From principles to practice: a spatial approach to systematic conservation planning in the deep sea

Increases in the demand and price for industrial metals, combined with advances in technological capabilities have now made deep-sea mining more feasible and economically viable. In order to balance economic interests with the conservation of abyssal plain ecosystems, it is becoming increasingly important to develop a systematic approach to spatial management and zoning of the deep sea. Here, we describe an expert-driven systematic conservation planning process applied to inform science-based recommendations to the International Seabed Authority for a system of deep-sea marine protected areas (MPAs) to safeguard biodiversity and ecosystem function in an abyssal Pacific region targeted for nodule mining (e.g. the Clarion–Clipperton fracture zone, CCZ). Our use of geospatial analysis and expert opinion in forming the recommendations allowed us to stratify the proposed network by biophysical gradients, maximize the number of biologically unique seamounts within each subregion, and minimize socioeconomic impacts. The resulting proposal for an MPA network (nine replicate 400 × 400 km MPAs) covers 24% (1 440 000 km²) of the total CCZ planning region and serves as example of swift and pre-emptive conservation planning across an unprecedented area in the deep sea. As pressure from resource extraction increases in the future, the scientific guiding principles outlined in this research can serve as a basis for collaborative international approaches to ocean management.     

Patterns in species richness, size, and latitudinal range of East Atlantic fishes

Examination of latitudinal patterns in species richness, size, and distributional range of East Atlantic fish, based on a compilation of data encompassing the full latitudinal and depth distribution of 1746 East Atlantic fish species, showed that species richness declined towards higher latitudes at a rate of c 1 % of the number of species present, in five-degree bands, for each degree of latitude for both teleosts and elasmobranchs, regardless of habitat However, the latitudinal patterns in maximum fish size and latitudinal range differed between teleosts and elasmobranchs, and changed with habitat No clear evidence was obtained that the latitudinal range occupied increased with latitude, indicating that Rapoport's rule does not apply to E Atlantic fishes Rather, the latitudinal patterns in species richness, size, and distributional range of benthic Atlantic fish were depth-dependent, because species richness, average maximum size, and the average latitudinal range increased with depth and declined with latitude The importance of accounting for this depth-latitude covariation in the distribution of marine fish demonstrated here, together with recent evidence obtained for deep-sea benthic macrofauna, points to depth and latitude as the main factors in the distribution of marine animals     

Southern Ocean deep-sea isopod species richness (Crustacea, Malacostraca): influences of depth, latitude and longitude

We examined deep-sea epibenthic sledge isopod data from the Atlantic sector of the Southern Ocean (SO) (depth range=742–5,191 m). Samples were taken during the expeditions EASIZ II (ANT XV-3) in 1998 and ANDEEP I and II (ANT XIX3/4) in 2002. A total of 471 isopod species were recorded from 28 sites. The species richness of the epibenthic sledge samples was highly variable (6–82 species). Species richness was highest at site 131-3 in 3,053 m depth in the north-eastern Weddell Sea. The highest numbers of species were sampled in the middle depth range and lower species richness was found in the shallower and deeper parts of the study area. Depth is suggested to explain isopod species richness better than both latitude and longitude. Between 58°S and 65°S, the number of species ranged from 9 to 82 (mean=35.9). Further south in the Weddell Sea, between 73°S and 74°S, species richness was lower and the number of species ranged from 6 to 35 (mean=19.2). With regard to longitude, the highest species richness (up to 82 species) was found between 50°W and 60°W in the area of the South Shetland Islands and around the Antarctic Peninsula, while numbers did not exceed 50 species in the eastern Weddell Sea. The haul length, ranging from 807 to 6,464 m, was positively correlated with depth; however, there was no linear relationship between haul length and species richness. We therefore suggest that depth was the most important factor explaining isopod species richness. However, only 28 sites were visited and the statistical power is thus limited. Sampling in the deep sea is expensive and time consuming and as yet this is the best isopod data set available from the Atlantic sector of the SO. Future expeditions are therefore important to better explain the current patterns of benthic diversity in Antarctica.     

Diversity of isopods (Crustacea): new data from the Arctic and Atlantic Oceans

New data on the diversity pattern of isopods (Crustacea) from the northern most part of the North Atlantic and the Arctic Oceans is presented. The pattern of diversity with depth is similar at depths <1000m, but differs considerably below about 1000m. In the Arctic the diversity of isopods (expressed both as numbers of species per sled and expected number of species) increased with increased depth to a maximum at depths of about 320 to 1100m, but then declined towards deeper waters. There was a significant increase in numbers per sled and in the expected number of species with increased depth in the northernmost part of the North Atlantic Ocean. Additionally, changes occurred in the relative composition of the shallow and deep water fauna, with asellote isopods being relatively larger part of the isopod fauna in the Arctic than in the northern most part of the North Atlantic. This indicates major faunistic changes occurring at the Greenland-Iceland-Faeroe Ridge, possibly caused by rapid changes in the temperature. Furthermore, that the low diversity of the Arctic deep-sea is a regional phenomenon, and not a part of a large scale latitudinal pattern in the North Atlantic.     

Benthic colonization and succession on temperate sublittoral rocky cliffs

Patterns of benthic colonization and succession were investigated on a temperate rocky cliff (Aegean Sea, Eastern Mediterranean). Cement and ceramic panels deployed on the rocky substratum at 25-30 m depth were sampled every 3 months over a 2-year period yielding 28 floral and 156 animal species. Diversity, cover and abundance had low values at short immersion periods and increased at the long ones. The vagile fauna responded to the increasing habitat complexity offered by the development of algal turfs and sessile species, and the community structure remained highly dynamic. Unlike the duration of immersion, the type of substratum didn't affect species colonization except for decapods that showed a preference for cement panels. Three to four stages of succession were recorded over immersion periods, according to vagile and sessile biota, respectively, during which species richness and abundance increased. The structure of the developed communities on both artificial materials differed from the natural algal-dominated benthic community of the same area, suggesting that the recovery of rocky shore communities on temperate cliffs is time consuming.     

Diversity and species distribution of polychaetes,isopods and bivalves in the Atlantic sector of the deep Southern Ocean

We examined deep-sea benthic data on polychaetes, isopods and bivalves from the Atlantic sector of the Southern Ocean. Samples were taken during the expeditions EASIZ II (1998), ANDEEP I and II (2002) (depth: 742–6,348 m). The range between sites varies from 3 to 1,900 km. Polychaetes (175 species in total) and isopods (383 species) had a high proportion of species restricted to one or two sites (72 and 70%, respectively). Bivalves (46 species) had a higher proportion of species represented at more sites. Beta diversity (Whittaker and Jaccard) was higher for polychaetes and isopods than for bivalves. The impact of depth on species richness was not consistent among groups; polychaetes showed a negative relationship to depth, isopods displayed highest richness in the middle depth range (2,000–4,000 m), whereas bivalves showed no clear relationship to depth. Species richness was not related to latitude (58–74°S) or longitude (22–60°W) for any group.     

The effect of substratum type,orientation and depth on the development of bacterial deep-sea biofilm communities grown on artificial substrata deployed in the Eastern Mediterranean

An increasing number of deep-sea studies have highlighted the importance of deep-sea biofouling, especially in relation to the protection of deep-sea instruments. In this study, the microbial communities developed on different substrata (titanium, aluminum, limestone, shale and neutrino telescope glass) exposed for 155 days at different depths (1500 m, 2500 m, 3500 m and 4500 m) and positions (vertical and horizontal) in the Eastern Mediterranean Deep Sea were compared. Replicated biofilm samples were analyzed using a Terminal Restriction Fragment Length Polymorphisms (T-RFLP) method. The restriction enzymes CfoI and RsaI produced similar total numbers (94, 93) of different T-RFLP peaks (T-RFs) along the vertical transect. In contrast, the mean total T-RF number between each sample according to substratum type and depth was higher in more samples when CfoI was used. The total species richness (S) of the bacterial communities differed significantly between the substrata, and depended on the orientation of each substratum within one depth and throughout the water column (ANOVA). T-RFLP analyses using the Jaccard similarity index showed that within one depth layer, the composition of microbial communities on different substrata was different and highly altered among communities developed on the same substratum but exposed to fouling at different depths. Based on Multidimensional Scaling Analyses (MDS), the study suggests that depth plays an important role in the composition of deep-sea biofouling communities, while substratum type and orientation of substrata throughout the water column are less important. To the authors’ knowledge, this is the first study of biofilm development in deep waters, in relation to the effects of substratum type, orientation and depth.     

Regional patterns of nematode assemblages in the Arctic deep seas

Surface primary productivity and carbon flux in the Arctic Seas are higher along the warm Spitsbergen Water Current than along the ice-infested East Greenland Current. These contrasting oceanographic conditions are reflected in the deep-sea environment and may shape nematode assemblages. However, the paucity of samples in the Arctic deep seas precludes any regional scale assessment. In the present study, nematode assemblages were investigated in relation to a range of environmental variables along the 2,000 m isobath between latitudes 72°N and 79°N for both East and Western margins of the northern North Atlantic. Results showed that both margins had distinct environmental characteristics, with respect to chloroplastic pigments, sediment water content, sediment-bound organic matter, phospholipids and particulate proteins. Nematode assemblages varied according to these environmental changes. Along the more oligotrophic western margin, chloroplastic pigments increased towards the North, while the other environmental variables, nematode abundances and species richness decreased. In contrast, along the eastern margin, we observed higher quantities of organic matter and particulate protein, which supported higher abundance and species richness. Nematode assemblages along both margins varied according to food availability with species composition more variable in areas with lower amounts. Seventy percent of the species occurred in both margins indicating a low turnover of species. The present results support the hypothesis of a positive latitudinal gradient across the North Atlantic and further suggest that contemporary climate and recent ecological processes may predict nematode diversity patterns at larger scales.     

The effect of substratum type, orientation and depth on the development of bacterial deep-sea biofilm communities grown on artificial substrata deployed in the Eastern Mediterranean

An increasing number of deep-sea studies have highlighted the importance of deep-sea biofouling, especially in relation to the protection of deep-sea instruments. In this study, the microbial communities developed on different substrata (titanium, aluminum, limestone, shale and neutrino telescope glass) exposed for 155 days at different depths (1500?m, 2500?m, 3500?m and 4500 m) and positions (vertical and horizontal) in the Eastern Mediterranean Deep Sea were compared. Replicated biofilm samples were analyzed using a Terminal Restriction Fragment Length Polymorphisms (T-RFLP) method. The restriction enzymes CfoI and RsaI produced similar total numbers (94, 93) of different T-RFLP peaks (T-RFs) along the vertical transect. In contrast, the mean total T-RF number between each sample according to substratum type and depth was higher in more samples when CfoI was used. The total species richness (S) of the bacterial communities differed significantly between the substrata, and depended on the orientation of each substratum within one depth and throughout the water column (ANOVA). T-RFLP analyses using the Jaccard similarity index showed that within one depth layer, the composition of microbial communities on different substrata was different and highly altered among communities developed on the same substratum but exposed to fouling at different depths. Based on Multidimensional Scaling Analyses (MDS), the study suggests that depth plays an important role in the composition of deep-sea biofouling communities, while substratum type and orientation of substrata throughout the water column are less important. To the authors' knowledge, this is the first study of biofilm development in deep waters, in relation to the effects of substratum type, orientation and depth.     

Bathymetric distribution and diversity of deep water polychaetous annelids in the Sigsbee Basin, northwestern Gulf of Mexico

The deep water polychaete fauna is analyzed in this study particularly regarding its composition and variations with depth in the Sigsbee Basin, northwestern region of the Gulf of Mexico. Samples were taken at 10 stations along a bathymetric gradient with depth ranges from 200 to 3760 m with a USNEL (0.25 m²) corer. A total of 287 individuals were identified, from 21 families and 65 species. The most important families, both in terms of abundance and species richness, were: Paraonidae (65.4 ind./0.25 m², 9 spp.), Cirratulidae (28.93 ind./0.25 m², 7 spp.) and Spionidae (18.07 ind./0.25 m², 7 spp.). In general, density tended to decrease with depth with minima at around 2000 m, although two abundance peaks were detected at 3700 and 3760 m, making the pattern seem an inverted parabolic curve. The Shannon-Wiener diversity values varied from 0.54–0.92 at around 2000 m to 3.39 at 3620 m and 3.34 at 3760 m. These results contrast with what is already reported from the North Atlantic and the Tropical Pacific deep benthic communities, where highest diversities are found at 2000 m. Faunal changes evaluated through Beta Diversity (0.08–0.1) and the low similarity found between the stations, emphasized the high variability in the composition of the fauna in the Sigsee Basin, meaning that the faunal composition is practically different at all the sampling stations. Ten species are newly recorded for the Mexican fauna.     

Basing conservation policies for the deep-sea floor on current-diversity concepts: a consideration of rarity

Exploitation of deep-sea resources is now underway and there is economic pressure to renew and expand currently restricted waste disposal in that environment. Since the deep sea is noted for very high species diversity, it is appropriate that diversity conservation be initiated. Review of current concepts of diversity maintenance finds that the ideas have evolved more through increasing information about sources of heterogeneity than through rigorous testing. This history weakens the immediate value of these concepts for the development of conservation strategies and demonstrates the need for additional investigation. Such inquiry might focus upon the rare component of overall species richness. A comparison of box core samples at 2100m in the western Atlantic and the Gulf of Mexico continental shelf reveals that deep soft bottoms are not unique in having many rare species. The rare component at depth is largely comprised of species more common at other locations near and far. The rare component on the shelf is comprised mostly of species which are consistently rare and restricted in distribution. These observations suggest a shallow–deep difference that is more one of degree than fundamental in nature; the deep having larger regions and regional species pools.     

Ocean basin and depth variability of oxygen isotopes in cenozoic benthic foraminifera

One of the longest, most detailed quantitative records of oceanographic change in the Cenozoic is that provided by oxygen isotope measurements made on the tests of foraminifera. As indicated by measurements on benthic foraminifera, the deep waters of the world ocean have undergone an overall cooling of about 10°C in the Cenozoic. This change has been neither monotonic nor gradual. Rather, it is evidenced by a few, relatively rapid increases in the ¹³O content of the benthic shells. These “steps” in the isotopic record have been associated with major evolutionary changes in the mean state of the deep ocean. The variance around this mean state has also changed through the Cenozoic. From relatively high variance in the Middle Eocene, the oceans showed low variance in the Late Eocene and Oligocene. In the Miocene the variance of the isotopic measurement again increased, reaching a maximum of short duration in the Middle Miocene. This maximum as well as that which occurred during the Late Pliocene and Quaternary, may be attributable to fluctuations in the isotopic composition of the oceans caused by growth and decay of large ice sheets.In the Late Miocene the benthic oxygen isotopes in Atlantic sites less than 3000 m deep have a higher variance than sites at similar depths in the Pacific and Indian Oceans. It is thought that this high variance results from long-term changes in the importance of the cool and salty North Atlantic Deep Water relative to that of the warmer and less saline Antarctic Intermediate Water at Atlantic sites between 1000 m and 3000 m water depth. Such significant differences in benthic isotopic variance between the ocean basins have been demonstrated only in post-Middle Miocene intervals.     

Biodiversity of peracarid crustaceans(Malacostraca) from the shelf downto the deep Arctic Ocean

During three expeditions with the RVs Meteor and Polarstern more than sixty thousand peracarids were sampled from the deep Arctic Ocean (northern North Atlantic) by means of an epibenthic sledge. Sampling areas were the Kolbeinsey Ridge north of Iceland (800–1100 m), the Northeast Water Polynya, off Greenland (45–517m), and 75°N east of Greenland (197–2681m). Until now 288 species of Peracarida have been identified to species level. These 288 species comprise 152 genera and 59 families of Amphipoda, Cumacea, Isopoda, Mysidacea and Tanaidacea. Thirty-eight genera were very frequent and were sampled at each expedition (these were 22 species of Isopoda, seven species of Cumacea, three species of Amphipoda and Mysidacea, each, and two species of Tanaidacea). Sixty genera are eurybathic, occurring at least over a depth range of 1000m, some even from the shelf up to 2681m depth. Only 10 genera are stenobathic, occurring only in the deep sea. No significant decrease in species number with depth or latitude could be observed. The influencing factors probably causing different community structures are diverse, ranging from food availability over substrate or hydrographical qualities to interspecific competition.     

Viral Abundance, Decay, and Diversity in the Meso- and Bathypelagic Waters of the North Atlantic

To elucidate the potential importance of deep-water viruses in controlling the meso- and bathypelagic picoplankton community, the abundance, decay rate, and diversity of the virioplankton community were determined in the meso- and bathypelagic water masses of the eastern part of the subtropical North Atlantic. Viral abundance averaged 1.4 × 10⁶ ml⁻¹ at around 100 m of depth and decreased only by a factor of 2 at 3,000 to 4,000 m of depth. In contrast, picoplankton abundance decreased by 1 order of magnitude to the Lower Deep Water (LDW; 3,500- to 5,000-m depth). The virus-to-picoplankton ratio increased from 9 at about 100 m of depth to 110 in the LDW. Mean viral decay rates were 3.5 × 10⁻³ h⁻¹ between 900 m and 2,750 m and 1.1 × 10⁻³ h⁻¹ at 4,000 m of depth, corresponding to viral turnover times of 11 and 39 days, respectively. Pulsed-field gel electrophoresis fingerprints obtained from the viral community between 2,400 m and 4,000 m of depth revealed a maximum of only four bands from 4,000 m of depth. Based on the high viral abundance and the low picoplankton production determined via leucine incorporation, we conclude that the viral production calculated from the viral decay is insufficient to maintain the high viral abundance in the deep North Atlantic. Rather, we propose that substantial allochthonous viral input or lysogenic or pseudolysogenic production is required to maintain the high viral abundance detected in the meso- and bathypelagic North Atlantic. Consequently, deep-water prokaryotes are apparently far less controlled in their abundance and taxon richness by lytic prokaryotic phages than the high viral abundance and the virus-to-picoplankton ratio would suggest.     

A benthic foraminiferal record of middle to late Pliocene (3.15-2.85 Ma) deep water change in the North Atlantic

Records of benthic foraminifera from North Atlantic DSDP Site 607 and Hole 610A indicate changes in deep water conditions through the middle to late Pliocene (3.15 to 2.85 Ma). Quantitative analyses of modern associations in the North Atlantic indicate that seven species, Fontbotia wuellerstorfi, Cibicidoides kullenbergi, Uvigerina peregrina, Nuttallides umboniferus, Melonis pompilioides, Globocassidulina subglobosa and Epistominella exigua are useful for paleoenvironmental interpretation. The western North Atlantic basin (Site 607) was occupied by North Atlantic Deep Water (NADW) until ~2.88 Ma. At that time, N. umboniferus increased, indicating an influx of Southern Ocean Water (SOW). The eastern North Atlantic basin (Hole 610A) was occupied by a relatively warm water mass, possibly Northeastern Atlantic Deep Water (NEADW), through ~2.94 Ma when SOW more strongly influenced the site. These interpretations are consistent with benthic δ¹⁸O and δ¹³C records from 607 and 610A (Raymo et al., 1992). The results presented in this paper suggest that the North Atlantic was strongly influenced by northern component deep water circulation until 2.90–2.95 Ma. After that there was a transition toward a glacially driven North Atlantic circulation more strongly influenced by SOW associated with the onset of Northern Hemisphere glaciation. The circulation change follows the last significant SST and atmospheric warming prior to ~2.6 Ma.     

Large-Scale Geographic Variation in Distribution and Abundance of Australian Deep-Water Kelp Forests

Despite the significance of marine habitat-forming organisms, little is known about their large-scale distribution and abundance in deeper waters, where they are difficult to access. Such information is necessary to develop sound conservation and management strategies. Kelps are main habitat-formers in temperate reefs worldwide; however, these habitats are highly sensitive to environmental change. The kelp Ecklonia radiate is the major habitat-forming organism on subtidal reefs in temperate Australia. Here, we provide large-scale ecological data encompassing the latitudinal distribution along the continent of these kelp forests, which is a necessary first step towards quantitative inferences about the effects of climatic change and other stressors on these valuable habitats. We used the Autonomous Underwater Vehicle (AUV) facility of Australia’s Integrated Marine Observing System (IMOS) to survey 157,000 m² of seabed, of which ca 13,000 m² were used to quantify kelp covers at multiple spatial scales (10–100 m to 100–1,000 km) and depths (15–60 m) across several regions ca 2–6° latitude apart along the East and West coast of Australia. We investigated the large-scale geographic variation in distribution and abundance of deep-water kelp (>15 m depth) and their relationships with physical variables. Kelp cover generally increased with latitude despite great variability at smaller spatial scales. Maximum depth of kelp occurrence was 40–50 m. Kelp latitudinal distribution along the continent was most strongly related to water temperature and substratum availability. This extensive survey data, coupled with ongoing AUV missions, will allow for the detection of long-term shifts in the distribution and abundance of habitat-forming kelp and the organisms they support on a continental scale, and provide information necessary for successful implementation and management of conservation reserves.     

Deep-Sea Biodiversity in the Mediterranean Sea: The Known,the Unknown,and the Unknowable

Deep-sea ecosystems represent the largest biome of the global biosphere, but knowledge of their biodiversity is still scant. The Mediterranean basin has been proposed as a hot spot of terrestrial and coastal marine biodiversity but has been supposed to be impoverished of deep-sea species richness. We summarized all available information on benthic biodiversity (Prokaryotes, Foraminifera, Meiofauna, Macrofauna, and Megafauna) in different deep-sea ecosystems of the Mediterranean Sea (200 to more than 4,000 m depth), including open slopes, deep basins, canyons, cold seeps, seamounts, deep-water corals and deep-hypersaline anoxic basins and analyzed overall longitudinal and bathymetric patterns. We show that in contrast to what was expected from the sharp decrease in organic carbon fluxes and reduced faunal abundance, the deep-sea biodiversity of both the eastern and the western basins of the Mediterranean Sea is similarly high. All of the biodiversity components, except Bacteria and Archaea, displayed a decreasing pattern with increasing water depth, but to a different extent for each component. Unlike patterns observed for faunal abundance, highest negative values of the slopes of the biodiversity patterns were observed for Meiofauna, followed by Macrofauna and Megafauna. Comparison of the biodiversity associated with open slopes, deep basins, canyons, and deep-water corals showed that the deep basins were the least diverse. Rarefaction curves allowed us to estimate the expected number of species for each benthic component in different bathymetric ranges. A large fraction of exclusive species was associated with each specific habitat or ecosystem. Thus, each deep-sea ecosystem contributes significantly to overall biodiversity. From theoretical extrapolations we estimate that the overall deep-sea Mediterranean biodiversity (excluding prokaryotes) reaches approximately 2805 species of which about 66% is still undiscovered. Among the biotic components investigated (Prokaryotes excluded), most of the unknown species are within the phylum Nematoda, followed by Foraminifera, but an important fraction of macrofaunal and megafaunal species also remains unknown. Data reported here provide new insights into the patterns of biodiversity in the deep-sea Mediterranean and new clues for future investigations aimed at identifying the factors controlling and threatening deep-sea biodiversity.     

The energy–diversity relationship of complex bacterial communities in Arctic deep-sea sediments

The availability of nutrients and energy is a main driver of biodiversity for plant and animal communities in terrestrial and marine ecosystems, but we are only beginning to understand whether and how energy–diversity relationships may be extended to complex natural bacterial communities. Here, we analyzed the link between phytodetritus input, diversity and activity of bacterial communities of the Siberian continental margin (37–3427 m water depth). Community structure and functions, such as enzymatic activity, oxygen consumption and carbon remineralization rates, were highly related to each other, and with energy availability. Bacterial richness substantially increased with increasing sediment pigment content, suggesting a positive energy–diversity relationship in oligotrophic regions. Richness leveled off, forming a plateau, when mesotrophic sites were included, suggesting that bacterial communities and other benthic fauna may be structured by similar mechanisms. Dominant bacterial taxa showed strong positive or negative relationships with phytodetritus input and allowed us to identify candidate bioindicator taxa. Contrasting responses of individual taxa to changes in phytodetritus input also suggest varying ecological strategies among bacterial groups along the energy gradient. Our results imply that environmental changes affecting primary productivity and particle export from the surface ocean will not only affect bacterial community structure but also bacterial functions in Arctic deep-sea sediment, and that sediment bacterial communities can record shifts in the whole ocean ecosystem functioning.