral reefs. Self‐organization theory shows that self‐organized ecosystems can withstand large environmental changes by adjusting their spatial configuration. We found indications that cold‐water corals can similarly adjust their spatial configuration, possibly providing resilience in the face of climate change. Dead coral framework remains in the environment for extended periods of time, providing a template for spatial patterns that facilitates live coral recovery. The notion of regular spatial patterns in cold‐water coral reefs is interesting for cold‐water coral restoration, as transplantation will be more successful when it follows the patterns that are naturally present. This finding also underlines that anthropogenic effects such as ocean acidification and bottom trawling that destroy the dead coral template undermine cold‐water coral resilience. Differences in the pattern periodicities of live and dead coral cover further present an interesting new angle to investigate past and present environmental conditions in cold‐water coral reefs.

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Article

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The export of particulate organic matter (POM) to deep-sea is crucial for deep-sea ecosystems. However, in situ measurements of large-scale POM export flux are scarce in the tropical and subtropical western Pacific, leading to reliance on biogeochemical models or sediment trap data from a few stations. To address this gap, the underwater vision profiler was used to measure particulate density and to calculate particulate organic carbon (POC) fluxes along the Kyushu–Palau Ridge (KPR) in the Philippine Sea. The results revealed a significant latitudinal gradient of POC fluxes: 37% of the POC output from 200 m depth was preserved to 2000 m in the Western Pacific Warm Pool and up to 51% was preserved in the North Pacific Subtropical Gyre. The near-bottom POC fluxes north of 25°N (1.64 ± 0.80 mg m-² d-¹) were significantly higher than the average near-bottom value of the entire transect (0.60 ± 0.43 mg m-² d-¹). Multiple linear regression analysis showed that the chlorophyll concentration had a significant positive effect on the POC fluxes at all depths, except near the bottom, while local factors such as mesoscale eddies and the interaction effect between the topography and current velocity only had significant effects on the POC fluxes at depths of greater than 2000 m. Particle size spectrum analysis revealed that particles ranging from 64 to 323 μm in size exerted a dominant influence on the increase in the POC fluxes in the near-bottom layers situated north of 25°N. These findings indicated that the spatial heterogeneity of POC fluxes in the western Pacific was governed not only by upper ocean primary productivity but also by mesoscale processes, current velocity, and topography. These results provided crucial fundamental information for cartography of the distribution and simulation of the dynamics of deep-sea organisms along the KPR in the Philippine Sea.

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Article

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Feb 2024
BG

Framework-forming cold-water corals (CWCs) are ecosystem engineers that build mounds in the deep sea that can be up to several hundred metres high. The effect of the presence of cold-water coral mounds on their surroundings is typically difficult to separate from environmental factors that are not affected by the mounds. We investigated the environmental control on and the importance of ecosystem engineering for cold-water coral reefs using annotated video transect data, spatial variables (MEMs), and hydrodynamic model outputs in a redundancy analysis and with variance partitioning. Using available hydrodynamic simulations with cold-water coral mounds and simulations where the mounds were artificially removed, we investigated the effect of coral mound ecosystem engineering on the spatial configuration of reef habitat and discriminated which environmental factors are and which are not affected by the mounds. We find that downward velocities in winter, related to non-engineered environmental factors, e.g. deep winter mixing and dense-water cascading, cause substantial differences in reef cover at the broadest spatial scale (20–30 km). Such hydrodynamic processes that stimulate the food supply towards the corals in winter seem more important for the reefs than cold-water coral mound engineering or similar hydrodynamic processes in summer. While the ecosystem-engineering effect of cold-water corals is frequently discussed, our results also highlight the importance of non-engineered environmental processes. We further find that, due to the interaction between the coral mound and the water flow, different hydrodynamic zones are found on coral mounds that likely determine the typical benthic zonations of coral rubble at the mound foot, the dead coral framework on the mound flanks, and the living corals near the summit. Moreover, we suggest that a so-called Massenerhebung effect (well known for terrestrial mountains) exists, meaning that benthic zonation depends on the location of the mound rather than on the height above the seafloor or water depth. Our finding that ecosystem engineering determines the configuration of benthic habitats on cold-water coral mounds implies that cold-water corals cannot grow at deeper depths on the mounds to avoid the adverse effects of climate change.

Cold-water coral framework architecture is selectively shaped by bottom current flow

Article

Full-text available

Feb 2023
CORAL REEFS

The three-dimensional (3D) structure of habitat-forming corals has profound impacts on reef ecosystem processes. Elucidating coral structural responses to the environment is therefore crucial to understand changes in these ecosystems. However, little is known of how environmental factors shape coral structure in deep and dark waters, where cold-water coral (CWC) reefs thrive. Here, we attempt to infer the influence of current flow on CWC framework architecture, using 3D scanning to quantify colony shape traits (volume compactness and surface complexity) in the reef-building CWC Desmophyllum pertusum from adjacent fjord and offshore habitats with contrasting flow regimes. We find substantial architectural variability both between and within habitats. We show that corals are generally more compact in the fjord habitat, reflecting the prevailing higher current speeds, although differences in volume compactness between fjord and offshore corals are more subtle when comparing the fjord with the more exposed side of the offshore setting, probably due to locally intensified currents. Conversely, we observe no clear disparity in coral surface complexity between habitats (despite its positive correlation with volume compactness), suggesting it is not affected by current speed. Unlike volume compactness, surface complexity is similarly variable within a single colony as it is between colonies within the same habitat or between habitats and is therefore perhaps more dependent than volume compactness on microenvironmental conditions. These findings suggest a highly plastic, trait-specific and functionally relevant structural response of CWCs to current flow and underscore the importance of multiple concurrent sources of hydrodynamic forcing on CWC growth.

Revisionary systematics of Octocorallia (Cnidaria: Anthozoa) guided by phylogenomics

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Full-text available

Oct 2022

The anthozoan sub-class Octocorallia includes over 3500 nominal species of soft corals and gorgonian sea fans, many of which serve as critical foundation species in benthic marine ecosystems in shallow waters to the deep sea. Despite their familiarity and ecological impor-tance, the diversity and taxonomy of octocorals remain poorly known. All of the orders, subordinal groups, and a majority of families have been recognized to be poly- or paraphyletic, but poor resolution of the deeper nodes in mitochondrial or single-locus nuclear gene trees have hindered formal revision of the higher-level taxonomy of the group. We used sequence data from target-capture of 739 ultraconserved and exon loci to reconstruct a fully resolved phylogeny for 185 octocoral taxa represent-ing 55 of 63 currently recognized families. We use this phylogeny, sup-plemented with a gene tree for mitochondrial mtMutS for an additional 107 taxa, to guide a revision of the families and orders of Octocorallia. We (1) elevate the anthozoan sub-classes Octocorallia and Hexacorallia to the rank of Class; (2) replace the three currently recognized orders of Octocorallia (Alcyonacea, Pennatulacea, Helioporacea) with two new orders reflecting reciprocally monophyletic major clades; and (3) revise all families with the exception of the 15 recognized families of sea pens, which we accommodate within a new superfamily. The revised classifi-cation of Octocorallia thus comprises 79 families, including 18 that are newly described and three that have been reinstated or elevated in rank. In addition, two new genera are described and another three reinstated. We leave the family assignment of 46 of 413 genera as incertae sedis until further molecular or morphological data can be obtained to confirm their phylogenetic affinities.

Cold‐water coral ecosystems under future ocean change: Live coral performance vs. framework dissolution and bioerosion

Article

Full-text available

Sep 2022

Physiological sensitivity of cold‐water corals to ocean change is far less understood than of tropical corals and very little is known about the impacts of ocean acidification and warming on degradative processes of dead coral framework. In a 13‐month laboratory experiment, we examined the interactive effects of gradually increasing temperature and pCO2 levels on survival, growth, and respiration of two prominent color morphotypes (colormorphs) of the framework‐forming cold‐water coral Lophelia pertusa, as well as bioerosion and dissolution of dead framework. Calcification rates tended to increase with warming, showing temperature optima at ~ 14°C (white colormorph) and 10–12°C (orange colormorph) and decreased with increasing pCO2. Net dissolution occurred at aragonite undersaturation (ΩAr < 1) at ~ 1000 μatm pCO2. Under combined warming and acidification, the negative effects of acidification on growth were initially mitigated, but at ~ 1600 μatm dissolution prevailed. Respiration rates increased with warming, more strongly in orange corals, while acidification slightly suppressed respiration. Calcification and respiration rates as well as polyp mortality were consistently higher in orange corals. Mortality increased considerably at 14–15°C in both colormorphs. Bioerosion/dissolution of dead framework was not affected by warming alone but was significantly enhanced by acidification. While live corals may cope with intermediate levels of elevated pCO2 and temperature, long‐term impacts beyond levels projected for the end of this century will likely lead to skeletal dissolution and increased mortality. Our findings further suggest that acidification causes accelerated degradation of dead framework even at aragonite saturated conditions, which will eventually compromise the structural integrity of cold‐water coral reefs.

Hydrography and food distribution during a tidal cycle above a cold-water coral mound

Article

Full-text available

Aug 2022
DEEP-SEA RES PT I

Cold-water corals (CWCs) are important ecosystem engineers in the deep sea that provide habitat for numerous species and can form large coral mounds. These mounds influence surrounding currents and induce distinct hydrodynamic features, such as internal waves and episodic downwelling events that accelerate transport of organic matter towards the mounds, supplying the corals with food. To date, research on organic matter distribution at coral mounds has focussed either on seasonal timescales or has provided single point snapshots. Data on food distribution at the timescale of a diurnal tidal cycle is currently limited. Here, we integrate physical, biogeochemical, and biological data throughout the water column and along a transect on the south-eastern slope of Rockall Bank, Northeast Atlantic Ocean. This transect consisted of 24-hour sampling stations at four locations: Bank, Upper slope, Lower slope, and the Oreo coral mound. We investigated how the organic matter distribution in the water column along the transect is affected by tidal activity. Repeated CTD casts indicated that the water column above Oreo mound was more dynamic than above other stations in multiple ways. First, the bottom water showed high variability in physical parameters and nutrient concentrations, possibly due to the interaction of the tide with the mound topography. Second, in the surface water a diurnal tidal wave replenished nutrients in the photic zone, supporting new primary production. Third, above the coral mound an internal wave (200 m amplitude) was recorded at 400 m depth after the turning of the barotropic tide. After this wave passed, high quality organic matter was recorded in bottom waters on the mound coinciding with shallow water physical characteristics such as high oxygen concentration and high temperature. Trophic markers in the benthic community suggest feeding on a variety of food sources, including phytodetritus and zooplankton. We suggest that there are three transport mechanisms that supply food to the CWC ecosystem. First, small phytodetritus particles are transported downwards to the seafloor by advection from internal waves, supplying high quality organic matter to the CWC reef community. Second, the shoaling of deeper nutrient-rich water into the surface water layer above the coral mound could stimulate diatom growth, which form fast-sinking aggregates. Third, evidence from lipid analysis indicates that zooplankton faecal pellets also enhance supply of organic matter to the reef communities. This study is the first to report organic matter quality and composition over a tidal cycle at a coral mound and provides evidence that fresh high-quality organic matter is transported towards a coral reef during a tidal cycle.

The important role of sponges in carbon and nitrogen cycling in a deep‐sea biological hotspot

Article

Full-text available

Jul 2022
FUNCT ECOL

Deep‐sea sponge grounds are hotspots of biodiversity, harbouring thriving ecosystems in the otherwise barren deep sea. It remains unknown how these sponge grounds survive in this food‐limited environment. Here, we unravel how sponges and their associated fauna sustain themselves by identifying their food sources and food‐web interactions using bulk and compound‐specific stable isotope analysis of amino and fatty acids. We found that sponges with a high microbial abundance had an isotopic composition resembling organisms at the base of the food web, suggesting that they are able to use dissolved resources that are generally inaccessible to animals. In contrast, low microbial abundance sponges had a bulk isotopic composition that resembles a predator at the top of a food web, which appears to be the result of very efficient recycling pathways that are so far unknown. The compound‐specific‐isotope analysis, however, positioned low‐microbial abundance sponges with other filter‐feeding fauna. Furthermore, fatty‐acid analysis confirmed transfer of sponge‐derived organic material to the otherwise food‐limited associated fauna. Through this subsidy, sponges are key to the sustenance of thriving deep‐sea ecosystems and might have, due to their ubiquitous abundance, a global impact on biogeochemical cycles. Read the free Plain Language Summary for this article on the Journal blog.

Major environmental drivers determining life and death of cold-water corals through time

Article

Full-text available

May 2022
PLOS BIOL

Cold-water corals (CWCs) are the engineers of complex ecosystems forming unique biodiversity hotspots in the deep sea. They are expected to suffer dramatically from future environmental changes in the oceans such as ocean warming, food depletion, deoxygenation, and acidification. However, over the last decades of intense deep-sea research, no extinction event of a CWC ecosystem is documented, leaving quite some uncertainty on their sensitivity to these environmental parameters. Paleoceanographic reconstructions offer the opportunity to align the on- and offsets of CWC proliferation to environmental parameters. Here, we present the synthesis of 6 case studies from the North Atlantic Ocean and the Mediterranean Sea, revealing that food supply controlled by export production and turbulent hydrodynamics at the seabed exerted the strongest impact on coral vitality during the past 20,000 years, whereas locally low oxygen concentrations in the bottom water can act as an additional relevant stressor. The fate of CWCs in a changing ocean will largely depend on how these oceanographic processes will be modulated. Future ocean deoxygenation may be compensated regionally where the food delivery and food quality are optimal.

Living on the edge: environmental variability of a shallow late Holocene cold-water coral mound

Article

Full-text available

Aug 2022
CORAL REEFS

Similar to their tropical counterparts, cold-water corals (CWCs) are able to build large three-dimensional reef structures. These unique ecosystems are at risk due to ongoing climate change. In particular, ocean warming, ocean acidification and changes in the hydrological cycle may jeopardize the existence of CWCs. In order to predict how CWCs and their reefs or mounds will develop in the near future one important strategy is to study past fossil CWC mounds and especially shallow CWC ecosystems as they experience a greater environmental variability compared to other deep-water CWC ecosystems. We present results from a CWC mound off southern Norway. A sediment core drilled from this relatively shallow (~ 100 m) CWC mound exposes in full detail hydrographical changes during the late Holocene, which were crucial for mound build-up. We applied computed tomography, 230Th/U dating, and foraminiferal geochemical proxy reconstructions of bottom-water-temperature (Mg/Ca-based BWT), δ18O for seawater density, and the combination of both to infer salinity changes. Our results demonstrate that the CWC mound formed in the late Holocene between 4 kiloannum (ka) and 1.5 ka with an average aggradation rate of 104 cm/kiloyears (kyr), which is significantly lower than other Holocene Norwegian mounds. The reconstructed BWTMg/Ca and seawater density exhibit large variations throughout the entire period of mound formation, but are strikingly similar to modern in situ observations in the nearby Tisler Reef. We argue that BWT does not exert a primary control on CWC mound formation. Instead, strong salinity and seawater density variation throughout the entire mound sequence appears to be controlled by the interplay between the Atlantic Water (AW) inflow and the overlying, outflowing Baltic-Sea water. CWC growth and mound formation in the NE Skagerrak was supported by strong current flow, oxygen replenishment, the presence of a strong boundary layer and larval dispersal through the AW, but possibly inhibited by the influence of fresh Baltic Water during the late Holocene. Our study therefore highlights that modern shallow Norwegian CWC reefs may be particularly endangered due to changes in water-column stratification associated with increasing net precipitation caused by climate change. Supplementary information: The online version contains supplementary material available at 10.1007/s00338-022-02249-4.

Identification of tolerance levels on the cold-water coral Desmophyllum pertusum (Lophelia pertusa) from realistic exposure conditions to suspended bentonite, barite and drill cutting particles

Article

Full-text available

Feb 2022
PLOS ONE

Cold-water coral (CWC) reefs are numerous and widespread along the Norwegian continental shelf where oil and gas industry operate. Uncertainties exist regarding their impacts from operational discharges to drilling. Effect thresholds obtained from near-realistic exposure of suspended particle concentrations for use in coral risk modeling are particularly needed. Here, nubbins of Desmophyllum pertusum ( Lophelia pertusa ) were exposed shortly (5 days, 4h repeated pulses) to suspended particles (bentonite BE; barite BA, and drill cuttings DC) in the range of ~ 4 to ~ 60 mg.l ⁻¹ (actual concentration). Physiological responses (respiration rate, growth rate, mucus-related particulate organic carbon OC and particulate organic nitrogen ON) and polyp mortality were then measured 2 and 6 weeks post-exposure to assess long-term effects. Respiration and growth rates were not significantly different in any of the treatments tested compared to control. OC production was not affected in any treatment, but a significant increase of OC:ON in mucus produced by BE-exposed (23 and 48 mg.l ⁻¹ ) corals was revealed 2 weeks after exposure. Polyp mortality increased significantly at the two highest DC doses (19 and 49 mg.l ⁻¹ ) 2 and 6 weeks post-exposure but no significant difference was observed in any of the other treatments compared to the control. These findings are adding new knowledge on coral resilience to short realistic exposure of suspended drill particles and indicate overall a risk for long-term effects at a threshold of ~20 mg.l ⁻¹ .

Suspension feeders: diversity, principles of particle separation and biomimetic potential

Article

Full-text available

Jan 2022
J R SOC INTERFACE

Suspension feeders (SFs) evolved a high diversity of mechanisms, sometimes with remarkably convergent morphologies, to retain plankton, detritus and man-made particles with particle sizes ranging from less than 1 µm to several centimetres. Based on an extensive literature review, also including the physical and technical principles of solid-liquid separation, we developed a set of 18 ecological and technical parameters to review 35 taxa of suspension-feeding Metazoa covering the diversity of morphological and functional principles. This includes passive SFs, such as gorgonians or crinoids that use the ambient flow to encounter particles, and sponges, bivalves or baleen whales, which actively create a feeding current. Separation media can be flat or funnel-shaped, built externally such as the filter houses in larvaceans, or internally, like the pleated gills in bivalves. Most SFs feed in the intermediate flow region of Reynolds number 1-50 and have cleaning mechanisms that allow for continuous feeding. Comparison of structure-function patterns in SFs to current filtration technologies highlights potential solutions to common technical design challenges, such as mucus nets which increase particle adhesion in ascidians, vanes which reduce pressure losses in whale sharks and changing mesh sizes in the flamingo beak which allow quick adaptation to particle sizes.

Natural variability in seawater temperature compromises the metabolic performance of a reef-forming cold-water coral with implications for vulnerability to ongoing global change

Article

May 2022

Seawater temperature is one of the main variables that determines cold-water coral distribution worldwide. As part of an initiative to explore new areas of deep-sea habitats along the Southeast United States (SEUS) continental margin, a series of expeditions were carried out as part of the Deep-Sea Exploration to Advance Research on Corals/Canyons/Cold seeps (DEEP SEARCH) project. During these explorations, a cold-water coral reef complex composed mainly of Lophelia pertusa was located off the coast of South Carolina at 650–850 m depth. In this geographic area the species normally has a thermal tolerance between 6 and 12 °C with the capacity to form extensive calcium carbonate structures, thus creating complex habitat for a variety of associated species. Owing to the paucity of these structures and the unusual environmental conditions of this geographic area, with regular arrival of warm surface waters from the Gulf Stream, the main aim of this study was to understand the physiological response of L. pertusa to the variation in extreme temperature events in this region. Short-term experiments simulated the rate of temperature increase from the ambient temperature (8 °C) to the environmental maximum (14 °C) (heat-wave treatment). We found that temperature had a significant effect on the metabolic functions through an increase in respiration (0.108 to 0.247 µmol O2 g−1DW h−1) and excretion rates (0.002 to 0.011 µmol NH3 g−1DW h−1) at 14 °C. Oxygen to Nitrogen ratios (O:N) also showed an effect of temperature where corals switched from lipid-dominated toward a mix of lipid-protein and protein-dominated catabolism. To further characterize the metabolic response, feeding assays (capture rate of Artemia) were performed at the same temperature range with an overall three-fold decrease in capture rates under 14 °C compared to ambient temperature, thus increasing the probability of temperature-induced metabolic stress. Our results suggest that temperature variations affect the metabolic response of cold-water corals, particularly along the SEUS continental margin. Since the incursion of warm surface water to deeper zones is predicted to increase in frequency and duration due to climate change, L. pertusa may be implicated negatively, followed by ecological consequences for the survival and functionality for the ecosystem it supports.

On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

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