Abstract
Cold-water coral (CWC) reefs of the Angolan margin (SE Atlantic) are dominated by Desmophyllum pertusum and support a diverse community of associated fauna, despite hypoxic conditions. In this study, we use carbon and nitrogen stable isotope analyses (δ13C and δ15N) to decipher the trophic network of this relatively unknown CWC province. Although fresh phytodetritus is available to the reef, δ15N signatures indicate that CWCs (12.90 ± 1.00 ‰) sit two trophic levels above Suspended Particulate Organic Matter (SPOM) (4.23 ± 1.64 ‰) suggesting that CWCs are highly reliant on an intermediate food source, which may be zooplankton. Echinoderms and the polychaete Eunice norvegica occupy the same trophic guild, with high δ13C signatures (-14.00 ± 1.08 ‰) pointing to a predatory feeding behavior on CWCs and sponges, although detrital feeding on 13C enriched particles might also be important for this group. Sponges presented the highest δ15N values (20.20 ± 1.87 ‰), which could be due to the role of the sponge holobiont and bacterial food in driving intense nitrogen cycling processes in sponges’ tissue, helping to cope with the hypoxic conditions of the reef. Our study provides first insights to understand trophic interactions of CWC reefs under low-oxygen conditions.
Similar content being viewed by others
Introduction
Cold-water corals (CWCs) are heterotrophic cnidarians with an opportunistic suspension-feeding behavior1. In the food-limited deep sea, carbon processing in CWC reefs is higher compared to other adjacent habitats2,3 and trophic interactions are one of the processes contributing to the transfer and cycling of organic carbon between different functional groups within the reef2. Topography-enhanced hydrodynamics4,5,6,7 and vertical downwelling bringing surface waters to the deep8 are some of the mechanisms responsible for the enhanced transport of organic carbon to CWC reefs, driving CWC occurrence and distribution9,10,11.
The CWC Desmophyllum pertusum, also known as Lophelia pertusa12, forms biogenic frameworks with three-dimensional complexity13,14 representing a model of ecosystem engineering in the deep sea15. As for other framework-forming CWCs, D. pertusum reefs increase the local biodiversity of associated fauna16,17,18,19,20 by (i) providing a complex habitat with multiple ecological niches in areas of enhanced hydrodynamics favoring increased food supply21,22 and (ii) by locally reducing flow velocity and turbulence in the shadowed central zones of the reef improving food capture23,24 and the settlement of larvae23.
Thriving CWC reefs dominated by D. pertusum25, with the presence of Madrepora oculata26, have recently been found between 331 and 473 m water depth along the Angolan margin (SE Atlantic), coinciding with the center of the local oxygen minimum zone (OMZ). The discovery of the Angolan D. pertusum reefs challenged some of the previously assumed ecological requirements for the species27,28, given that CWCs were found in very low oxygen concentrations (0.5 to 1.3 mL L−1) and relatively high temperatures (6.8 to 14.2 °C)11,25,26. Despite the hypoxic conditions, the Angolan CWC reefs are prosperous and harbor a community of associated mega- and macrofauna, mainly composed of sponges, octocorals, and antipatharians29,30. Most studies on the trophic ecology of CWCs are available for communities occurring in normoxic conditions in the Mediterranean Sea31,32,33 and in the North Atlantic Ocean34,35,36,37,38, with scarce information for other deep-sea regions. To date, no trophic studies have been conducted in the recently discovered reefs of Angola.
Previous works showed that D. pertusum is a passive suspension-feeder, capable of feeding on different food sources, including dissolved organic matter (DOM)39,40, particulate organic matter (POM) in the form of phytodetritus from surface primary production37,41 and zooplankton31,34,42,43,44,45. In the Angolan CWC reefs, high-quality and abundant organic matter (OM) resulting from a productive upwelling system46 is available to benthic communities11. This abundant food supply could be a key mechanism for CWC survival under the Angolan OMZ11,47,48,49. A recent study by Gori et al.50, showed that D. pertusum in Angola can maintain high respiration rates under deoxygenation, suggesting acclimation and local adaptation of the species to the environmental conditions of the reefs. Some of the proposed adaptations of benthic organisms to hypoxia might include changes in body size and shape47,49, changes in energetic metabolic pathways49,50 as well as symbiotic associations with anoxic-bearing bacteria51,52,53. As far as we know, the effect of OMZs in the trophic ecology of CWCs and associated fauna has not yet been described. However, previous studies of trophic webs in OMZs showed the importance of microbe-mediated trophic processes54,55 in delivering OM to benthic organisms under low-oxygen conditions56, in particular, through the role of nitrifying and denitrifying bacteria55,57. Therefore, investigating the trophic interactions in the Angolan CWC reefs could provide new understanding of the food sources available to these communities, and how CWC reef trophic webs in OMZs might differ from those in more oxygenated regions.
Because of their remoteness and therefore the difficulty to obtain samples or conduct in situ experiments, disentangling energy flows within CWC ecosystems is challenging; nonetheless, different methodologies may allow to overcome the inherent difficulties. Gut content analysis is a widely used technique to decipher the diet of both terrestrial and marine organisms and has also been used for deep-sea animals58,59. However, data on the gastrovascular content of CWCs are very rare60 because of the complications in identifying preys due to the small size of the food particles61 and the difficulties in assessing the gut content by dissection of the corals’ polyps (in particular the ones from scleractinian corals). In situ detection of feeding interactions is possible through visual observations62,63, but such interactions are not easily captured on camera, and a large amount of data, over a large temporal scale, is needed. For these reasons, carbon (δ13C) and nitrogen (δ15N) stable isotope analyses have become the most widely used tools to investigate the trophic structures of deep-sea communities64,65,66,67,68,69,70. Stable isotope signals do not decay over time, thus integrating long-term diets and giving information on the dietary choices of an organism over a wide temporal range (from days to months, depending on the tissue turnover)71. In a standard food web, δ15N increases in a stepwise manner from one trophic level to the next, usually resulting in an enrichment of 3.4–5.0 ‰ in δ15N72 from the prey to consumer, thus, allowing to estimate the trophic position of the different organisms73. In addition, there is a small enrichment in δ13C of approximately 1 ‰ from one trophic level to the next74. Furthermore, the δ13C signature provides information of the primary source of the OM supporting the trophic web75. For example, enriched 13C ratios point to photosynthetic production (e.g., from − 22 to − 14 ‰31), while more depleted δ13C values suggest a trophic web fueled by chemoautotrophy (e.g., from − 50 to − 15 ‰ in hydrothermal and methane seep communities76).
In this study, we provide a first insight in the trophic structure of the Angolan CWC reefs, using stable isotope analyses. This work is a pivotal step to understand the trophic interactions of CWC reefs under hypoxic conditions and will contribute with new baseline knowledge on the ecological functioning of a poorly investigated deep-sea area of the SE Atlantic Ocean. This could shed light on how CWCs and associated deep-sea communities might cope with the forecasted impacts of climate change, specifically with the expected expansion of OMZs in the future77.
Results
Carbon and nitrogen stable isotope (δ13C and δ15N) analyses were conducted on benthic megafauna samples and on three types of Particulate Organic Matter (POM; filtered Suspended Particulate Organic Matter (SPOM), SPOM from a sediment trap and POM from sediment) collected from the Angolan CWC reefs. The lowest measured δ13C value was for SPOM sampled at 342 m water depth (− 22.46 ± 0.34 ‰) and the highest was for Echinus sp. (− 12.81 ± 1.65 ‰), while δ15N values ranged from 2.00 ± 1.48 ‰ for SPOM sampled at 532 m water depth to 21.90 ‰ in a Hexactinellid sponge. The carbon and nitrogen stable isotope bi-plot (Fig. 1) represents a total isotopic range of 9.65 ‰ for δ13C and of 19.9 ‰ for δ15N, with a correlation of R = 0.74 (p-value < 2.2 × 10–16) between δ13C and δ15N. The four clusters obtained with the k-means analysis match with the trophic position (TP) calculations (Table 1), indicating that each cluster represents a different trophic guild in the Angolan CWC reefs.
The three types of POM analyzed are included in cluster 1, presenting a mean stable isotopic composition of − 21.57 ± 0.59 ‰ and 4.83 ± 1.58 ‰ for δ13C and δ15N, respectively. Within this cluster, sediment sampled at 345 m water depth presented the most enriched values (− 20.84 ‰ for δ13C and 6.19 ‰ for δ15N), being 4.19 ‰ more enriched, in terms of δ15N, than SPOM sampled at 532 m water depth. The two types of SPOM analyzed (filtered SPOM and SPOM from the trap), presented a mean δ13C value of − 21.87 ± 0.44 ‰ and a mean δ15N value of 4.23 ± 1.64 ‰, while sediment had more enriched mean values of − 20.96 ± 0.17 ‰ for δ13C and of 6.05 ± 0.21 ‰ for δ15N. The SPOM samples collected at deeper sites present more enriched mean δ13C signatures (− 21.65 ± 0.35 ‰) than the ones collected at shallower sites (− 22.10 ± 0.52).
The stable isotopic signature of consumers ranged from 10.52 ± 1.07 ‰ to 21.9 ‰ in δ15N, corresponding to M. oculata and a hexactinellid sponge, respectively, whereas the consumer with most the δ13C-depleted signature was D. pertusum (− 19.77 ± 1.0 ‰) and with the most δ13C-enriched signature was Echinus sp. (− 12.81 ± 1.65 ‰).
The consumers included in cluster 2 varied from − 19.77 ± 1.0 ‰ to − 17.25 ‰, in terms of δ13C and from 10.52 ± 1.07 ‰ to 14.00 ‰, in terms of δ15N, presenting a mean δ13C value of − 18.70 ± 0.83 ‰ and a mean δ15N value of 12.90 ± 1.00 ‰. The mean calculated TP of this cluster is 3.54 ± 0.29, with the maximum TP (3.87) occupied by a polynoid annelid (Polynoidae sp.). The consumers included in this cluster are all analyzed CWC species as well as the above-mentioned annelid (Polynoidae sp.), a hydrozoan (unidentified), a sea anemone (Actinaria) and a fish (Myctophidae sp.). The distance between the mean stable isotope ratios of cluster 1 (POM) to cluster 2 is 2.9 ‰ for δ13C and 8.07 ‰ for δ15N, which corresponds to 2.37 trophic levels, if a trophic enrichment for δ15N of 3.4 ‰ is considered.
All the echinoderm taxa analyzed, plus the polychaete Eunice norvegica are part of cluster 3. This group presents the most enriched carbon stable isotope signatures with mean δ13C of − 14.00 ± 1.08 ‰ and mean δ15N of 15.00 ± 1.59 ‰. The mean TP of this group is 4.16 ± 0.47.
The organism most enriched in δ15N was a glass sponge (Hexactinellida sp.; 21.90 ‰). All analyzed sponge taxa (cluster 4) presented the highest mean δ15N ratios (mean 20.20 ± 1.87 ‰) consequently corresponding, according to the TP calculations, to the highest mean TP in the trophic web (mean TP of 5.69 ± 0.53).
Discussion
The basic structure of the food web of CWC reefs offshore Angola was deciphered, for the first time. Our results indicate a reef trophic web composed of four different trophic guilds (Fig. 2). The carbon isotope signatures of POM (− 22.46 to − 20.84 ‰) indicate that the CWC reefs are sustained by photosynthesis-derived primary production from the photic zone, consistent with what was first shown by Le Guilloux et al.78; nonetheless, the gap of one trophic level between POM (cluster 1) and suspension feeders (cluster 2) suggests that an additional food source was missed in our sampling. Although the significant correlation between δ13C and δ15N indicates a network supported by a single primary source65,79,80, the enriched δ13C signatures of predators and detritus-feeders (− 15.39 to − 12.81 ‰) and the high δ15N values of sponges (17.33 to 21.90 ‰) point to different food sources for the consumers at the Angolan CWC reefs.
The Angolan basin is an area with exceptionally high primary productivity, derived from the Benguela upwelling system46,81, and fueled by nutrients delivered by the Cuanza and Congo Rivers82. It has been argued that a nutritive food source delivered by the upwelling system could play an important role in allowing the corals to tolerate the potential stress that hypoxia and high temperatures off Angola could cause25,26,83,84, since an abundant and easily digestible food source could help balance the energetic metabolic demands of species under oxygen stress47,48. Indeed, Hanz et al.11, showed that high-quality and abundant OM, in the form of fresh phytodetritus, is available to the CWC reefs, corroborated by the low isotopic signature of δ15N of SPOM, as well as the low C/N ratios and the little degraded phytopigments of the analyzed OM11. In addition, fluvial input of terrestrial OM slightly enriches the δ13C signature of the SPOM and sediment (− 22.46 to − 21.40 ‰)11. Our results show that D. pertusum and M. oculata are 2 ‰ enriched compared to the mean δ13C signature of the analyzed POM (see cluster 1, Fig. 1), indicating that possibly the corals do not directly feed on the terrigenous-enriched POM. However, the high input of nutrients associated with the terrestrial material transported with the riverine discharges could, instead, be important to maintain the primary productivity that supports the baseline of the trophic web85. The OM fluxes to the Angolan basin fluctuate seasonally86, because of seasonal changes in the upwelling system and riverine discharges87. It is possible that this seasonality is also reflected in the diet of the CWCs, with the corals exploiting fresh phytodetritus, when available, but also opportunistically feeding on other types of food, when fresher phytodetritus is absent1,45,88.
At the Angolan CWC reefs, D. pertusum and M. oculata presented slightly higher δ15N values (11.56 ± 1.37 ‰ and 10.52 ± 1.07 ‰, respectively) than the ones reported for other CWC reefs (7.6 to 10.1 ‰ for D. pertusum and 6.9 to 10 ‰ for M. oculata) in the NE Atlantic Ocean34,35,37,89 and the Mediterranean Sea31, even though the δ15N signature of SPOM in our study (2.00 to 5.32 ‰) is comparable to the ones reported in literature (2.2 to 8.3 ‰31,34,35,37,41,44,79). In our study area in the SE Atlantic Ocean, δ15N ratios show an enrichment of 7.33 ‰ and 6.29 ‰ between SPOM and D. pertusum and M. oculata, respectively. In other studies, the observed δ15N enrichment between D. pertusum and SPOM ranged from 2.7 to 7.1 ‰31,34,35,37,44. The observed isotopic enrichment at the Angolan reefs is only similar to the one observed in the Galicia Bank (7.1 ‰34) where the authors could not define a conclusive food source for the CWCs, suggesting a mixture of different sources34. In fact, isotopic enrichment might differ between deep-sea environments and conditions35,44,70 depending on the available food sources, the metabolic rate of organisms and the isotopic composition of the surrounding water column. Furthermore, the observed δ15N enrichment in our study could also point to the presence of an additional trophic level between the phytodetritus and the corals, missed in our sampling. This gap could indicate that, in addition to fresh phytodetritus, zooplankton might be an important food source for the CWCs offshore Angola, as previously observed in other CWC reefs dominated by scleractinians31,34,89,90. Indeed, zooplankton is a nutritional rich food source for cold-water scleractinians45,91, octocorals92,93, and antipatharians31,33,94. The Angolan basin harbors abundant and diverse zooplankton communities95 whose dial vertical migrations coincide with the water depth where CWCs are found (331 to 473 m)96. The zooplankton δ15N ratios (ranging from 3.5 to 10 ‰) from other regions of the Atlantic sampled in the same depth range (300 to 500 m) as our study34,37,97,98,99 fit with the expected enrichment of the intermediate trophic level. Thus, zooplankton prey should be considered available to the examined CWCs. Accordingly, we hypothesize that the corals’ diet is most likely based on fresh phytodetritus, when available100, but zooplankton might contribute the most to the CWCs diet. However, the role of zooplankton as primary food source in the Angola CWC reefs still needs to be investigated in future studies.
Black coral and octocorals occupy the same trophic guild of D. pertusum and M. oculata (cluster 2, Fig. 1) however, their δ13C and δ15N signatures are more enriched than those of the latter two. These differences might be explained by taxon-specific (morphological and physiological) requirements36,101, since colony morphology102 and polyp size103 influence the rates of food capture104 and the selection of prey type and size61 between CWC species. This possibly leads to a less-opportunistic feeding strategy and food selection61 focused in capturing more of one type of food source, potentially zooplankton, resulting in differences in their trophic strategies93 and, consequently, isotopic signatures.
The crustacean decapod Munida sp., a fish of the family Myctophidae, and a polynoid polychaete also belong to the same trophic group as CWCs. This result highlights their suspension-feeding behavior and, most likely, all of them exploit the same food sources as the CWCs. Moreover, given that small fish are known to preferably feed on zooplankton97, this finding further supports the hypothesis of the importance of zooplankton as a food source to cluster 2. On the other hand, the polychaete E. norvegica and the analyzed echinoderms (Asteroids, Ophiuroids and Echinus sp.) are the most 13C-enriched organisms (δ13C from − 15.39 to − 12.81 ‰) with a corresponding mean TP of 4.16 ± 0.47 (cluster 3). The polychaete E. norvegica is known to live in close association with D. pertusum and M. oculata13,105,106,107 and to contribute to reef formation106, where the polychaete could benefit from extra food supply from the coral host by feeding directly on detritus in the corallites105. In the Angolan CWC reefs, E. norvegica was present at the basal part of the reef-building coral colonies29. The δ15N of E. norvegica is in the same range as the one for the other polychaete analyzed in this study. However, the comparative δ13C enrichment of E. norvegica indicates an exploitation of different food sources that could be related to its association with D. pertusum since it has been shown that, in the presence of the coral, E. norvegica assimilates more carbon through selective feeding on bigger particles108. It is possible that bigger particles consumed by E. norvegica indicate fresher particles, with a higher content of chlorophyll-a, resulting in 13C-enrichment109.
The high standard deviation in δ15N of asteroids and in the δ13C of Echinus sp. could be attributed to the opportunistic feeding behavior of the organisms in these groups110,111,112,113. Given that all the organisms included in this trophic group are mobile species, they are potentially able to exploit different food sources within the reef, including detritus31,114, zooplankton37,115 or, by directly predating corals and sponges116. The latter seems more likely, since ROV video observations have shown the sea urchin Echinus sp. on top of D. pertusum colonies (Fig. 3), and the dissection of collected specimens confirmed the presence of fragments of D. pertusum in their gut’s contents29, supporting the evidence of its predatory feeding behavior. Moreover, echinoderms in the CWC reef presented the most enriched δ13C ratios (an enrichment of 5 ‰ compared to cluster 2). One possible explanation to the 13C-enrichement of this group could be a “deep-sea sponge loop”40,70,117,118, where the sponges’ feeding on bacteria and DOM, will result in the release of 13C-enriched particulate detritus that can be assimilated by associated fauna, both through detrital feeding and by directly feeding on sponges through a predatory pathway40,118. However, this interpretation should be taken with caution since in situ experiments are needed to support a “deep-sea sponge loop”.
Sponges are active filter-feeders and, therefore, it was expected that sponges act as primary consumers on the Angolan CWC reefs. However, sponges exhibited the highest δ15N values (from 17.33 to 21.90 ‰) of all samples analyzed in this study. These results are in the range of, and sometimes higher than, values usually attributed to top predators in marine trophic webs119,120. According to TP calculations following Post,72, the 15N-enriched ratios of sponges correspond to a mean TP of 5.69 ± 0.53 (Table 1), being inconsistent with the expected filter feeding behavior in the trophic web. Hanz et al.70 showed that TP calculations based on δ15N might not be appropriate to infer the TP of deep-sea sponges because when other biomarkers are used (such as compound specific isotope analyses), sponges act as normal filter feeders. Instead, the high δ15N values of sponges possibly indicate that sponges rely on additional food sources that have not been included in our stable isotope food model.
Sponges are capable of opportunistically exploiting a wide range of both organic and inorganic food sources, including DOM45,121, phyto- and bacterioplankton118,122,123,124,125, or even small zooplankton through the specialization of a group of sponges (Family Cladorhizidae) to utilize carnivory feeding modes126,127. In fact, the enriched δ15N values of hexactinellid sponges in the Angolan reefs are not entirely surprising since similarly high ratios have also been reported for deep-sea sponges in several other studies in the North Atlantic37,79,98, Pacific125,128, Arctic70,114,129 and Antarctic66,130 Oceans. The 15N-enriched values of sponges could be attributed to intense nitrogen cycling pathways in the sponge’s tissue70,131 driven by (1) the sponge holobiont37,79, defined here as the sponge and its associated microbial communities, and/or (2) the sponge’s feeding on heterotrophic re-suspended bacteria that are 15N-enriched because of the uptake of waste material of higher trophic levels70,125,130.
The Angolan CWC reefs occur in the center of the local OMZ and OMZs are zones with thriving microbial communities55 and complex nitrogen cycling dynamics54,132,133. The tissue of sponges is rich in microbial communities53,129,134,135 and the nitrogen isotope fractionation in sponges changes according to their bacterial richness53,70,125, i.e., if High Microbial Abundance (HMA) sponges or Low Microbial Abundance (LMA) sponges70,136. The sponge holobiont takes energy from DOM137 and, as a result of OM degradation, will release ammonium (NH4+)70,123,138, an isotopically depleted metabolic end-product139, leading to increased δ15N in the sponge tissue. Moreover, symbiotic relationships with bacteria, capable of both denitrification and anammox131,140,141, play an important role in sponge survival under low oxygen environmental conditions52,53,142,143. Likewise, it has been shown by Middelburg et al.52 that denitrification can occur in D. pertusum, due to the dominance of denitrifying bacteria in the coral’s holobiont and this process is enhanced by low-oxygen conditions. It is beyond the scope of our study to identify the exact physiological mechanisms used by benthic organisms to cope with low-oxygen environments, but the observed δ15N ratios of sponges in our study hints that interactions with microbes could be a plausible mechanism to withstand the hypoxic conditions. Given the slightly enriched δ15N values of D. pertusum, the CWC holobiont could also potentially play a role in the coral’s coping with the hypoxia conditions of the Angolan CWC reefs50,52, although this is more likely to be more significant for sponges given their enriched stable nitrogen isotope values.
This study gives the first insights into the trophic structure of the Angolan CWC reefs, where different feeding strategies are utilized by the organisms inhabiting in this OMZ. Our observations provide the first evidence pointing to an important role of zooplankton as food source for CWCs in Angola, and to a strong reliance of sponges, through their holobiont, on bacteria as food source in hypoxic conditions. The use of other biomarkers in future studies, such as compound specific stable isotope and fatty acids analyses, or in situ experiments with isotopically labelled food will contribute to a better understanding of CWCs and sponge’s nutrition. We further suggest that, in the future, special attention should be given to the potential role of the holobiont in allowing CWCs and sponges to withstand the conditions of the Angolan and other OMZs.
Methods
Study area
The Angola basin is located along the SW African continent in the SE Atlantic Ocean and belongs to the Benguela Current Large Marine Ecosystem (BCLME)144. The region is influenced by the Benguela upwelling system, one of the world’s most productive145, with an estimated primary production of 156 million t C yr–1146. Induced by coastal parallel winds, the upwelling of nutrient-rich cold waters results in enhanced primary productivity81, while the remineralization of high concentrations of OM in the water column results in severe mid-depth oxygen depletion and in a pronounced OMZ147 that coincides with the presence of the Angola CWC mounds25. In addition, the area receives a high input of riverine discharges from the Congo and Cuanza Rivers, which leads to further increase in primary production due to a high terrigenous nutrient input11,82. At approximately 17°S, the cold nutrient-rich waters transported northward by the Benguela Current interact with the warm nutrient-poor Angola Current148, forming the Angola-Benguela Frontal Zone (ABFZ)149. Oxygen-depleted and nutrient-rich waters are characteristic from 70 to 600 m water depth, indicating the presence of the South Atlantic Central Water (SACW)150, which is transported southward by the Angola Current.
The Angola CWC reefs cover long ridges to individual coral mounds that can reach up to 100 m above the surrounding sea floor. These CWC ridges and mounds have formed on millennial and longer time scales151, through successive periods of CWC reef development. They are composed of CWC fragments and other shells loosely embedded in fine hemipelagic sediments25,29,30.
Sample collection
Samples were collected in January 2016 during the M122 (“ANNA”) expedition on board the R/V Meteor29. In total, 18 reef sites topping seven different CWC mound complexes (Fig. 4, Table 2) were sampled for stable isotope analyses. Samples of organisms belonging to the taxa Porifera, Cnidaria, Arthropoda, Annelida, Echinodermata and Chordata were collected by means of a box corer (box dimensions: 50 × 50 cm, 55 cm high), a Van-Veen grab sampler or the Remotely Operated Vehicle (ROV) SQUID (MARUM, Bremen, Germany)29 (Supplementary Table S1). Each organism was identified to the lowest possible taxonomic level, rinsed in seawater and put in plastic bags or vials.
To investigate potential food sources for the megabenthic fauna, three types of POM were collected: SPOM from the water column, settling material from the sediment trap (SPOM trap), and sediment. SPOM was collected at two depths (342 and 532 m) at 40 cm above the seafloor using a McLane phytoplankton pump, attached to the ALBEX lander (NIOZ), with a maximum of 7.5 L of water pumped every 2 h for a period of 48 h over 24 GF/F filters (47 mm Whatman™ GF/F filters pre-combusted at 450 °C) (for more details see Hanz et al.11). Settling SPOM (SPOM trap) was also collected with a sediment trap (Technicap PPS4/3) attached to the ALBEX lander, with the collector at 2 m above the bottom over a sampling duration of 2.5 days, at both 342 and 526 m depth. Additionally, two sediment samples were collected at two depths (259 and 345 m): one with the box corer and another one with the Van-Veen grab sampler. All organisms and POM samples were stored on board at – 20 °C and, afterwards, were freeze-dried in the laboratory and stored at − 20 °C until further analysis.
Sample preparation for stable isotope analyses
Fragments of freeze-dried faunal samples were ground to powder with a mortar and, depending on the quantity of sample available, two subsamples of 10 to 50 mg were weighted. One subsample was left untreated for δ15N determination, whereas the other was acidified with the addition of 10% HCl drop-by-drop until effervescence ceased and used for δ13C determination. The acidification of samples is a common practice in stable isotope analyses and aims to remove inorganic calcium carbonate from the organisms, known to interfere with δ13C ratios112. All samples analyzed for δ13C were acidified, except fish samples due to their low carbonate content152. After acidification, the subsamples were oven-dried at 50 °C for 72 h. Afterwards, three pseudo replicates of each subsample were weighted with a precision balance (± 0.001 mg) into tin capsules (11 × 4 mm, Elementar Microanalysis) to conduct the isotopic composition analyses. Depending on the taxonomic group, subsamples of 0.4 to 4 mg were weighted.
Sample preparation for the determination of δ15N and δ13C for the three types of POM considered (filtered SPOM, SPOM trap and sediment) is described in detail in Hanz et al.9. These samples were acidified by fuming HCl (20%) vapor over night for δ13C determination. Three replicates of sediment (1.6 to 3.6 mg for δ13C and 9 mg for δ15N) and sediment trap material (1 mg δ13C and 4 to 5 mg for δ15N) were weighted into tin capsules. For SPOM, a ¼ section of each GF/F filter was transferred into tin capsules for δ13C and δ15N analyses.
Stable isotope analyses
Analyses of benthic megafauna samples were performed using the Elementar IsoPrime 100 isotope ratio–mass spectrometry (IR–MS) instrument (IsoPrime Ltd.) coupled to a CNS elemental analyzer (Elementar Vario Pyro Cube EA CNS; Elementar Analysensysteme GmbH). Stable carbon isotopic values (δ13C) were quality checked and calibrated by using the reference materials Glucose (BCR-657) and Polyethylene (IAEA-CH-7), while for the stable nitrogen isotopic (δ15N) values potassium nitrate (USGS32), caffeine (IAEA600) and ammonium sulfate (USGS25) were used.
The δ15N and δ13C values of filtered SPOM, SPOM trap and sediment were analyzed by a Delta V Advantage IR–MS coupled online to an elemental analyzer (Flash 2000 EA-IRMS) by a ConFlo IV (Thermo Fisher Scientific Inc.). Benzoic acid and acetanilide were used as standards for δ13C, whereas acetanilide, urea and casein were used as standards for δ15N (for more details see Hanz et al.9).
Vienna Pee Dee belemnite (V.P.D.B.) for carbon, and atmospheric N2 (Air) for nitrogen, were used as reference materials, and stable isotope values are here reported with respect to those. Precision is based on the standard deviation between replicate analyses and was < 0.50 ‰ for δ15N and < 0.20 ‰ for δ13C for faunal samples, and < 0.15 ‰ for δ15N and δ13C for POM.
Stable isotope ratios (δ13C and δ15N), in relation to the standards, were calculated as following:
where R corresponds to 13C/12C or 15N/14N of the analyzed sample (Rsample) and standard used (Rstandard).
Data analysis
The Trophic Position (TP) of consumers was calculated following Post72, as in similar studies on deep-sea habitats98,115,153,154. The TP of each consumer was calculated using the following equation:
where TPn corresponds to the trophic position of the organism, δ15Nn corresponds to its stable nitrogen isotope ratios, δ15Nbaseline represents the nitrogen isotopic composition of the baseline, TEF corresponds to the Trophic Enrichment Factor for δ15N and λ represents the trophic level occupied by the baseline. The δ15N of the baseline considered was 4.23 ± 1.65 ‰, corresponding to the mean ratio measured for SPOM (λ = 1). A TEF of 3.4 ‰ for δ15N was considered, since it has been regarded as appropriate in other CWC habitats31,37.
To explore the different trophic guilds of the Angolan CWC reefs, a k-means clustering analysis was applied to the δ13C and δ15N data, computed using the “factoextra” package155 within R Studio156 under R version 4.1.3157. The optimal number of clusters (k = 4) was investigated using the “NbClust” R package158 by applying three different methods: elbow, silhouette, and gap statistic methods (Supplementary Fig. S2). The Pearson correlation between δ13C and δ15N ratios was calculated using the “cor.test” function available in the “stats” package in R. Since fauna and POM samples were collected along different CWC mounds, it was not possible in our study to assess how the stable isotopic ratios would differ between mounds.
Data availability
Dataset with samples metadata and carbon and nitrogen stable isotope values are available in Pangaea159 (https://doi.org/10.1594/PANGAEA.955091).
References
Mueller, C. E., Larsson, A. I., Veuger, B., Middelburg, J. J. & van Oevelen, D. Opportunistic feeding on various organic food sources by the cold-water coral Lophelia pertusa. Biogeosciences 11, 123–133. https://doi.org/10.5194/bg-11-123-2014 (2014).
van Oevelen, D. et al. The cold-water coral community as hotspot of carbon cycling on continental margins: A food-web analysis from Rockall Bank (northeast Atlantic). Limnol. Oceanogr. 54, 1829–1844. https://doi.org/10.4319/lo.2009.54.6.1829 (2009).
Cathalot, C. et al. Cold-water coral reefs and adjacent sponge grounds: Hotspots of benthic respiration and organic carbon cycling in the deep sea. Front. Mar. Sci. 2, 37. https://doi.org/10.3389/fmars.2015.00037 (2015).
Thiem, Ø., Ravagnan, E., Fosså, J. H. & Berntsen, J. Food supply mechanisms for cold-water corals along a continental shelf edge. J. Mar. Syst. 60, 207–219. https://doi.org/10.1016/j.jmarsys.2005.12.004 (2006).
Mohn, C. et al. Linking benthic hydrodynamics and cold-water coral occurrences: A high-resolution model study at three cold-water coral provinces in the NE Atlantic. Prog. Oceanogr. 122, 92–104. https://doi.org/10.1016/j.pocean.2013.12.003 (2014).
Frederiksen, R., Jensen, A. & Westerberg, H. The distribution of the scleractinian coral Lophelia pertusa around the Faroe islands and the relation to internal tidal mixing. Sarsia 77, 157–171. https://doi.org/10.1080/00364827.1992.10413502 (1992).
van Haren, H., Mienis, F., Duineveld, G. C. A. & Lavaleye, M. S. S. High-resolution temperature observations of a trapped nonlinear diurnal tide influencing cold-water corals on the Logachev mounds. Prog. Oceanogr. 125, 16–25. https://doi.org/10.1016/j.pocean.2014.04.021 (2014).
Davies, A. J. et al. Downwelling and deep-water bottom currents as food supply mechanisms to the cold-water coral Lophelia pertusa (Scleractinia) at the Mingulay Reef Complex. Limnol. Oceanogr. 54, 620–629. https://doi.org/10.4319/lo.2009.54.2.0620 (2009).
Hebbeln, D. et al. Environmental forcing of the Campeche cold-water coral province, southern Gulf of Mexico. Biogeosciences 11, 1799–1815. https://doi.org/10.5194/bg-11-1799-2014 (2014).
de Clippele, L. H. et al. Using novel acoustic and visual mapping tools to predict the small-scale spatial distribution of live biogenic reef framework in cold-water coral habitats. Coral Reefs 36, 255–268. https://doi.org/10.1007/s00338-016-1519-8 (2017).
Hanz, U. et al. Environmental factors influencing benthic communities in the oxygen minimum zones on the Angolan and Namibian margins. Biogeosciences 16, 4337–4356. https://doi.org/10.5194/bg-16-4337-2019 (2019).
Addamo, A. M. et al. Merging scleractinian genera: The overwhelming genetic similarity between solitary Desmophyllum and colonial Lophelia. BMC Evol. Biol. 16, 1–17. https://doi.org/10.1186/s12862-016-0654-8 (2016).
Buhl-Mortensen, L. et al. Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar. Ecol. 31, 21–50. https://doi.org/10.1111/j.1439-0485.2010.00359.x (2010).
Price, D. M., Robert, K., Callaway, A., Hall, R. A. & Huvenne, V. A. I. Using 3D photogrammetry from ROV video to quantify cold-water coral reef structural complexity and investigate its influence on biodiversity and community assemblage. Coral Reefs 38, 1007–1102. https://doi.org/10.1007/s00338-019-01827-3 (2019).
Hennige, S. J. et al. Using the Goldilocks Principle to model coral ecosystem engineering. Proc. R. Soc. B 288, 20211260. https://doi.org/10.1098/rspb.2021.1260 (2021).
Henry, L. A. & Roberts, J. M. Biodiversity and ecological composition of macrobenthos on cold-water coral mounds and adjacent off-mound habitat in the bathyal Porcupine Seabight, NE Atlantic. Deep Sea Res. Part I 54, 654–672. https://doi.org/10.1016/j.dsr.2007.01.005 (2007).
Lessard-Pilon, S. A., Podowski, E. L., Cordes, E. E. & Fisher, C. R. Megafauna community composition associated with Lophelia pertusa colonies in the Gulf of Mexico. Deep Sea Res. Part II 57, 1882–1890. https://doi.org/10.1016/j.dsr2.2010.05.013 (2010).
Rueda, J. L. et al. Cold-water coral associated fauna in the Mediterranean Sea and adjacent areas. Mediterr. Cold-Water Corals 9, 295–333. https://doi.org/10.1007/978-3-319-91608-8_29(Springer (2019).
Costello, M. J. et al. Role of cold-water coral reefs as fish habitat in the NE Atlantic. Cold-Water Corals Ecosyst. https://doi.org/10.1007/3-540-27673-4_41 (2005).
Purser, A. et al. Local variation in the distribution of benthic megafauna species associated with cold-water coral reefs on the Norwegian margin. Cont. Shelf Res. 54, 37–51. https://doi.org/10.1016/j.csr.2012.12.013 (2013).
Buhl-Mortensen, P., Hovland, M., Brattegard, T. & Farestveit, R. Deep water bioherms of the scleractinian coral Lophelia pertusa (L) at 64° N on the Norwegian shelf: Structure and associated megafauna. Sarsia 80, 145–158. https://doi.org/10.1080/00364827.1995.10413586 (1995).
Buhl-Mortensen, P., Buhl-Mortensen, L. & Purser, A. Trophic ecology and habitat provision in cold-water coral ecosystems. In Marine Animal Forests (eds Rossi, S. et al.) (Springer, 2017).
Bartzke, G. et al. Investigating the prevailing hydrodynamics around a cold-water coral colony using a physical and a numerical approach. Front. Mar. Sci. 8, 1375. https://doi.org/10.3389/fmars.2021.663304 (2021).
Corbera, G. et al. Local-scale feedbacks influencing cold-water coral growth and subsequent reef formation. Sci. Rep. 12, 20389. https://doi.org/10.1038/s41598-022-24711-7 (2022).
Hebbeln, D. et al. Cold-water coral reefs thriving under hypoxia. Coral Reefs 39, 853–859. https://doi.org/10.1007/s00338-020-01934-6 (2020).
Orejas, C. et al. Madrepora oculata forms large frameworks in hypoxic waters off Angola (SE Atlantic). Sci. Rep. 11, 15170. https://doi.org/10.1038/s41598-021-94579-6 (2021).
Dodds, L. A., Roberts, J. M., Taylor, A. C. & Marubini, F. Metabolic tolerance of the cold-water coral Lophelia pertusa (Scleractinia) to temperature and dissolved oxygen change. J. Exp. Mar. Biol. Ecol. 349, 205–214. https://doi.org/10.1016/j.jembe.2007.05.013 (2007).
Davies, A. J., Wisshak, M., Orr, J. C. & Murray Roberts, J. Predicting suitable habitat for the cold-water coral Lophelia pertusa (Scleractinia). Deep Sea Res. Part I 55, 1048–1062. https://doi.org/10.1016/j.dsr.2008.04.010 (2008).
Hebbeln, D. et al. ANNA Cold-Water Coral Ecosystems off Angola and Namibia, Cruise No. M122, 30 December 2015–31 January 2016, Walvis Bay (Namibia), Walvis Bay (Namibia). METEOR-Berichte. https://doi.org/10.2312/cr_m122 (2017).
Wienberg, C. et al. (accepted) Cold-water coral reefs in the oxygen minimum zones off West Africa. In Cold-Water Coral Reefs of the World (eds. Cordes, E. & Mienis, F. ) (Springer series: Coral Reefs of the World).
Carlier, A. et al. Trophic relationships in a deep Mediterranean cold-water coral bank (Santa Maria di Leuca, Ionian Sea). Mar. Ecol. Prog. Ser. 397, 125–137. https://doi.org/10.3354/meps08361 (2009).
Gori, A. et al. Size and spatial structure in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Mar. Biol. 158, 1721–1732. https://doi.org/10.1007/s00227-011-1686-7 (2011).
Coppari, M. et al. Seasonal variation of the stable C and N isotopic composition of the mesophotic black coral Antipathella subpinnata (Ellis & Solander, 1786). Estuar Coast Shelf Sci. 233, 106520. https://doi.org/10.1016/j.ecss.2019.106520 (2020).
Duineveld, G. C. A., Lavaleye, M. S. S. & Berghuis, E. M. Particle flux and food supply to a seamount cold-water coral community (Galicia Bank, NW Spain). Mar. Ecol. Prog. Ser. 277, 13–23. https://doi.org/10.3354/meps277013 (2004).
Duineveld, G. C. A., Lavaleye, M. S. S., Bergman, M. J. N., de Stigter, H. & Mienis, F. Trophic structure of a cold-water coral mound community (Rockall Bank, NE Atlantic) in relation to the near-bottom particle supply and current regime. Bull. Mar. Sci. 81, 449–467 (2007).
Sherwood, O. A., Jamieson, R. E., Edinger, E. N. & Wareham, V. E. Stable C and N isotopic composition of cold-water corals from the Newfoundland and Labrador continental slope: Examination of trophic, depth and spatial effects. Deep Sea Res. Part I 55, 1392–1402. https://doi.org/10.1016/j.dsr.2008.05.013 (2008).
van Oevelen, D., Duineveld, G. C. A., Lavaleye, M. S. S., Kutti, T. & Soetaert, K. Trophic structure of cold-water coral communities revealed from the analysis of tissue isotopes and fatty acid composition. Mar. Biol. Res. 14, 287–306. https://doi.org/10.1080/17451000.2017.1398404 (2018).
Becker, E. L., Cordes, E. E., Macko, S. A. & Fisher, C. R. Importance of seep primary production to Lophelia pertusa and associated fauna in the Gulf of Mexico. Deep Sea Res. Part I 56, 786–800. https://doi.org/10.1016/j.dsr.2008.12.006 (2009).
Gori, A., Grover, R., Orejas, C., Sikorski, S. & Ferrier-Pagès, C. Uptake of dissolved free amino acids by four cold-water coral species from the Mediterranean Sea. Deep Sea Res. Part II 99, 42–50. https://doi.org/10.1016/j.dsr2.2013.06.007 (2014).
Maier, S. R. et al. Recycling pathways in cold-water coral reefs: Use of dissolved organic matter and bacteria by key suspension feeding taxa. Sci. Rep. 10, 1–13. https://doi.org/10.1038/s41598-020-66463-2 (2020).
Duineveld, G. C. A. et al. Spatial and tidal variation in food supply to shallow cold-water coral reefs of the Mingulay Reef complex (Outer Hebrides, Scotland). Mar. Ecol. Prog. Ser. 444, 97–115. https://doi.org/10.3354/meps09430 (2012).
Dodds, L. A., Black, K. D., Orr, H. & Roberts, J. M. Lipid biomarkers reveal geographical differences in food supply to the cold-water coral Lophelia pertusa (Scleractinia). Mar. Ecol. Prog. Ser. 397, 113–124. https://doi.org/10.3354/meps08143 (2009).
Naumann, M. S., Orejas, C., Wild, C. & Ferrier-Pagès, C. First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral. J. Exp. Biol. 214, 3570–3576. https://doi.org/10.1242/jeb.061390 (2011).
Kiriakoulakis, K. et al. Lipids and nitrogen isotopes of two deep-water corals from the North-East Atlantic: Initial results and implications for their nutrition. In Cold-Water Corals and Ecosystems 715–729 (Springer, 2005).
Maier, S. R., Bannister, R. J., van Oevelen, D. & Kutti, T. Seasonal controls on the diet, metabolic activity, tissue reserves and growth of the cold-water coral Lophelia pertusa. Coral Reefs 39, 173–187. https://doi.org/10.1007/S00338-019-01886-6 (2020).
Messié, M. & Chavez, F. P. Seasonal regulation of primary production in eastern boundary upwelling systems. Prog. Oceanogr. 134, 1–18. https://doi.org/10.1016/j.pocean.2014.10.011 (2015).
Levin, L. A., Huggett, C. L. & Wishner, K. F. Control of deep-sea benthic community structure by oxygen and organic-matter gradients in the eastern Pacific Ocean. J. Mar. Res. 49, 763–800. https://doi.org/10.1357/002224091784995756 (1991).
Diaz, R. J. & Rosenberg, R. Marine benthic hypoxia: A review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr. Mar. Biol. 33, 243–245 (1995).
Levin, L. A. Oxygen minimum zone benthos: Adaptation and community response to hypoxia. Oceanogr. Mar. Biol. Annu. Rev. 41, 1–45 (2003).
Gori, A. et al. Natural hypoxic conditions do not affect the respiration rates of the cold-water coral Desmophyllum pertusum (Lophelia pertusa) living in the Angola margin (Southeastern Atlantic Ocean). Deep Sea Res. Part I https://doi.org/10.1016/j.dsr.2023.104052 (2023).
Hoffmann, F. et al. An anaerobic world in sponges. Geomicrobiol. J. 22(1–2), 1–10. https://doi.org/10.1080/01490450590922505 (2007).
Middelburg, J. J. et al. Discovery of symbiotic nitrogen fixation and chemoautotrophy in cold-water corals. Sci. Rep. 5, 1–9. https://doi.org/10.1038/srep17962 (2015).
Maldonado, M. et al. A microbial nitrogen engine modulated by Bacteriosyncytia in hexactinellid sponges: Ecological implications for deep-sea communities. Front. Mar. Sci. https://doi.org/10.3389/fmars.2021.638505 (2021).
Lam, P. & Kuypers, M. M. M. Microbial nitrogen cycling processes in oxygen minimum zones. Ann. Rev. Mar. Sci. 3, 317–345. https://doi.org/10.1146/annurev-marine-120709-142814 (2010).
Wright, J. J., Konwar, K. M. & Hallam, S. J. Microbial ecology of expanding oxygen minimum zones. Nat. Rev. Microbiol. 10, 381–394. https://doi.org/10.1038/nrmicro2778 (2012).
Levin, L. A. et al. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6, 2063–2098. https://doi.org/10.5194/bg-6-2063-2009 (2009).
Kalvelage, T. et al. Aerobic microbial respiration in oceanic oxygen minimum zones. PLoS ONE 10, e0133526. https://doi.org/10.1371/journal.pone.0133526 (2015).
Churchill, D. A. et al. Trophic interactions of common elasmobranchs in deep-sea communities of the Gulf of Mexico revealed through stable isotope and stomach content analysis. Deep Sea Res. Part II 115, 92–102. https://doi.org/10.1016/j.dsr2.2014.10.011 (2015).
Hoving, H. J. T. & Haddock, S. H. D. The giant deep-sea octopus Haliphron atlanticus forages on gelatinous fauna. Sci. Rep. 7, 1–4. https://doi.org/10.1038/srep44952 (2017).
Coma, R., Gili, J.-M., Zabala, M. & Riera, T. Feeding and prey capture cycles in the aposymbiontic gorgonian Paramuricea clavata. Mar. Ecol. Prog. Ser. 115, 257–270 (1994).
Orejas, C., Gili, J. M. & Arntz, W. The role of the small planktonic communities in the diet of two Antarctic octocorals (Primnoisis antarctica and Primnoella sp.). Mar. Ecol. Prog. Ser. 250, 105–116. https://doi.org/10.3354/meps250105 (2003).
Hoving, H. J. T. & Robison, B. H. Deep-sea in situ observations of gonatid squid and their prey reveal high occurrence of cannibalism. Deep Sea Res. Part I 116, 94–98. https://doi.org/10.1016/j.dsr.2016.08.001 (2016).
Choy, C. A., Haddock, S. H. D. & Robison, B. H. Deep pelagic food web structure as revealed by in situ feeding observations. Proc. R. Soc. B 284, 20172116. https://doi.org/10.1098/rspb.2017.2116 (2017).
Iken, K., Bluhm, B. A. & Gradinger, R. Food web structure in the high Arctic Canada Basin: Evidence from δ13C and δ15N analysis. Polar Biol. 28, 238–249. https://doi.org/10.1007/s00300-004-0669-2 (2005).
Polunin, N. V. C. et al. Feeding relationships in Mediterranean bathyal assemblages elucidated by stable nitrogen and carbon isotope data. Mar. Ecol. Prog. Ser. 220, 13–23. https://doi.org/10.3354/meps220013 (2001).
Mincks, S. L., Smith, C. R., Jeffreys, R. M. & Sumida, P. Y. G. Trophic structure on the West Antarctic Peninsula shelf: Detritivory and benthic inertia revealed by δ13C and δ15N analysis. Deep Sea Res. Part II 55, 2502–2514. https://doi.org/10.1016/j.dsr2.2008.06.009 (2008).
Boyle, M. D., Ebert, D. A. & Cailliet, G. M. Stable-isotope analysis of a deep-sea benthic-fish assemblage: Evidence of an enriched benthic food web. J. Fish Biol. 80, 1485–1507. https://doi.org/10.1111/j.1095-8649.2012.03243.x (2012).
Rossi, S. & Elias-Piera, F. Trophic ecology of three echinoderms in deep waters of the Weddell Sea (Antarctica). Mar. Ecol. Prog. Ser. 596, 143–153. https://doi.org/10.3354/meps12544 (2018).
Puccinelli, E., Smart, S. M. & Fawcett, S. E. Temporal variability in the trophic composition of benthic invertebrates in the Indian Sub-Antarctic Ocean. Deep Sea Res. Part I 163, 103340. https://doi.org/10.1016/j.dsr.2020.103340 (2020).
Hanz, U. et al. The important role of sponges in carbon and nitrogen cycling in a deep-sea biological hotspot. Funct. Ecol. 00, 1–12. https://doi.org/10.1111/1365-2435.14117 (2022).
Tieszen, L. L., Boutton, T. W., Tesdahl, K. G. & Slade, N. A. Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57, 32–37. https://doi.org/10.1007/bf00379558 (1983).
Post, D. M. Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology 83, 703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:usitet]2.0.co;2 (2002).
Deniro, M. J. & Epstein, S. Influence of diet on the distribution of nitrogen isotopes in animals. Geochim. Cosmochim. Acta 45, 341–351. https://doi.org/10.1016/0016-7037(81)90244-1 (1981).
Fry, B. & Sherr, E. B. δC Measurements as Indicators of Carbon Flow in Marine and Freshwater Ecosystems 196–229 (Elsevier, 1989).
Smith, B. N. & Epstein, S. Two categories of 13C/12C ratios for higher plants. Plant Physiol. 47, 380–384. https://doi.org/10.1104/PP.47.3.380 (1971).
Yamanaka, T. et al. A compilation of the stable isotopic compositions of Carbon, Nitrogen, and Sulfur in soft body parts of animals collected from deep-sea hydrothermal vent and methane seep fields: Variations in energy source and importance of subsurface microbial processes in the sediment-hosted systems. In Subseafloor biosphere linked to hydrothermal systems 105–129 (Springer, 2015). https://doi.org/10.1007/978-4-431-54865-2_10.
Sweetman, A. K. et al. Major impacts of climate change on deep-sea benthic ecosystems. Elementa https://doi.org/10.1525/elementa.203 (2017).
le Guilloux, E. et al. First observations of deep-sea coral reefs along the Angola margin. Deep Sea Res. Part II 56, 2394–2403. https://doi.org/10.1016/j.dsr2.2009.04.014 (2009).
Iken, K., Brey, T., Wand, U., Voigt, J. & Junghans, P. Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): A stable isotope analysis. Prog. Oceanogr. 50, 383–405. https://doi.org/10.1016/s0079-6611(01)00062-3 (2001).
Fanelli, E., Cartes, J. E. & Papiol, V. Food web structure of deep-sea macrozooplankton and micronekton off the Catalan slope: Insight from stable isotopes. J. Mar. Syst. 87, 79–89. https://doi.org/10.1016/j.jmarsys.2011.03.003 (2011).
Carr, M. E. & Kearns, E. J. Production regimes in four Eastern Boundary Current systems. Deep Sea Res. Part II 50, 3199–3221. https://doi.org/10.1016/j.dsr2.2003.07.015 (2003).
Baudin, F. et al. Organic carbon accumulation in modern sediments of the Angola basin influenced by the Congo deep-sea fan. Deep Sea Res. Part II 142, 64–74. https://doi.org/10.1016/j.dsr2.2017.01.009 (2017).
Juva, K., Flögel, S., Karstensen, J., Linke, P. & Dullo, W. C. Tidal dynamics control on cold-water coral growth: A high-resolution multivariable study on Eastern Atlantic cold-water coral sites. Front. Mar. Sci. 7, 132. https://doi.org/10.3389/fmars.2020.00132 (2020).
da Portilho-Ramos, R. C. et al. Major environmental drivers determining life and death of cold-water corals through time. PLoS Biol. 20, e3001628. https://doi.org/10.1371/journal.pbio.3001628 (2022).
Mienis, F. et al. The influence of near-bed hydrodynamic conditions on cold-water corals in the Viosca Knoll area, Gulf of Mexico. Deep Sea Res. Part I 60, 32–45. https://doi.org/10.1016/j.dsr.2011.10.007 (2012).
Signorini, S. R. et al. Biological and physical signatures in the tropical and subtropical Atlantic. J. Geophys. Res. Oceans 104, 18367–18382. https://doi.org/10.1029/1999jc900134 (1999).
Reason, C. J. C., Landman, W. & Tennant, W. Seasonal to decadal prediction of Southern African climate and its links with variability of the Atlantic Ocean. Bull. Am. Meteorol. Soc. 87, 941–956. https://doi.org/10.1175/BAMS-87-7-941 (2006).
Gori, A. et al. Reproductive cycle and trophic ecology in deep versus shallow populations of the Mediterranean gorgonian Eunicella singularis (Cap de Creus, northwestern Mediterranean Sea). Coral Reefs 31, 823–837. https://doi.org/10.1007/s00338-012-0904-1 (2012).
de Froe, E. et al. Hydrography and food distribution during a tidal cycle above a cold-water coral mound. Deep Sea Res. Part I 189, 103854. https://doi.org/10.1016/j.dsr.2022.103854 (2022).
Kiriakoulakis, K., Bett, B. J., White, M. & Wolff, G. A. Organic biogeochemistry of the Darwin Mounds, a deep-water coral ecosystem, of the NE Atlantic. Deep Sea Res. Part I 51, 1937–1954. https://doi.org/10.1016/j.dsr.2004.07.010 (2004).
Naumann, M. S., Tolosa, I., Taviani, M., Grover, R. & Ferrier-Pagès, C. Trophic ecology of two cold-water coral species from the Mediterranean Sea revealed by lipid biomarkers and compound-specific isotope analyses. Coral Reefs 34, 1165–1175. https://doi.org/10.1007/s00338-015-1325-8 (2015).
Sherwood, O. A. et al. Stable isotopic composition of deep-sea gorgonian corals Primnoa spp.: A new archive of surface processes. Mar. Ecol. Prog. Ser. 301, 135–148. https://doi.org/10.3354/meps301135 (2005).
Rakka, M. et al. Contrasting metabolic strategies of two co-occurring deep-sea octocorals. Sci. Rep. 11, 10633. https://doi.org/10.1038/s41598-021-90134-5 (2021).
Rakka, M. et al. Feeding biology of a habitat-forming antipatharian in the Azores Archipelago. Coral Reefs 39, 1469–1482. https://doi.org/10.1007/s00338-020-01980-0 (2020).
Teuber, L. et al. Distribution and ecophysiology of calanoid copepods in relation to the oxygen minimum zone in the eastern tropical Atlantic. PLoS ONE 8, e77590. https://doi.org/10.1371/journal.pone.0077590 (2013).
Postel, L. et al. Zooplankton biomass variability off Angola and Namibia investigated by a lowered ADCP and net sampling. J. Mar. Syst. 68, 143–166. https://doi.org/10.1016/j.jmarsys.2006.11.005 (2007).
Bode, A. et al. The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: Natural abundance of stable carbon and nitrogen isotopes. ICES J. Mar. Sci. 60, 11–22. https://doi.org/10.1006/jmsc.2002.1326 (2003).
Colaço, A., Giacomello, E., Porteiro, F. & Menezes, G. M. Trophodynamic studies on the condor seamount (Azores, Portugal, North Atlantic). Deep Sea Res. Part II 98, 178–189. https://doi.org/10.1016/j.dsr2.2013.01.010 (2013).
Figueiredo, G. G. A. A. et al. Body size and stable isotope composition of zooplankton in the western tropical Atlantic. J. Mar. Syst. 212, 103449. https://doi.org/10.1016/j.jmarsys.2020.103449 (2020).
Gori, A. et al. Biochemical composition of the cold-water coral Dendrophyllia cornigera under contrasting productivity regimes: Insights from lipid biomarkers and compound-specific isotopes. Deep Sea Res. Part I 141, 106–117. https://doi.org/10.1016/j.dsr.2018.08.010 (2018).
Salvo, F., Hamoutene, D., Hayes, V. E. W., Edinger, E. N. & Parrish, C. C. Investigation of trophic ecology in Newfoundland cold-water deep-sea corals using lipid class and fatty acid analyses. Coral Reefs 37, 157–171. https://doi.org/10.1007/s00338-017-1644-z (2018).
Mortensen, P. B. & Buhl-Mortensen, L. Morphology and growth of the deep-water gorgonians Primnoa resedaeformis and Paragorgia arborea. Mar. Biol. 147, 775–788. https://doi.org/10.1007/s00227-005-1604-y (2005).
Palardy, J. E., Grottoli, A. G. & Matthews, K. A. Effects of upwelling, depth, morphology and polyp size on feeding in three species of Panamanian corals. Mar. Ecol. Prog. Ser. 300, 79–89. https://doi.org/10.3354/meps300079 (2005).
Tsounis, G. et al. Prey-capture rates in four Mediterranean cold water corals. Mar. Ecol. Prog. Ser. 398, 149–155. https://doi.org/10.3354/meps08312 (2010).
Mortensen, P. B. Aquarium observations on the deep-water coral Lophelia pertusa (L, 1758) (scleractinia) and selected associated invertebrates. Ophelia 54, 83–104. https://doi.org/10.1080/00785236.2001.10409457 (2001).
Roberts, J. M. Reef-aggregating behaviour by symbiotic eunicid polychaetes from cold-water corals: Do worms assemble reefs?. J. Mar. Biol. Assoc. U.K. 85, 813–819. https://doi.org/10.1017/s0025315405011756 (2005).
Oppelt, A., López Correa, M. & Rocha, C. Biogeochemical analysis of the calcification patterns of cold-water corals Madrepora oculata and Lophelia pertusa along contact surfaces with calcified tubes of the symbiotic polychaete Eunice norvegica: Evaluation of a ‘mucus’ calcification hypothesis. Deep Sea Res. Part I 127, 90–104. https://doi.org/10.1016/j.dsr.2017.08.006 (2017).
Mueller, C. E., Lundälv, T., Middelburg, J. J. & van Oevelen, D. The symbiosis between Lophelia pertusa and Eunice norvegica stimulates coral calcification and worm assimilation. PLoS ONE 8, e58660. https://doi.org/10.1371/journal.pone.0058660 (2013).
Miller, R. J., Page, H. M. & Brzezinski, M. A. δ13C and δ15N of particulate organic matter in the Santa Barbara Channel: Drivers and implications for trophic inference. Mar. Ecol. Prog. Ser. 474, 53–66. https://doi.org/10.3354/meps10098 (2013).
Gale, K. S. P., Hamel, J.-F. & Mercier, A. Trophic ecology of deep-sea Asteroidea (Echinodermata) from eastern Canada. Deep Sea Res. Part I 80, 25–36. https://doi.org/10.1016/j.dsr.2013.05.016 (2013).
Michel, L. N., David, B., Dubois, P., Lepoint, G. & de Ridder, C. Trophic plasticity of Antarctic echinoids under contrasted environmental conditions. Polar Biol. 39, 913–923. https://doi.org/10.1007/s00300-015-1873-y (2016).
Jacob, U., Mintenbeck, K., Brey, T., Knust, R. & Beyer, K. Stable isotope food web studies: A case for standardized sample treatment. Mar. Ecol. Prog. Ser. 287, 251–253. https://doi.org/10.3354/meps287251 (2005).
Jacob, U. et al. Towards the trophic structure of the Bouvet Island marine ecosystem. Polar Biol. 29, 106–113. https://doi.org/10.1007/s00300-005-0071-8 (2006).
Bergmann, M., Dannheim, J., Bauerfeind, E. & Klages, M. Trophic relationships along a bathymetric gradient at the deep-sea observatory HAUSGARTEN. Deep Sea Res. Part I 56, 408–424. https://doi.org/10.1016/j.dsr.2008.10.004 (2009).
Parzanini, C., Parrish, C. C., Hamel, J.-F. & Mercier, A. Trophic relationships of deep-sea benthic invertebrates on a continental margin in the NW Atlantic inferred by stable isotope, elemental, and fatty acid composition. Prog. Oceanogr. 168, 279–295. https://doi.org/10.1016/j.pocean.2018.10.007 (2018).
Bo, M., Canese, S. & Bavestrello, G. On the coral-feeding habit of the sea star Peltaster placenta. Mar. Biodivers. 49, 2009–2012. https://doi.org/10.1007/s12526-018-0931-4 (2019).
Rix, L. et al. Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems. Sci. Rep. 6, 1–11. https://doi.org/10.1038/srep18715 (2016).
Bart, M. C., Hudspith, M., Rapp, H. T., Verdonschot, P. F. M. & de Goeij, J. M. A deep-sea sponge loop? Sponges transfer dissolved and particulate organic carbon and nitrogen to associated fauna. Front. Mar. Sci. 8, 229. https://doi.org/10.3389/fmars.2021.604879 (2021).
Borisova, E. A. et al. Ecotype and geographical variation in carbon and nitrogen stable isotope values in western North Pacific killer whales (Orcinus orca). Mar. Mamm. Sci. 36, 925–938. https://doi.org/10.1111/mms.12688 (2020).
Pethybridge, H. et al. A global meta-analysis of marine predator nitrogen stable isotopes: Relationships between trophic structure and environmental conditions. Glob. Ecol. Biogeogr. 27, 1043–1055. https://doi.org/10.1111/geb.12763 (2018).
Bart, M. C. et al. Differential processing of dissolved and particulate organic matter by deep-sea sponges and their microbial symbionts. Sci. Rep. 10, 1–13. https://doi.org/10.1038/s41598-020-74670-0 (2020).
Pile, A. J. & Young, C. M. The natural diet of a hexactinellid sponge: Benthic–pelagic coupling in a deep-sea microbial food web. Deep Sea Res. Part I 53, 1148–1156. https://doi.org/10.1016/j.dsr.2006.03.008 (2006).
Yahel, G., Whitney, F., Reiswig, H. M., Eerkes-Medrano, D. I. & Leys, S. P. In situ feeding and metabolism of glass sponges (Hexactinellida, Porifera) studied in a deep temperate fjord with a remotely operated submersible. Limnol. Oceanogr. 52, 428–440. https://doi.org/10.4319/lo.2007.52.1.0428 (2007).
Robertson, L. M., Hamel, J. F. & Mercier, A. Feeding in deep-sea demosponges: Influence of abiotic and biotic factors. Deep Sea Res. Part I 127, 49–56. https://doi.org/10.1016/j.dsr.2017.07.006 (2017).
Kahn, A. S., Chu, J. W. F. & Leys, S. P. Trophic ecology of glass sponge reefs in the Strait of Georgia, British Columbia. Sci. Rep. 8, 1–11. https://doi.org/10.1038/s41598-017-19107-x (2018).
Vacelet, J. & Boury-Esnault, N. Carnivorous sponges. Nature 373, 333–335. https://doi.org/10.1038/373333a0 (1995).
Godefroy, N. et al. Sponge digestive system diversity and evolution: Filter feeding to carnivory. Cell Tissue Res. 377, 341–351. https://doi.org/10.1007/s00441-019-03032-8 (2019).
Archer, S. K. et al. Foundation species abundance influences food web topology on glass sponge reefs. Front. Mar. Sci. 7, 799. https://doi.org/10.3389/fmars.2020.549478 (2020).
Morganti, T. M. et al. Giant sponge grounds of Central Arctic seamounts are associated with extinct seep life. Nat. Commun. 13, 1–15. https://doi.org/10.1038/s41467-022-28129-7 (2022).
Mintenbeck, K., Jacob, U., Knust, R., Arntz, W. E. & Brey, T. Depth-dependence in stable isotope ratio δ15N of benthic POM consumers: The role of particle dynamics and organism trophic guild. Deep Sea Res. Part I 54, 1015–1023. https://doi.org/10.1016/j.dsr.2007.03.005 (2007).
Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: From microbes to ecosystems. Microbiome 6, 1–18. https://doi.org/10.1186/s40168-018-0428-1 (2018).
Kalvelage, T. et al. Oxygen sensitivity of anammox and coupled N-cycle processes in oxygen minimum zones. PLoS ONE 6, e29299. https://doi.org/10.1371/journal.pone.0029299 (2011).
Kalvelage, T. et al. Nitrogen cycling driven by organic matter export in the South Pacific oxygen minimum zone. Nat. Geosci. 6, 228–234. https://doi.org/10.1038/ngeo1739 (2013).
de Kluijver, A. et al. Bacterial precursors and unsaturated long-chain fatty acids are biomarkers of North-Atlantic deep-sea demosponges. PLoS ONE 16, e0241095. https://doi.org/10.1371/journal.pone.0241095 (2021).
Busch, K. et al. Biodiversity, environmental drivers, and sustainability of the global deep-sea sponge microbiome. Nat. Commun. 13, 1–16. https://doi.org/10.1038/s41467-022-32684-4 (2022).
Weisz, J. B., Hentschel, U., Lindquist, N. & Martens, C. S. Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar. Biol. 152, 475–483. https://doi.org/10.1007/s00227-007-0708-y (2007).
de Kluijver, A. et al. An integrative model of carbon and nitrogen metabolism in a common deep-sea sponge (Geodia barretti). Front. Mar. Sci. 7, 1131. https://doi.org/10.3389/fmars.2020.596251 (2021).
Kahn, A. S., Yahel, G., Chu, J. W. F., Tunnicliffe, V. & Leys, S. P. Benthic grazing and carbon sequestration by deep-water glass sponge reefs. Limnol. Oceanogr. 60, 78–88. https://doi.org/10.1002/lno.10002 (2015).
Montoya, J. P. Nitrogen stable isotopes in marine environments. Nitrogen Mar. Environ. 2, 1277–1302. https://doi.org/10.1016/b978-0-12-372522-6.00029-3 (2008).
Schläppy, M. L. et al. Evidence of nitrification and denitrification in high and low microbial abundance sponges. Mar. Biol. 157, 593–602. https://doi.org/10.1007/S00227-009-1344-5 (2010).
Hoffmann, F. et al. Complex nitrogen cycling in the sponge Geodia barretti. Environ. Microbiol. 11, 2228–2243. https://doi.org/10.1111/j.1462-2920.2009.01944.x (2009).
Rubin-Blum, M. et al. Fueled by methane: Deep-sea sponges from asphalt seeps gain their nutrition from methane-oxidizing symbionts. ISME J. 13, 1209–1225. https://doi.org/10.1038/s41396-019-0346-7 (2019).
Schuster, A., Strehlow, B. W., Eckford-Soper, L., McAllen, R. & Canfield, D. E. Effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake in Lough Hyne, Ireland. mSphere https://doi.org/10.1128/mSphere.00991-20 (2021).
Kainge, P. et al. Fisheries yields, climate change, and ecosystem-based management of the Benguela Current Large Marine Ecosystem. Environ. Dev. 36, 100567. https://doi.org/10.1016/j.envdev.2020.100567 (2020).
Messié, M. et al. Potential new production estimates in four eastern boundary upwelling ecosystems. Prog. Oceanogr. 83, 151–158. https://doi.org/10.1016/j.pocean.2009.07.018 (2009).
Demarcq, H., Richardson, A. J. & Field, J. G. Generalised model of primary production in the southern Benguela upwelling system. Mar. Ecol. Prog. Ser. 354, 59–74. https://doi.org/10.3354/meps07136 (2008).
Chapman, P. & Shannon, L. V. Seasonality in the oxygen minimum layers at the extremities of the Benguela system. S. Afr. J. Mar. Sci. 5, 85–94. https://doi.org/10.2989/025776187784522162 (1987).
Kopte, R. et al. The Angola Current: Flow and hydrographic characteristics as observed at 11°S. J. Geophys. Res. Oceans 122, 1177–1189. https://doi.org/10.1002/2016JC012374 (2017).
John, H. C. et al. Oceanographic and faunistic structures across an Angola Current intrusion into northern Namibian waters. J. Mar. Syst. 46, 1–22. https://doi.org/10.1016/j.jmarsys.2003.11.021 (2004).
Stramma, L. & England, M. On the water masses and mean circulation of the South Atlantic Ocean. J. Geophys. Res. Oceans 104, 20863–20883. https://doi.org/10.1029/1999jc900139 (1999).
Wefing, A. M. et al. High precision U-series dating of scleractinian cold-water corals using an automated chromatographic U and Th extraction. Chem. Geol. 475, 140–148. https://doi.org/10.1016/j.chemgeo.2017.10.036 (2017).
Carabel, S., Godínez-Domínguez, E., Verísimo, P., Fernández, L. & Freire, J. An assessment of sample processing methods for stable isotope analyses of marine food webs. J. Exp. Mar. Biol. Ecol. 336, 254–261. https://doi.org/10.1016/j.jembe.2006.06.001 (2006).
Nyssen, F. et al. A stable isotope approach to the eastern Weddell Sea trophic web: Focus on benthic amphipods. Polar Biol. 25, 280–287. https://doi.org/10.1007/s00300-001-0340-0 (2002).
Quiroga, E., Gerdes, D., Montiel, A., Knust, R. & Jacob, U. Normalized biomass size spectra in high Antarctic macrobenthic communities: Linking trophic position and body size. Mar. Ecol. Prog. Ser. 506, 99–113. https://doi.org/10.3354/meps10807 (2014).
Kassambara, A. & Mundt, F. Extract and visualize the results of multivariate data analyses. R Package Version 1.0. 5. R package version (2020).
Team, Rs. RStudio: Integrated Development for R. (RStudio, Inc., 2022) http://www.rstudio.com.
Team, R. C. R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, 2022). http://www.R-project.org/.
Charrad, M., Ghazzali, N., Boiteau, V. & Niknafs, A. NbClust: An R package for determining the relevant number of clusters in a data set. J. Stat. Softw. 61, 1–36. https://doi.org/10.18637/jss.v061.i06 (2014).
Vinha, B. et al. Carbon and nitrogen stable isotopes of benthic megafauna on the angolan cold-water coral reefs (SE Atlantic). PANGAEA. https://doi.org/10.1594/PANGAEA.955091 (2023).
GEBCO Compilation Group. GEBCO_2022 Grid. (2022).
Hebbeln, D. et al. Multibeam Bathymetry Raw Data (Kongsberg EM710 Entire Dataset) of RV METEOR During Cruise M122. https://doi.org/10.1594/PANGAEA.945015 (2022).
Acknowledgements
We wish to express our sincere gratitude to the crew and scientific team aboard the RV Meteor cruise M122 for their on-board assistance. We would like to thank the German Science Foundation (DFG) for enabling the RV Meteor cruise M122 and for funding the application of the MARUM ROV SQUID. The research included in this manuscript received funding from the European Union’s Horizon 2020 iAtlantic project (Grant Agreement No. 818123). This manuscript reflects the authors’ view alone, and the European Union cannot be held responsible for any use that may be made of the information contained herein. This research received further support from the Cluster of Excellence “The Ocean Floor—Earth’s Uncharted Interface” (Germany’s Excellence Strategy—EXC-2077-390741603 of the DFG) (DH, CW, JT, AF). BV’s PhD research is funded by POR Puglia FESR FSE 2014-2020. VH is funded by NERC Grant No NE/R015953/1 (CLASS). Further support was provided to S.R. and S.P. by the EU project number 101060072 “ACTNOW—Advancing understanding of Cumulative Impacts on European marine biodiversity, ecosystem functions and services for human wellbeing”. BV, CO and VH enjoyed a Fellowship from the Hanse-Wissenschaftskolleg Institute for Advanced Study during the final preparation stages of this manuscript.
Author information
Authors and Affiliations
Contributions
B.V., S.R., A.G., S.P., C.O. and V.H. conceived the scope of the manuscript. D.H. was the chief scientist of the M122 ANNA expedition and A.G., C.O., F.M., C.W., J.T. and A.F. collected, processed and identified samples on board. B.V. and A.P. prepared and analyzed faunal samples with G.E. D.B. providing the lab technical facilities and U.H. and F.M. prepared and analyzed POM samples. B.V. analyzed the results and wrote the manuscript. All authors discussed the results and reviewed the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Vinha, B., Rossi, S., Gori, A. et al. Trophic ecology of Angolan cold-water coral reefs (SE Atlantic) based on stable isotope analyses. Sci Rep 13, 9933 (2023). https://doi.org/10.1038/s41598-023-37035-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-023-37035-x
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.