ALBERT

Description: The original version of the Description of Additional Supplementary Files associated with this Article contained errors in the legends of Supplementary Data 5–8 and omitted legends for the Source Data. The HTML has been updated to include a corrected version of the Description of Additional Supplementary Files; the original incorrect version of this file can be found as Supplementary Information associated with this Correction.

Description: © The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Howell, K. L., Hilario, A., Allcock, A. L., Bailey, D. M., Baker, M., Clark, M. R., Colaco, A., Copley, J., Cordes, E. E., Danovaro, R., Dissanayake, A., Escobar, E., Esquete, P., Gallagher, A. J., Gates, A. R., Gaudron, S. M., German, C. R., Gjerde, K. M., Higgs, N. D., Le Bris, N., Levin, L. A., Manea, E., McClain, C., Menot, L., Mestre, N. C., Metaxas, A., Milligan, R. J., Muthumbi, A. W. N., Narayanaswamy, B. E., Ramalho, S. P., Ramirez-Llodra, E., Robson, L. M., Rogers, A. D., Sellanes, J., Sigwart, J. D., Sink, K., Snelgrove, P. V. R., Stefanoudis, P., V., Sumida, P. Y., Taylor, M. L., Thurber, A. R., Vieira, R. P., Watanabe, H. K., Woodall, L. C., & Xavier, J. R. A blueprint for an inclusive, global deep-sea ocean decade field program. Frontiers in Marine Science, 7, (2020): 584861, doi:10.3389/fmars.2020.584861.

Description: The ocean plays a crucial role in the functioning of the Earth System and in the provision of vital goods and services. The United Nations (UN) declared 2021–2030 as the UN Decade of Ocean Science for Sustainable Development. The Roadmap for the Ocean Decade aims to achieve six critical societal outcomes (SOs) by 2030, through the pursuit of four objectives (Os). It specifically recognizes the scarcity of biological data for deep-sea biomes, and challenges the global scientific community to conduct research to advance understanding of deep-sea ecosystems to inform sustainable management. In this paper, we map four key scientific questions identified by the academic community to the Ocean Decade SOs: (i) What is the diversity of life in the deep ocean? (ii) How are populations and habitats connected? (iii) What is the role of living organisms in ecosystem function and service provision? and (iv) How do species, communities, and ecosystems respond to disturbance? We then consider the design of a global-scale program to address these questions by reviewing key drivers of ecological pattern and process. We recommend using the following criteria to stratify a global survey design: biogeographic region, depth, horizontal distance, substrate type, high and low climate hazard, fished/unfished, near/far from sources of pollution, licensed/protected from industry activities. We consider both spatial and temporal surveys, and emphasize new biological data collection that prioritizes southern and polar latitudes, deeper (〉 2000 m) depths, and midwater environments. We provide guidance on observational, experimental, and monitoring needs for different benthic and pelagic ecosystems. We then review recent efforts to standardize biological data and specimen collection and archiving, making “sampling design to knowledge application” recommendations in the context of a new global program. We also review and comment on needs, and recommend actions, to develop capacity in deep-sea research; and the role of inclusivity - from accessing indigenous and local knowledge to the sharing of technologies - as part of such a global program. We discuss the concept of a new global deep-sea biological research program ‘Challenger 150,’ highlighting what it could deliver for the Ocean Decade and UN Sustainable Development Goal 14.

Description: Development of this paper was supported by funding from the Scientific Committee on Oceanic Research (SCOR) awarded to KH and AH as working group 159 co-chairs. KH, BN, and KS are supported by the UKRI funded One Ocean Hub NE/S008950/1. AH work is supported by the CESAM (UIDP/50017/2020 + 1432 UIDB/50017/2020) that is funded by Fundação para a Ciência e a Tecnologia (FCT)/MCTES through national funds. AA is supported by Science Foundation Ireland and the Marine Institute under the Investigators Program Grant Number SFI/15/IA/3100 co-funded under the European Regional Development Fund 2014–2020. AC is supported through the FunAzores -ACORES 01-0145-FEDER-000123 grant and by FCT through strategic project UID/05634/2020 and FCT and Direção-Geral de Politica do Mar (DGPM) through the project Mining2/2017/005. PE is funded by national funds (OE), through FCT in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of the article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. SG research is supported by CNRS funds. CG is supported by an Independent Study Award and the Investment in Science Fund at WHOI. KG gratefully acknowledges support from Synchronicity Earth. LL is funded by the NOAA Office of Ocean Exploration and Research (NA19OAR0110305) and the US National Science Foundation (OCE 1634172). NM is supported by FCT and DGPM, through the project Mining2/2017/001 and the FCT grants CEECIND/00526/2017, UIDB/00350/2020 + UIDP/00350/2020. SR is funded by the FCTgrant CEECIND/00758/2017. JS is supported by ANID FONDECYT #1181153 and ANID Millennium Science Initiative Program #NC120030. JX research is funded by the European Union’s Horizon 2020 research and innovation program through the SponGES project (grant agreement no. 679849) and further supported by national funds through FCT within the scope of UIDB/04423/2020 and UIDP/04423/2020. The Natural Sciences and Engineering Council of Canada supports AM and PVRS. MB and the Deep-Ocean Stewardship Initiative are supported by Arcadia - A charitable fund of Lisbet Rausing and Peter Baldwin. BN work is supported by the NERC funded Arctic PRIZE NE/P006302/1.

Description: In the deep ocean symbioses between microbes and invertebrates are emerging as key drivers of ecosystem health and services. We present a large-scale analysis of microbial diversity in deep-sea sponges (Porifera) from scales of sponge individuals to ocean basins, covering 52 locations, 1077 host individuals translating into 169 sponge species (including understudied glass sponges), and 469 reference samples, collected anew during 21 ship-based expeditions. We demonstrate the impacts of the sponge microbial abundance status, geographic distance, sponge phylogeny, and the physical-biogeochemical environment as drivers of microbiome composition, in descending order of relevance. Our study further discloses that fundamental concepts of sponge microbiology apply robustly to sponges from the deep-sea across distances of 〉10,000 km. Deep-sea sponge microbiomes are less complex, yet more heterogeneous, than their shallow-water counterparts. Our analysis underscores the uniqueness of each deep-sea sponge ground based on which we provide critical knowledge for conservation of these vulnerable ecosystems.

Description: Caminella Lendenfeld, 1894 is a poorly known Geodiidae genus with unclear phylogenetic relationships. In order to find new lines of evidence that could shed light on the evolutionary history of Caminella, we decided to revise type material and museum material, as well as examine new material from underwater caves and deep-sea ecosystems. In doing so, we formally show that Isops maculosus Vosmaer, 1894 and Caminella loricata Lendenfeld, 1894 are junior synonyms of Caminella intuta (Topsent, 1892). We discuss different spicule morphological phenotypes in C. intuta, which may be linked to silica availability. We also discovered two new species of deep-sea Caminella: 1) from Cape Verde (Caminella caboverdensis sp. nov.) and 2) from seamounts located south of the Azores archipelago and the North of Spain (Caminella pustula sp. nov.). We reveal that Caminella sterrasters have complex surface microstructures, unique amongst the Geodiidae, where actin tips are linked to each other. Molecular markers (COI, 28S (C1-D2) and 18S) sequenced for some specimens led to new phylogenetic analyses, which continue to suggest a close relationship of Caminella with the Erylinae and Calthropella; these affinities are discussed in light of morphological characters.

Description: The allele matrix contains the genotypes (coded as length of fragments) for 10 microsatellite markers described in Taboada et al. (2015). There are 280 individuals for 10 populations across the Atlanto-Mediterranean distribution of the species.

Description: Emerald Basin on the Scotian Shelf off Nova Scotia, Canada, is home to a globally unique population of the glass sponge Vazella pourtalesi. Through the analysis of both in situ photographs and trawl catch data from annual multispecies bottom-trawl surveys, we examined community composition, species density, and abundance of epibenthos and fish associated with V. pourtalesi compared to locations without this sponge. Using generalized linear models and analysis of similarities, the importance of V. pourtalesi in enhancing species density and abundance of the associated epibenthic community was assessed against that of the hard substrate on which it settles. Our results indicated that the megafaunal assemblage associated with V. pourtalesi was significantly different in composition and higher in species density and abundance compared to locations without V. pourtalesi. Analysis of similarity of trawl catch data indicated that fish communities associated with the sponge grounds are significantly different from those without V. pourtalesi, although no species were found exclusively on the sponge grounds. Our study provides further evidence of the role played by sponge grounds in shaping community structure and biodiversity of associated deep-sea epibenthic and fish communities. The mechanism for biodiversity enhancement within the sponge grounds formed by V. pourtalesi is likely the combined effect of both the sponge itself and its attachment substrate, which together comprise the habitat of the sponge grounds. We also discuss the role of habitat provision between the mixed-species tetractinellid sponges of the Flemish Cap and the monospecific glass sponge grounds of Emerald Basin.

Description: Supplementary Material 1: List of specimens analysed in this study with detailed information of the stations in which they were sampled. All specimens are deposited in the MNHN Paris.

Description: Sponges are commonly known as general nutrient providers for the marine ecosystem, recycling organic matter into various forms of bio-available nutrients such as ammonium and nitrate. In this study we challenge this view. We show that nutrient removal through microbial denitrification is a common feature in six cold-water sponge species from boreal and Arctic sponge grounds. Denitrification rates were quantified by incubating sponge tissue sections with 15NO3- - amended oxygen saturated seawater, mimicking conditions in pumping sponges, and de-oxygenated seawater, mimicking non-pumping sponges. Rates of anaerobic ammonium oxidation (anammox) using incubations with 15NH4+ could not be detected. Denitrification rates of the different sponge species ranged from 0 to 97 nmol N cm-3 sponge day-1 under oxic conditions, and from 24 to 279 nmol N cm-3 sponge day-1 under anoxic conditions. A positive relationship between the highest potential rates of denitrification (in the absence of oxygen) and the species-specific abundances of nirS and nirK genes encoding nitrite reductase, a key enzyme for denitrification, suggests that the denitrifying community in these sponge species is active and prepared for denitrification. The lack of a lag phase in the linear accumulation of the 15N labelled N2 gas in any of our tissue incubations is another indicator for an active community of denitrifiers in the investigated sponge species. Low rates for coupled nitrification-denitrification indicate that also under oxic conditions, nitrate to fuel denitrification rates was derived rather from the ambient sea-water than from sponge nitrification. The lack of nifH genes encoding nitrogenase, the key enzyme for nitrogen fixation, shows that the nitrogen cycle is not closed in the sponge grounds. The denitrified nitrogen, no matter of its origin, is then no longer available as a nutrient for the marine ecosystem. These results reveal the following scenario for the potential denitrification capacity of sponge grounds based on typical sponge biomass on boreal and Arctic sponge grounds:, Areal denitrification rates of 0.6 mmol N m-2 day-1 assuming non-pumping sponges and still 0.3 mmol N m-2 day-1 assuming pumping sponges may be possible. This is well within the range of denitrification rates of continental shelf sediments. For the most densely populated boreal sponge grounds we calculated potential denitrification rates of up to 1,7 mmol N m-2 day-1, which is higher than typical rates in continental shelf sediments. Increased future impact of sponge grounds by anthropogenic stressors reducing sponge pumping activity and further stimulating sponge anaerobic processes may thus lead to that deep-sea sponge grounds change their role in the marine ecosystem from being mainly nutrient sources to becoming mainly nutrient sinks.