Diversity of Abyssal Marine Life
1Brigitte Ebbe, 2David S. M. Billett, 3Angelika Brandt, 4Kari Ellingsen, 5Adrian Glover, 1Stefanie Keller, 6Marina Malyutina, 1Pedro Martínez Arbizu, 7Tina Molodtsova, 8Michael Rex, 9Craig Smith, 10Anastasios Tselepides
1Senckenberg Institute, Deutsches Zentrum für Marine Biodiversitätsforschung, Wilhelmshaven, Germany
2National Oceanography Centre, Southampton, UK
3Zoologisches Museum und Biozentrum Grindel, Hamburg, Germany
4Norwegian Institute for Nature Research, Polar Environment Centre, Tromsø, Norway
5Natural History Museum, London, UK
6A.V. Zhirmunsky Institute of Marine Biology, Vladivostok, Russia
7P.P Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia
8Department of Biology, University of Massachusetts, Boston, Massachusetts, USA
9Marine Sciences Building, University of Hawaii at Manoa, Honolulu, Hawaii, USA
10Thalassocosmos, Heraklion, Crete, Greece
The Census of the Diversity of Abyssal Marine Life (CeDAMar) was devoted to the study of the largest and remotest ecosystem on Earth, the major deep basins stretching between continental margins and the mid-ocean ridge system. Abyssal plains and basins account for about half of Earth's surface (Tyler 2003) and harbor a great variety of life forms. As part of the overall Census of Marine Life, the field project CeDAMar was designed to study the diversity, distribution, and abundance of organisms living in, on, or directly above the seafloor. Prominent features such as ridges, seamounts, trenches, and chemosynthetic environments were covered by other Census projects.
8.2. Abyssal Plains
Until the late nineteenth century, abyssal sediments were believed to be azoic deserts owing to a lack of sunlight and primary production. This view changed dramatically with the British Challenger expedition (1872–1876), which found deep-sea life throughout the world ocean. Modern marine diversity research began in the 1960s when Sanders, Hessler, and co-workers were able to show that the abundance of macrobenthic organisms decreased with depth whereas the number of species increased (Sanders et al. 1965; Hessler & Sanders 1967; Sanders & Hessler 1969). Pivotal in the development of the scientific interest in marine diversity patterns was a study by Grassle & Maciolek (1992) of a series of box corer samples collected along a 176 km transect on the northwest Atlantic continental slope. Species turnover rates along the transect suggested that the number of species at the deep-ocean floor may rival that of tropical rainforests. This study led to broad debate about the number of marine species and the distribution of diversity along bathymetric and latitudinal gradients (Poore & Wilson 1993; Rex et al. 1993, 1997; Thomas & Gooday 1996; Culver & Buzas 2000).
Before the year 2000, biological research in the abyss had been conducted only sporadically as part of the classic worldwide expeditions aboard American, German, Danish, and Swedish vessels around the turn of the century into the mid-1990s. More recently, between 1948 and 2000, the P.P. Shirshov Institute sampled more than 1,700 stations below 3,000 m including abyssal plains, basins, and trenches down to 9,000 m. Studies of abyssal diversity and biogeography were complicated by the logistic challenges of deep-sea exploration. When the first CeDAMar expeditions were planned, the total sampled area of deep-sea floor was equal to no more than a few football fields, and by the year 2005 the total sampled area below 4,000 m amounted to about 1.4 × 10 –9% (Stuart et al. 2008).
8.3. The CeDAMar Rationale
When CeDAMar was initiated, published results suggested that deep-sea sediments supported low biotic abundance and biomass, but potentially high species richness depending on taxon. All expeditions to abyssal plains and basins showed that regardless of the location, roughly 90% of the infaunal species collected in a typical abyssal sample were new to science.
8.3.1. Open Questions in Deep-Sea Research
One fundamental gap in our knowledge of the abyss was the existence of vast geographic areas that had not been sampled, for example, the central Pacific Ocean and oceans of the southern hemisphere, because they were so remote from oceanographic institutions. CeDAMar expeditions were specifically designed to explore both sides of the southern Atlantic, southern Indian Ocean, and the Southern Ocean; the Northeast Atlantic; the central Pacific; and, as an example for a warm, ultra-oligotrophic deep sea, the eastern Mediterranean Sea (Fig. 8.1).
|Figure 8.1 Study areas of CeDAMar. For explanations of project names see sections 8.4.1 through 8.4.8.
The occurrence of high biodiversity in the extreme habitat conditions that characterize the abyss, such as low temperature, very high hydrostatic pressure, little habitat complexity, and extremely low food availability, was perceived to be one of the major biogeographic puzzles of our time. Despite the potential importance of this vast ecosystem as a reservoir for genetic diversity and evolutionary novelty, very little was known about the factors regulating deep-sea species richness (Gage & Tyler 1991; Gray 2002). CeDAMar therefore aimed to collect new reliable data on species assemblages of ocean basins and determine the large-scale distribution of species among these basins. Documentation of the actual species diversity of abyssal plains provided a baseline for global-change research and for a better understanding of historical causes and ecological factors regulating biodiversity.
Even less is known about the biology of abyssal organisms. One of the unanswered questions in this context was the relation between food supply and the number of species present in a given deep-sea area. The deep-sea benthos depends ultimately on surface production that sinks through the water column. Although it seems evident that the biomass of deep-sea organisms should be positively correlated with food availability (Rowe 1971; C.R. Smith et al. 1997; Brown 2001), the productivity–biodiversity relationship is less clear.
8.3.2. Specific CeDAMar Questions
Considering our lack of knowledge, CeDAMar focused research efforts in a way that would produce tangible results within a set timeframe of less than ten years. Deep-sea biologists identified the most urgent questions to be addressed by CeDAMar expeditions, keeping in mind the overarching Census themes of diversity, abundance, and distribution.
184.108.40.206. Questions Concerning Diversity
How does diversity vary at different geographic scales, between different size classes of organisms, and with differences in food supply?
Are there centers of high diversity (hot spots of diversity) in the deep sea?
What is the role of evolutionary-historic processes in determining diversity levels?
How do manganese nodules or drop stones influence benthic diversity?
220.127.116.11. Questions Concerning Abundance
How do organisms of different size classes respond to environmental factors?
What is the relation between food availability and benthic standing stock?
18.104.22.168. Questions Concerning Distribution
Do biogeographic barriers affect the distribution of abyssal fauna? How endemic is the abyssal fauna?
How common are cosmopolitan species in the abyss? Is there gene flow between distant abyssal communities of the same species?
Are there latitudinal gradients in species richness? Is the diversity of a given basin similar to the diversity of basins in other oceans at similar latitudes?
8.4. Finding Answers: Methods and Programs of CeDAMar
The most prominent reason why the abyss has been explored to such a small degree is the difficulty of reaching it. Apart from the scarcity of research vessels, there are many logistic challenges, the time required for sampling great ocean depths not being the least. To lower sampling gear to the seafloor some 4,500 m below the surface and retrieve it back to the ship, several hours are necessary for each single sampling. The control of the actual sampling process on the bottom is limited by the great depth and the amount of wire between ship and gear. The methodology that CeDAMar used was more traditional than hi-tech, consisting of coring devices (box corer and multicorer), epibenthic sledges, Agassiz trawls, and, when possible, a sediment profiling camera with or without a video camera. This set of gear was used in a standardized way to ensure (1) collection of organisms of all size classes from bacteria to large epifauna such as corals, sea anemones, sponges, holothurians, and stalked crinoids, and (2) comparability of results among CeDAMar projects and with the existing literature. The Time Series study of the seafloor in the Porcupine Abyssal Plain used a time-lapse camera and sediment traps to monitor processes on the seafloor.
8.4.1. Project DIVA
DIVA (diversity gradients in the Atlantic) is the seed project of CeDAMar, with the main focus on the question of latitudinal gradients in biodiversity in the southern Atlantic. Sampling locations were the abyssal basins off west Africa from the Cape to the equator and the Argentine and Brazil basins off the east coast of South America.
8.4.2. Project ANDEEP
ANDEEP (Antarctic benthic deep-sea biodiversity – colonization and recent community patterns) was dedicated to the abyssal waters in the Atlantic sector of the Southern Ocean. This region is one of the least investigated and it closed the gap between the two study areas of DIVA. It is also the location closest to the pole and farthest away from the equator, which made it very suitable to prove or disprove that a decline in marine biodiversity is present from the equator to the poles.
8.4.3. Projects KAPLAN and NODINAUT
The study area of KAPLAN and NODINAUT was the manganese nodule field in the Clarion-Clipperton Fracture Zone (CCZ), with the main focus centered on the question of the impact of nodules on biodiversity at different scales. Results were used for recommendations concerning marine protected areas (MPAs) to protect the fauna in case of nodule mining. In light of increasing demand for minerals, deep-sea mining has become a realistic possibility.
8.4.4. Project Biozaire
Biozaire was conducted off West Africa, just inshore of the DIVA area, encompassing the deep slope, abyssal plain, and a chemosynthetic site (a so-called pockmark). The objective was to characterize the “benthic community structure in relation with physical and chemical processes in a region of oil and gas interest” (Sibuet & Vangriesheim 2009).
8.4.5. Project LEVAR
LEVAR (Levantine Basin Biodiversity Variability) was one of the younger projects of CeDAMar, the study area being the eastern Mediterranean Sea with its comparatively shallow abyss (around 3,000 m), warm water at depth, and extremely poor food supply. Stations near Crete were sampled during one cruise. The aim was to determine whether proximity to shore or the depth was more important in influencing community composition and the distributions of abyssal biota.
8.4.6. Project CROZEX
The relation between surface primary production and benthic community composition was also explored during three cruises of the CROZEX (Crozet circulation iron fertilization and export production experiment) expedition off the sub-Antarctic Crozet Islands (Indian Ocean). The background of this study was a proposal put forward by biogeochemists suggesting that natural iron fertilization might enhance algal growth, which would sink to the abyssal seafloor, thus sequestering CO 2 and taking it out of the atmosphere. By observing processes driven by natural fertilization through iron eroded from the islands, CROZEX was designed to assess whether artificial iron fertilization might be a feasible option to fight global warming.
8.4.7. Project Time Series
A time-lapse camera system and moorings including sediment traps have been used to observe the deep ocean floor in the Porcupine Abyssal Plain since 1989, changing our perception of the quiescent, stable abyss to that of a very dynamic environment with sometimes radical changes in communities. One incident, the so-called Amperima Event named after the sea cucumber Amperima rosea, has become famous because of substantial changes in abundance related to changes in food supply.
8.4.8. Project ENAB
Evolution in the deep sea was the focus of ENAB (Evolution in the North Atlantic Basin), with a sampling cruise conducted along the famous Gay Head–Bermuda transect that in the early 1960s had started biodiversity research in the deep sea. The program was dedicated to assessing spatial population genetic structure in deep-sea mollusks to determine patterns of population differentiation, speciation, and phyletic evolution.
8.4.9. CeDAMar Database
One of the legacies that may prove to be highly valuable to deep-sea researchers today and in the future is a freely accessible database that will be maintained and updated beyond the life of CeDAMar. So far, some 12,000 records, representing more than 3,000 species from nearly 4,800 locations distributed in all oceans can be queried. These records are made available to Ocean Biogeographic Information System (see Chapter 17), the database of the Census, from where they can also be accessed by anyone. With a special tool, maps can be created with different resolutions. Figure 8.2 shows the number of abyssal records per area, in this case a grid of 10 degree × 10 degree squares (roughly 100 km × 100 km). There are four areas with relatively extensive sampling on which much of our knowledge of the abyssal fauna is based: (1) the northwest Atlantic off the US east coast sampled in the 1980s, including stations on the continental slope that led to the estimates of deep-sea species richness by Grassle & Maciolek (1992); (2) the manganese nodule area off Peru, where the German DISCOL disturbance experiment was performed in the 1980s and 1990s to assess recovery of abyssal benthic fauna after massive disturbance mimicking possible effects of nodule mining; (3) the Porcupine Abyssal Plain and Gulf of Gascogne where British and French deep-sea investigations were concentrated; and (4) the Kurile–Kamchatka Trench, which was a main study area of Russian deep-sea research. The remaining area of the abyssal plains is still unsampled or poorly sampled, showing that even the substantial effort put into abyssal expeditions during CeDAMar has relatively little effect on sample coverage from a worldwide perspective.
8.4.10. Overcoming the Taxonomic Impediment
As all knowledge about ecosystems is based on knowing the identity of species in a particular system, much effort has been put into overcoming the so-called taxonomic impediment. The term means the general lack of specialists for identification of marine animals. Workshops and short-term stays at participating institutions (taxonomic exchanges) have helped to foster communication and intercalibration of the numerous personal databases from a broad range of projects. For polychaetes, a platform (www.polychaetes.info) was created with the help of the Natural History Museum (London) to exchange information by the Internet on yet unpublished but already well-defined “working species”, allowing specialists to share information on an additional 50–90% of their respective taxa. A more visible outcome for the entire scientific community was CeDAMar's goal to deliver formal descriptions of 500 new abyssal species by the end of the first Census in October 2010. The goal will have been reached by the time this book is published (Fig. 8.3). Nearly half of all newly described or redescribed species are crustaceans (243 species, 91 of which are isopods), followed by nematodes (55 species) and mollusks (41 species, including 32 gastropods).
|Figure 8.3 Newly described species from CeDAMar projects by major taxonomic groups. Names on the columns indicate smaller subgroups.
8.5. Major Results
Through the results generated by the CeDAMar project our perception of the abyss has changed fundamentally. This change in perception may be condensed into two statements which, although they may seem trivial at first glance, are significant changes in how scientists view the abyss: (1) extreme is normal; (2) rare is common.
8.5.1. Extreme Is Normal
Quite surprisingly, scientists even in the twentieth century viewed remote habitats on Earth from an anthropocentric perspective. The richness of life on abyssal seafloors showed quite convincingly that this habitat, which is extreme or even “inhospitable” to us, is highly habitable for a remarkable range of organisms. Even though we still know very little about the biology of abyssal organisms, it has become very apparent that many are well adapted to “extreme” conditions; reproduction takes place as well as speciation, and observations of a single site over time, such as the Porcupine Abyssal Plain (PAP) Time Series project, revealed that the abyssal seafloor can be unexpectedly dynamic. The massive bloom of the holothurian Amperima rosea in the PAP observed in the late 1990s was followed by a significant shift in the communities of several other deep-sea invertebrates that was documented over a period of 20 years (Billett et al. 2009). Not all other organisms seem to be affected by the alterations of the environment. Some of the polychaete populations, for example, did not react in any visible way, whereas others showed a significant increase in the number of individuals which could be related to increased nutrient input.
8.5.2. Rare Is Common
In terms of the general structure of benthic communities, there are large differences between the abyss and shallower environments. Nearly all species found in the abyss are rare, at least to our current knowledge. In practical terms it means that most species have been recorded as one or two individuals from one or two sampling sites, even in large programs during which thousands of animals were collected (Fig. 8.4). With very few exceptions, none of the communities sampled during CeDAMar expeditions were characterized by one or a few numerically dominating species as is typically the case in shelf communities.
8.5.3. Diversity of Abyssal Benthos
One of the ways to measure diversity is to look at the number of species at one particular site (alpha diversity), in addition species turnover along a certain distance (beta diversity) may also be assessed. Both measures of diversity were found to be much higher than expected. For example, copepods in the southeast Atlantic occurred everywhere in high abundances, but most species were undescribed (DIVA cruises): 98% of these species had never been seen before. Even smaller animals, the unicellular foraminiferans, showed high species turnover rates in the manganese nodule fields in the Pacific. At sampling sites no more than roughly 600 miles apart, different communities of foraminiferans were found. However, not all foraminiferan distributions appear to be restricted. In another study, including the ANDEEP material, other foraminiferans were discovered that are distributed from pole to pole, obviously coping with many very different habitat conditions.
Habitat heterogeneity is considered to be one of the major drivers of biodiversity because it provides a greater range of niches for the formation of new species. The abyssal seafloor was found to be as heterogeneous as shallower areas, perhaps most obviously in manganese nodule fields of the equatorial Pacific and in the Southern Ocean where stones drop out of melting icebergs and provide greater heterogeneity in substrata. The community structure of abyssal megafauna and macrofauna in manganese nodule fields was found to differ not only due to the availability and quality of food but also because of the heterogeneity in physical and chemical properties of the habitat (nodules and superficial sediment). Studies undertaken at the local scale (1–5 km in distance) with the manned submersible Nautile showed for the first time that nodule fields constitute a distinct habitat for infaunal communities, and that macrofauna and meiofauna components differ in abundance depending on the presence of nodules (Miljutina et al. 2009).
The geologic history of a basin can play an important role for biodiversity as well. A good example is the Southern Ocean. Its history includes not only periods of anoxia in the late Jurassic and cooling in the late Eocene/early Oligocene, but also cycles of glaciation and deglaciation which led to migration of shallow-water species into bathyal and abyssal depths (submergence) as well as recolonization of shallow sea bottoms from the deep (emergence). Applying molecular methods, Raupach et al. (2004, 2009) showed that shallow-water isopods colonized the deep sea at least on four separate occasions. Several isopod families underwent spectacular radiation events in the abyss, resulting in an exceptionally high number of species and species complexes (Fig. 8.5). The Scotia and Weddell Seas, the geographic focus of the ANDEEP investigations, are characterized by a complex tectonic history related to the Middle Jurassic break-up of the Gondwana supercontinent which began around 180 million years (Ma) ago (Storey 1995). The Scotia Sea is much younger and formed during the past approximately 40 Ma (Thomson 2004). However, it is unknown whether the great biodiversity documented for many taxa in the deep Weddell Sea can be explained by the age of the ocean floor.
Another example is the generally low diversity of the benthos in the deep Mediterranean Sea, which is related to, among other reasons, the complex paleoecological history characterized by the Messinian salinity crisis and the almost complete desiccation of the basin.
22.214.171.124. Spatial and Temporal Variability in Primary Productivity in the World's Oceans and Its Effects on Abyssal Communities
Changes in primary productivity in the surface waters of the world's oceans are mirrored in abyssal communities in both space and time (C.R. Smith et al. 2008a). Organic matter created by photosynthetic production provides the food for most deep-sea life. Changes in food production at the sea surface, therefore, and the subsequent transport of organic matter into the ocean's interior through the biological carbon pump, have a profound effect on life on the abyssal seafloor.
It is well known that in regions where seasons are evident in surface waters, seasonal changes occur on the deep-sea floor within a matter of weeks (Billett et al. 1983; C.R. Smith et al. 1997; Beaulieu 2002). Large-scale biogeographical provinces in surface waters are reflected in broad changes in the structure of abyssal communities (Smith C.R. et al. 2008a). Decadal-scale shifts in primary production, caused by climate-related oscillations, produce long-term radical changes in deep-sea communities (Billett et al. 2001, 2009; Ruhl & Smith 2004; Ruhl 2007; C.R. Smith et al. 2008a; Smith K.L. et al. 2009). The fall of the carcasses of whales and fish (C.R. Smith & Baco 2003) and the mass deposition of jellyfish (Billett et al. 2006) provide additional, if localized, organic inputs. The abyss is linked intimately to processes at the sea surface.
CeDAMar projects have contributed significantly to recent advances made in our understanding of how surface water productivity affects abyssal ecosystems. Spatial variations in the distribution of species have been related to changes in surface water productivity in the Kaplan, DIVA, and CROZEX projects. In addition, radical changes in abyssal communities with time have been documented at the PAP in the Northeast Atlantic Ocean. Similar large-scale changes with time have been noted in the northeast Pacific Ocean (K.L. Smith et al. 2009).
At the PAP, CeDAMar has documented how over a 20-year time series (1989 to 2009) the abyssal megafauna changed in total abundance by two orders of magnitude in 1996 (Billett et al. 2009). This was mainly due to the increase in the holothurian species Amperima rosea and became known as the “Amperima Event” (Billett et al. 2001). Significant changes in the abundances of several megafaunal taxa occurred, including ophiuroids, actiniarians, pycnogonids, tunicates, and holothurians other than A. rosea. The changes were evident over a vast area of the abyssal plain (Billett et al. 2001) and had a significant effect on the recycling of organic matter at the sediment surface (Bett et al. 2001). During the CeDAMar project it has been determined that protozoan and metazoan meiofauna (Gooday et al. 2010; Kalogeropoulou et al. 2010) and polychaete macrofauna (Soto et al. 2009) also increased significantly in abundance during the “Amperima Event”. All elements of the benthic community showed a simultaneous change indicative of a large environmental event.
Protozoan phytodetritus indicator species showed a sharp decrease in abundance, whereas trochamminaceans, which previously had been comparatively rare, became dominant, potentially because of the increased disturbance caused by the megafauna (Gooday et al. 2009). In the metazoan meiofauna increases in abundance were seen in the nematode and the meiofaunal polychaetes, but not in the copepods. Ostracods decreased in abundance. The three dominant macrofaunal polychaete families, Cirratulidae, Spionidae, and Opheliidae, all increased in abundance but no major changes occurred in the community structure and dominant species (Soto et al. 2009), unlike the megafauna.
These results show that abyssal benthic communities change significantly with time. Similar results in the northeast Pacific Ocean indicate that such phenomena are widespread in productive regions of the world's oceans (K.L. Smith et al. 2009). The flux of organic matter may change by about an order of magnitude from one year to the next (Lampitt et al. 2010) and abundances in fauna have been shown to be correlated to climate indices that influence the biological carbon pump on regional scales (K.L. Smith et al. 2006, 2009).
Although many elements of the benthic community change at the same time in the Time Series studies, the scale of the response is not the same in all taxa or size classes. Larger changes in abundance are apparent in the megafauna and there are greater changes in the dominant species. This has important implications for interpreting geographic variations in the distributions of species in the different size classes of the benthic community.
Annual particulate organic carbon (POC) flux and benthic parameters have been measured together at only a few sites in the abyssal ocean. However, where POC flux has been measured directly, there are strong linear relations between POC flux and the abundance and/or biomass of specific biotic size classes, including megafauna, macrofauna, and microbes (C.R. Smith et al. 1997; C.R. Smith et al. 2008a; K.L. Smith et al. 2009). Average biomass of megafauna (Lampitt et al. 1986) and macrofauna (Rowe 1971) decline significantly with increasing water depth (and hence decreasing POC flux), resulting in the smaller size classes (bacteria and meiofauna) dominating community biomass at abyssal water depths (greater than 3,000 m) (Rex et al. 2006). Despite this, experimental results (Witte et al. 2003) and time-lapse photography (Bett et al. 2001) indicate that larger organisms play important functional roles in energy flow through food-limited abyssal ecosystems by outcompeting the smaller size classes for freshly deposited detritus. Changes in the spatial distribution of abyssal fauna therefore not only reflect the total input of organic matter, but also the periodicity and predictability in its supply. In addition, changes may be related to the quality of the organic matter (Ginger et al. 2001; Wigham et al. 2003; FitzGeorge-Balfour et al. 2010).
In another CeDAMar study around the Crozet Islands in the southern Indian Ocean, the distributions of protozoan and metazoan meiofauna, and of megafauna, were studied in relation to an area of natural iron fertilization in the oceans (Pollard et al. 2009). Iron carried off the volcanic islands of Crozet leads to seasonal phytoplankton blooms to the north of the Crozet plateau, as opposed to the south of the islands where iron is limiting. The eutrophic site had a greater diversity of live foraminiferans, and the phytodetritus indicator species Epistominella exigua was more abundant at this locality (Hughes et al. 2007). In contrast, the megafaunal communities in the two areas were radically different (Wolff et al. personal communication). The most abundant species Peniagone crozeti (Cross et al. 2009), found only at the seasonally productive site, was new to science. This indicates that megafaunal communities may be the most sensitive to changes in surface water productivity, whereas the smaller size fractions may show broader distributions, depending on the taxon. However, broad generalizations are difficult to make because certain macrofaunal species, including isopods and polychaetes, are restricted to productive areas of the ocean, such as the Southern Ocean (Brandt et al. 2007a, 2007b, 2007c).
126.96.36.199. Latitudinal/Depth Gradients of Biodiversity in the Atlantic Ocean
Latitudinal gradients are the most conspicuous and ubiquitous biogeographic patterns in terrestrial and coastal ecosystems, but their explanation remains elusive. They were long assumed not to occur in the deep sea because the deep overlying water column buffered communities from the climatic phenomena thought to ultimately shape large-scale patterns of diversity. However, there is evidence that latitudinal gradients of diversity do exist in several macrofaunal taxa and foraminiferans in bathyal communities (Rex et al. 1993; Sun et al. 2006). They have not been examined previously at abyssal depths, largely because there are so few abyssal samples. The comprehensive DIVA datasets are being used to test whether latitudinal gradients do exist at abyssal depths. The results will be especially interesting because it is unclear whether latitudinal gradients in macrofaunal taxa exist in the southern hemisphere (Rex et al. 2000).
Results from the ANDEEP expeditions have shown that the impact of depth on species richness is not consistent among taxonomic groups. Ellingsen et al. (2007) examined general macrofaunal response to water depth in the Atlantic sector of the deep Southern Ocean using data on polychaetes, isopods, and bivalves collected during the EASIZ II (Ecology of the Antarctic Sea-Ice Zone, 1998) and ANDEEP I and II cruises (2002), ranging from 774 to 6,348 m depth. They found that the isopods displayed higher species richness in the middle depth range (216 species in 3,000 m depth) and lower in the shallower and deeper parts of the area (Brandt et al. 2005), as reported for other deep-sea areas (see, for example, Gage & Tyler 1991). However, the number of bivalve species showed no clear relation to depth, and polychaetes showed a negative relation to depth (Ellingsen et al. 2007) (Fig. 8.6). Although the data were collected over a wide geographical area (58°14¢–74°36¢ S, 22°08¢–60°44¢ W), the numbers of isopod, polychaete, and bivalve species did not show any consistent relation to latitude or longitude. Gastropods and bivalves show a variety of diversity–depth patterns among deep-sea basins (Allen 2008; Stuart & Rex 2009). Brandt et al. ( 2009) investigated the bathymetric distribution patterns of bivalves, gastropods, isopods and polychaetes in the Southern Ocean from 0 to 5,000 m, and found that the patterns differed between the different taxonomic groups.
|Figure 8.6 Depth distributions of major taxa in the bathyal and abyssal Southern Ocean. Species richness of polychaetes declines with depth (A), that of isopods peaks at about 3,000 m (B), whereas no relation with depth can be seen for bivalves (C).
188.8.131.52. Diversity and Biogeography of Antarctic Deep-Sea Fauna
Within the Southern Ocean, the abyssal benthic realm is the largest ecosystem and covers 27.9 million km 2 (Clarke & Johnston 2003). The Southern Ocean is characterized by some unique environmental features, which include a very deep continental shelf and a weakly stratified water column. It is also the source for the deep-water production influencing the deep circulation throughout the world. These physical characteristics led to the assumption that the Southern Ocean deep-sea fauna may be related both to adjacent shelf communities and to those living in other deep oceans. In the past century, Antarctic benthic shelf communities have been investigated extensively and are known to be characterized by high levels of endemism, gigantism, slow growth, longevity, and late maturity. Some amphipod, isopod, and fish families have adaptive radiations which have led to considerable novel biodiversity in these groups. Contrary to the Southern Ocean shelf, little was known about life in the vast Southern Ocean deep-sea region before the ANDEEP project. ANDEEP was a multidisciplinary international project which involved two expeditions to the Weddell and Scotia Seas in 2002 (Brandt & Hilbig 2004) and a third expedition (ANDEEP III) in 2005 to the Cape and Agulhas Basins, Weddell Sea, Bellingshausen Sea, and Drake Passage. In total, 40 stations were sampled between 748 and 6,348 m water depth with a focus on the abyss (Brandt & Hilbig 2004; Brandt & Ebbe 2007; Brandt et al. 2007a, 2007b, 2007c). The analyses revealed an astonishingly high biodiversity of several different taxa. From the material analyzed, more than 1,400 species were identified, and of these, more than 700 were new to science. In some groups of organisms, such as nematodes and isopods, greater than 90% of the species collected were new to science. Among the most important isopod families, over 95% of the species collected were unknown (Brandt et al. 2007a; Malyutina & Brandt 2007). Although we know that some species complexes have radiated in the deep Southern Ocean (Brökeland & Raupach 2008; Raupach & Wägele 2006; Raupach et al. 2007), it is unclear whether they have evolved here and subsequently spread into other ocean basins. Many species (>50%) were rare or patchy and occurred at only one station. Many species were singletons.
Biogeographic and bathymetric trends varied between groups and were probably related to differences in the reproductive mode (Brandt et al. 2007b, 2009; Pearse et al. 2009). In the isopods and polychaetes, slope assemblages included species that have invaded from either the shelf or the abyss through emergence or submergence, respectively, whereas in other taxa such as bivalves and gastropods, the shelf and slope assemblages were more distinct. Abyssal faunas tended to have stronger biogeographic links to other oceans, particularly the Atlantic, but mainly for organisms with good dispersal capabilities such as the foraminiferans (Brandt et al. 2007b; Pawlowski et al. 2007) and polychaetes (Schüller & Ebbe 2007; Schüller et al. 2009). The isopods, ostracods, and nematodes, which are poor dispersers, include many species currently known only from the Southern Ocean. In some groups, such as the Munnopsidae (Isopoda), the highest number of species (219) was reported in a worldwide biogeographical analysis (Malyutina & Brandt 2007). The ANDEEP results challenge the hypothesis that deep-sea diversity is depressed in the Southern Ocean and provide a sound basis for future explorations of the evolutionary significance of the varied biogeographic patterns observed in this remote environment.
184.108.40.206. The Mediterranean Sea: Diversity Patterns in a Warm Deep Sea
The Mediterranean region is characterized by the presence of both low and very high biodiversity, high levels of endemism are apparent, and in some areas strong energetic gradients in primary production and food supply to the deep occur decreasing from the western to the eastern basins and from shallower to deeper sites. The deep Mediterranean has generally been considered to have lower diversity than other deep-sea regions. Faunal exchange with the Atlantic Ocean is impaired by differences in deep-sea temperatures (approximately 10 °C higher in the Mediterranean than in the Atlantic Ocean at the same depth), which makes the establishment of incoming deep Atlantic fauna difficult. In particular, the abyssal basins of the Eastern Mediterranean are extremely unusual deep-sea systems with water temperatures at 4,000 m in excess of 14 °C. Barriers to colonization from the Atlantic also include salinity gradients and differences in food supply, as well as the existence of shallow sills. The deep Mediterranean is thus generally considered a “biological desert”, although certain areas display such high benthic activity as to be characterized as “benthic hot spots”. These areas are in most cases located at or near the mouth of submarine canyons that transport, through flash flooding, sediment failures, and dense shelfwater cascading, large amounts of sediment and organic material to the deep-sea floor (Canals et al. 2006). Abyssal trenches act as traps of organic matter of either terrestrial or pelagic origin (Tselepides & Lampadariou 2004; Boetius et al. 1996). Large-scale hydrographic changes (Eastern Mediterranean Transient) have also been implicated in enhancing the productivity of the euphotic zone and indirectly structuring the underlying deep benthic communities (Danovaro et al. 2004).
The Mediterranean differs from other deep-sea ecosystems in terms of its megafaunal species composition (Jones et al. 2003). Typical deep-water groups, such as echinoderms, glass sponges, and macroscopic Foraminifera (Xenophyophora) are absent in the deep Mediterranean, whereas other faunistic groups (fishes, decapod crustaceans, mysids, and gastropods) are represented poorly compared with the Northeast Atlantic.
Although the low-diversity pattern is based on the analysis of macro- and megabenthos, recent evidence (Danovaro et al. 2008) suggests that the Mediterranean deep-sea nematode fauna is rather diverse and cannot be considered “biodiversity depleted”. In fact, it was suggested that meiofaunal benthic biodiversity in the deep Atlantic and Mediterranean basins is similar.
A detailed analysis of food availability in the deep Mediterranean revealed that organic matter composition differed between the east and the west Mediterranean. Organic matter in the east was dominated by a high fraction of proteins and lipids. Therefore, although there were reduced amounts of organic matter in the east, this was to a certain extent compensated for by higher food quality and bioavailability. It seems that biodiversity patterns are not controlled by the amounts of food resources alone but also by the availability of the organic matter.
The project LEVAR explored not only the composition of benthic communities, but also environmental factors such as distance from shore, that is, supply of nutrients from shallower areas nearby, versus primary production in surface waters right above the sampling site and their respective influence on diversity. Preliminary results show that the benthic fauna at abyssal sites of the eastern Mediterranean is extremely poor in terms of abundance during normal oligotrophic periods, but can quickly develop high biomass when pulses of organic material settle down to the seafloor after unpredictable phytoplankton bloom events in surface waters (Figs. 8.7A and B).
|Figure 8.7 (A) Box corer sample taken in 1998 in the Ierapetra Basin at 4,300 m depth. Circular shaped surface structures are “lebenspuren”, made by the highly dominant polychaete Myriochele fragilis. (B) Sample from the same site taken in 2006 during LEVAR expedition. Myriochele fragilis was no longer found.
220.127.116.11. Abyssal Diversity Hot Spots
The diversity of life in the Southern Ocean (Brandt & Hilbig 2004) and the central Pacific Ocean (Glover et al. 2002) is high enough to characterize these areas as abyssal biodiversity hot spots. Glover et al. (2002) stated, “Local polychaete species diversity beneath the equatorial Pacific upwelling (measured by rarefaction) appears to be unusually high for the deep sea, exceeding by at least 10 to 20% that measured in abyssal sites in the Atlantic and Pacific, and on the continental slopes of the North Atlantic, North Pacific, and Indian Oceans.” The use of molecular genetic methods will likely reveal an even higher diversity as many organisms looking alike under the microscope turn out to belong to different species, discernible only by differences in their genes.
8.5.4. Abundance of Abyssal Benthos
Studies of the CeDAMar project Biozaire on the continental slope of the Gulf of Guinea, adjacent to the DIVA 1 study area in the abyss, revealed that benthic communities living closer to shore are influenced by a very complex system of environmental parameters. Nevertheless, as in the PAP, the megafauna seemed to respond most directly to the influence of the organic material supplied by the Congo channel, whereas densities of smaller organisms – macrofauna and meiofauna – were subject to changes in environmental parameters, particularly in trophic inputs, at regional scale beyond the effects of the Congo channel (Sibuet & Vangriesheim 2009). Two of three study sites were located in approximately 4,000 m depth, 15 and 150 km south of the Congo channel. They were sampled during three cruises that were roughly one and two years apart.
Abundance of macro- and meiofauna increased substantially between 2001 and 2003, but interestingly not near the Congo river fan where increased input of organic matter was observed but rather at the station away from the fan. Obviously it was the quality of the food rather than the quantity that had the most profound effect on abundance, the organic matter near the Congo channel being mostly terrigeneous and, thus, of lower value for the deep benthos. These results agree well with findings from the deep eastern Mediterranean Sea.
8.5.5. Distributional Patterns in the Abyss: Endemism Versus Cosmopolitanism
The traditional view of an abyssal cosmopolitan fauna has been strongly favored given the enormous, contiguous nature of abyssal environments, and the isolated records of apparently conspecific animals in separate ocean basins. Recent CeDAMar field projects such as the ANDEEP cruises in the Southern Ocean, the KAPLAN cruises in the central Pacific, and the DIVA cruises in the south Atlantic have created new opportunities to re-assess degrees of cosmopolitanism, which are reviewed here.
CeDAMar scientists have focused on a range of dominant abyssal taxa, which exhibit a range of reproductive strategies. These include peracarid crustaceans, copepods, polychaete worms, mollusks, holothurians, and foraminiferans. Peracarids generally brood young in their marsupium and there is no distinct larval stage (Brandt et al. personal communication). Copepods are direct-developing, with juveniles and adults both probably distributed by ocean currents. Polychaetes include species that either brood or display a bi-phasic life cycle with free-swimming planktotrophic or lecithotrophic larvae: both modes are thought to occur in abyssal species (Beesley et al. 2000). Deep-sea gastropods and bivalves generally reproduce by planktotrophic or lecithotrophic larval dispersal (Rex et al. 2005). Deep-sea holothurians have a broad range of egg sizes, from 180 to 4,000 µm (Billett 1991). The largest egg sizes are thought to lead to direct development of free-swimming juvenile holothurians within the abyssopelagic zone allowing for wide dispersal (Billett et al. 1985). Abyssal foraminiferans are thought to reproduce asexually (Murray 1991).
A study of cosmopolitanism in 45 deep-sea peracarid species has revealed only 11 species which occur in all oceans studied (the North Atlantic, South Atlantic, Southern Ocean, North and South Pacific, and Indian Oceans) (Brandt et al. personal communication). However, 33 species have distributions across more than one ocean basin, and 16 species are shared between the North Atlantic and North Pacific. Molecular-based studies of asellote isopods have revealed cryptic species, but these studies have so far been limited to a small range of taxa (Raupach et al. 2009). For benthic harpacticoid copepods, a study in the South Atlantic and Southern Ocean recorded 19 species of which 11 were restricted to particular regions, and eight widespread between ocean basins (Gheerardyn & Veit-Köhler 2009).
In polychaetes, sampling and analysis projects associated with CeDAMar have revealed both cosmopolitanism and cryptic speciation. Several species of small infaunal deposit-feeding spionids from abyssal depths are apparently distributed globally, based on examination of gross and ultra-structural morphology using scanning electron microscopy (Mincks et al. 2009; A. Glover unpublished data). Conversely, specimens of Aurospio dibranchiata Maciolek, 1981 from two central Pacific abyssal plain sites appear to be cryptic species based on 18S rRNA sequences, a normally highly-conserved gene (Mincks et al. 2009). A study of the distribution of multiple species of Southern Ocean abyssal polychaetes has revealed similar trends in terms of broad distributions of several species, based on morphology. Out of 70 Southern Ocean species studied in detail, 17 were shown to be cosmopolitan and only 13 apparently locally restricted to particular Southern Ocean sites (Schüller & Ebbe 2007). The remainder were at the very least broadly distributed, some between ocean basins (for example the Southern Ocean and North Atlantic).
A review of the distribution of protobranch bivalves in the east and west North Atlantic has revealed broadly distributed species at multiple bathymetric levels (McClain et al. 2009). Forty-three percent of the species studied were shared between the two ocean basins, of which 88% had overlapping depth ranges. The degree of apparent cosmopolitanism increased with depth, from 40% in bathyal regions to 60% in abyssal.
Systematic studies of deep-sea holothurians from the Galathea expedition revealed several cosmopolitan species in the abyss (Hansen 1975). Few taxa have been studied yet in detail using molecular methods, but the cosmopolitan species Oneirophanta mutabilis Théel, 1879 (Fig. 8.8A) and Psychropotes longicauda Théel, 1882 have been recovered from multiple ocean basins. These species are characterized by large egg sizes up to 1 mm, which suggests lecithotrophic larvae or direct development (Ramirez-Llodra et al. 2005).
|Figure 8.8 (A) Oneirophanta mutabilis, a cosmopolitan abyssal elasipod holothurian recovered from 5,000 m on the central Pacific abyssal plain. (B) Sphaerosyllis sp. B, a polychaete recovered from a central Indian site, apparently conspecific with specimens from the North Pacific and North Atlantic, with direct-developing juveniles visible budding off mid-body segments. Photographs: A. Glover.
One of the more enigmatic abyssal groups is the Komokiacea, a group of soft-bodied formaminfera that produce large branching tests. A recent systematic review of komokiaceans from the Southern Ocean has revealed nine species, of which five are also present in the North Atlantic (Gooday et al. 2007).
Some foraminiferans apparently are truly cosmoplitan as they cannot be discriminated even with molecular genetic methods, indicating that gene flow is taking place from pole to pole (Lecroq et al. 2009). This global gene flow is difficult to imagine at first glance, and it may be confined to organisms with certain traits in their biology. Body size, which is inversely related to population size (that is, the smaller the organism is, the more individuals there are), plays an important role, and so do planktonic dispersal capabilities and the ability to survive long periods of famine. For example, the cosmopolitan species Epistominella exigua can live in substrata with organic carbon concentrations spanning orders of magnitude and episodic flux to small ephemeral patches on a seemingly homogeneous seabed (Lecroq et al. 2009). This flexibility is thought to facilitate gene flow even under marginal conditions.
In summary, available data are sparse yet support the view that both cosmopolitanism and basin endemism occur across a wide range of taxa in the abyss. These include species that exhibit direct development and bi-phasic life cycles where larvae can be carried by ocean currents. Evidence from molecular genetics is now starting to challenge some of these apparent cosmopolitan distributions, but even if many abyssal species are cryptic, it is clear that gross morphologies, and in some cases fine ultrastructure, are highly conserved in the abyss. This pattern may be a result of relatively rapid colonization of the abyss from bathyal depths and subsequent slow rates of adaptive radiation, in response to relatively similar environmental conditions.
Studies of reproductive biology are extremely rare, and are required to find independent lines of evidence for species ranges. Polychaetes with clear direct-developing offspring have recently been recovered from an isolated, oligotrophic central Indian Ocean abyssal site that are apparently conspecific with specimens from both the north Atlantic and north Pacific (Fig. 8.8B). The simplification of a pattern where only species with larval stages are likely to be broadly dispersed is clearly being challenged, future studies involving physiological data (see, for example, Hall & Thatje 2009) and modeling of available habitats may yet provide the additional lines of evidence required to resolve the paradox of cosmopolitan abyssal species.
However, as so many animals in the abyss are rare, any distributional patterns have to be interpreted with great caution. “Endemic” species may just not have been found again in other locations, and all newly described species are by default “endemics”. Conversely, many species considered to be cosmopolitan may have been misidentified, for example, through the use of identification keys not pertaining to the area. There is some indication that generally, distributional patterns as we interpret them from samples taken so far may represent extreme patchiness. The scale of this patchiness may be rather small (Kaiser et al. 2007), and we may have to change sampling strategies from large-scale coverage of entire ocean basins to concentrated sampling at a single site.
8.5.6. Evolution and Speciation in the Abyss
During the past several decades, much has been learned about patterns of species diversity in the deep sea and their potential ecological causes. However, we are only now beginning to explore the evolutionary processes that generated this rich and distinctive fauna. How and where did all these species originate? Currently, our entire understanding of evolution is based on patterns in other ecosystems.
Deep-sea mollusks were chosen for a study of deep-sea evolution because their basic taxonomy and biogeography is particularly well known. The ENAB project is testing models of evolution based originally on analyses of shell form within species arrayed along depth gradients (Etter & Rex 1990). This research suggested that most population differentiation occurred at intermediate depths in the narrow bathyal zone along continental margins, and that the abyss played only a minor role in promoting deep-sea biodiversity. However, it was not possible to determine whether bathymetric ranges in shell form represented evolved genetic differences or simply environmentally caused morphological differences.
New laboratory methods were developed to extract, amplify, and sequence mitochondrial DNA from specimens that had been fixed in formalin and then preserved in alcohol, sometimes for decades. The resulting patterns of genetic differentiation tended to confirm that the bathyal zone was an evolutionary hot spot (Etter et al. 2005). This research has now been expanded to examine very large-scale geographic variation in mollusks among deep-sea basins in the North and South Atlantic (Zardus et al. 2006). A variety of patterns has emerged including differentiation at great depths.
In the summer of 2008, the first deep-sea sampling expedition devoted exclusively to studying evolutionary patterns in the deep sea was performed. The objective was to collect fresh material in order to sequence both nuclear and mitochondrial genes. A broad range of genes is essential to verifying geographic patterns of differentiation. Fresh material also enables us to develop better primers to more effectively sequence genes in the vast amount of archived preserved material. Being able to use multiple genes adds a new dimension to evolutionary studies in the deep sea. Except for foraminiferans, there is virtually no fossil record of deep-sea assemblages to assist us in unraveling long-term adaptive radiation and the global spread of higher taxa. Instead, phylogenetic evolution must be inferred from molecular genetic data. For the first time, we now have broadly distributed material that is amenable to phylogeographic analysis. This will allow us to answer very fundamental questions, adding an evolutionary-historical perspective to our understanding of life in the deep sea. One of the most puzzling discoveries of this research so far is an apparent genetic break within eurybathic species at about 3,300 m, indicating that there is limited gene flow around this depth. This phenomenon not only occurs in mollusks, but was also reported for a widely distributed amphipod (France & Kocher 1996).
8.5.7. Nodule Mining and MPAs in the Pacific Abyss
Manganese nodules, or polymetallic concretions of iron and manganese hydroxides, can be abundant at the abyssal seafloor beneath regions of low to moderate ocean primary productivity (Ghosh and Mukhopadhyay 2000). In some regions, nodules may cover more than 50% of the seafloor (Fig. 8.9) and are potential mineral sources of copper, nickel, and cobalt. Manganese nodule mining is expected to occur in the abyss by the year 2025 and could ultimately be the largest scale human activity to directly impact the deep-sea floor (C.R. Smith et al. 2008b). Thirteen pioneer investor countries and consortia have conducted hundreds of prospecting cruises to investigate areas of high manganese nodule coverage in the Pacific and Indian Oceans, especially in the area between the Clarion and the Clipperton fracture zones, which covers roughly 6 million km 2 and may contain 340 million tonnes of nickel and 265 million tonnes of copper (Ghosh and Mukhopadhyay 2000; Morgan 2000). Eight contractors are now licensed by the International Seabed Authority (ISA) to explore nodule resources and to test mining techniques within individual claim areas, each covering 75,000 km 2 (Fig. 8.10) (C.R. Smith et al. 2008b; www.isa.org.jm/en/home). In addition to harboring mineral resources, abyssal Pacific sediments in the CCZ may also be major reservoirs of biodiversity (Glover et al. 2002). However, it has been extremely difficult to predict the threat of nodule mining to biodiversity (in particular, the likelihood of species extinctions) because of very limited knowledge of (1) the number of species residing within areas likely to be perturbed by single mining operations, and (2) the typical geographic ranges of species within the nodule provinces (Glover & Smith 2003). During the CeDAMar field projects KAPLAN and NODINAUT, we used state-of-the-art molecular and morphological methods to begin to evaluate biodiversity and species ranges of three key faunal groups in the abyssal Pacific nodule province: polychaete worms, nematode worms, and foraminiferans. Together, these groups can constitute more than 50% of faunal abundance and species richness in abyssal sediments (Smith & Demopoulos 2003), and represent a broad range of ecological and life-history types.
|Figure 8.9 The yellow elasipod holothuroid Psychropotes longicauda, here shown on a dense bed of manganese nodules, is a widely distributed deposit feeder and uses its upright “sail” to use current energy for transport along the seafloor. It was collected at 4,900 m in the Clarion-Clipperton Fracture Zone. Photograph: IFREMER.
CeDAMar results indicate high, unanticipated levels of species diversity for all three sediment-dwelling faunal components studied at our individual sites E, C, and W (Fig. 8.10). Based on morphological analyses, the Foraminifera contain at least 252 species at site E and at least 180 species at site C (Nozawa et al. 2006). Many of these species are new to science and appear not to have been collected elsewhere (Nozawa et al. 2006; C.R. Smith et al. 2008c). Based on DNA sequencing studies, the nematode worms also exhibit very high within-site diversity, with 73 molecular operational taxonomic units (or putative species) from only 97 sequenced individuals (C.R. Smith et al. 2008c). Because of a high ratio of one new species for every 1.3 individuals sequenced, the total nematode species richness is still grossly undersampled; we can be certain that far more species remain to be collected at each of our abyssal Pacific sites.
The polychaetes also exhibit very high within-site diversity for the families studied in detail; for example, Site E contains at least 48 polychaete species within 16 polychaete families (C.R. Smith et al. 2008c). A high abundance of apparently cryptic species found with our molecular studies indicates that earlier estimates of polychaete species richness within abyssal Pacific sites based on morphological studies, for example the 170 species from 3 m 2 by Glover et al. ( 2002), are likely to be low by at least a factor of two. We speculate that, even based on the relatively limited number of samples we have been able to analyze thus far, the total species richness of sediment-dwelling foraminiferans, nematodes, and polychaetes (a subset of the total fauna) at a single site in the CCZ could easily exceed 1,000 species (C.R. Smith et al. 2008c).
Our combined results for the foraminferans, nematodes, and polychaetes suggest that there is a characteristic fauna of the Pacific abyss, indicating that the abyss is not merely a sink of non-reproducing individuals transported from the continental margins (Rex et al. 2005; C.R. Smith et al. 2008a). Many of the hundreds of species of Foraminifera identified from our samples appear to be restricted to, or at least characteristic of, the abyss (Nozawa et al. 2006; C.R. Smith et al. 2008c). Seventy of the 73 molecular operational taxonomic units (MOTUs) of nematodes appear to be new genera distinct from shallow-water genera, and thus may well have evolved in the abyss (C.R. Smith et al. 2008c). The molecular data for the polychaetes also indicate numerous cryptic new species in our KAPLAN abyssal samples, again suggesting that the abyssal polychaete fauna contains higher species diversity than previously appreciated, and may include numerous species evolved in the abyss. All of these results suggest that the central Pacific abyss harbors a specially adapted, diverse fauna distinct from the fauna of the continental margins. It seems very unlikely that all, or even many, species found in the CCZ abyss are protected from extinction by populations residing many thousands of kilometers away at much shallower depths on the continental margins (C.R. Smith et al. 2008a).
Although the data are still limited, there is significant evidence that community structure of the Foraminifera and polychaetes differ substantially on scales of 1,000–3,000 km across the CCZ. These apparent patterns of faunal turnover seem likely to be driven in part by the east to west decline in primary productivity thus the flux of food to the seafloor across the CCZ , but may also be driven in part by varying habitat heterogeneity (C.R. Smith et al. 2008c).
Using results from the KAPLAN and NODINAUT projects, CeDAMar helped to convene a workshop of experts to draft recommendations to ISA for the design of MPAs in the CCZ to conserve marine biodiversity and ecosystem structure and function in the region in the face of nodule mining. Based on sound scientific principles, it was recommended that a network of nine 400 km × 400 km protected areas (or “areas of particular environmental interest”) be set up within the CCZ where mining would be prohibited (Fig. 8.11) (International Seabed Authority 2008, 2009). This network of protected areas would be stratified by regional variations in primary productivity and protect a total area of 1,440,000 km 2, placing roughly 25% of the total CCZ management area under protection (International Seabed Authority 2008). The ISA is currently considering these recommendations. If implemented, these CeDAMar recommendations would initiate scientifically based conservation management in international waters, would establish the ISA as a leader in the application of modern conservation management, and would set a precedent for protecting seabed biodiversity, a common heritage of mankind, before the initiation of exploitive activities (International Seabed Authority 2008).
8.6. Remaining Challenges and New Questions
8.6.1. Natural History and Environmental Factors
Although we learned much about the faunal elements of abyssal benthos communities, we still know almost nothing about the natural history of abyssal animals or environmental factors structuring abyssal communities. To the human eye an abyssal plain looks uniform over hundreds of kilometers. Nonetheless, benthic communities are not nearly as homogeneous as originally thought. To abyssal animals, the habitat bears enough heterogeneity to cause species turnover even within a single ocean basin. However, we are just beginning to understand the scale of species turnover in abyssal plains.
In the deep Southern Ocean, the ANDEEP project has revealed patterns of biodiversity within different faunal groups, but we still do not know anything about the processes behind these biodiversity patterns. The ANDEEP follow-up International Polar Year project SYSTCO (system coupling) therefore focuses on coupling processes between atmosphere, water column, and deep-sea floor near the Polar Front and in the abyssal Weddell Sea and includes ecological questions and investigations of the role of deep-sea fauna in trophodynamic coupling and nutrient cycling in oceanic ecosystems.
8.6.2. Speciation in the Abyss
On an evolutionary scale, the same gap in our knowledge becomes apparent. We know very little about speciation in the abyss, and we are just now beginning to gain insights into the origin of the abyssal fauna and the very high diversity of abyssal benthic communities. Especially for soft-bodied organisms that leave no fossil record, molecular clocks have to be developed to reconstruct their evolutionary history. ENAB has developed novel techniques which are promising for future research.
8.6.3. Abyssal Species Numbers and Taxonomy
We will probably never know the true number of species in the abyss. The research area is far too large to be sampled adequately considering how heterogeneous this habitat turns out to be and how high the percentage is of rare species which have been recorded from just one site, often also by just one individual among thousands. Nevertheless, with knowledge gained continuously, scientists continue to try to reach better and better estimates.
The remarkable gain of knowledge about the abyssal benthos, notwithstanding the taxonomic impediment which brought about the birth of CeDAMar, is still apparent. We are still facing an overwhelming amount of species awaiting formal description and a scarcity of specialists to do the task. Taxonomic intercalibration, which has come a long way during CeDAMar, will have to continue as we have just scratched the surface. Molecular genetic and morphological methods will have to be integrated in a continuing effort to understand each other and communicate.
8.7. Moving On
Although public awareness about the deep sea has risen a great deal during CeDAMar, the abyss is still perceived by most people as a somewhat remote part of the planet, not affecting humankind in any way worth mentioning, and the research is still felt to be somewhat academic.
However, the abyss is on its way to become a resource for human exploitation very quickly. Industrial harvesting of manganese nodules may become a reality before most of us notice. Necessary technology is far advanced, largely unnoticed by anybody other than those directly involved. Even before man-made gear enters this still pristine environment, it is quite possible that the abyssal seafloor, which accounts for the largest area on the planet, may warrant our close attention because biogeochemical cycles of the seafloor have a strong influence on the global climate and climate change.
Climate warming is expected to increase regional sea surface temperatures and thermal stratification in low to mid-latitudes, yielding reductions in nutrient upwelling (C.R. Smith et al. 2008b; K.L. Smith et al. 2009). These changes will in turn alter the quantity and quality of food flux from the euphotic zone to the abyssal seafloor (Fig. 8.12). CeDAMar studies suggest that resulting long-term declines in POC flux to the abyss will cause reductions in the abundance and biomass of benthic fauna, and yield reductions in species diversity and body size over large regions, such as in the equatorial Pacific. Substantial shifts in the taxonomic composition of abyssal assemblages, especially the megafauna, are also expected, as well as changes in basic ecosystem functions at the seafloor, such as organic carbon burial and calcium carbonate mineralization. Climate induced reductions in abyssal food flux over large areas, such as the equatorial Pacific biodiversity hot spot, have the potential to cause regional species extinctions as populations are reduced below reproductively viable levels (Rex et al. 2005; C.R. Smith et al. 2008b). Because abyssal ecosystems are so sensitive to the quantity and quality of sinking food material from the upper ocean (C.R. Smith et al. 2008b; K.L. Smith et al. 2009), impacts on the abyss must be considered in predicting the effects of climate warming and eco-engineering (for example ocean fertilization to mitigate climate change) on the biodiversity and ecological functioning of ocean ecosystems.
8.7.1. What Needs to Be Done?
When the first Census has ended, keeping the momentum of global collaboration has to become our first action item. One idea might be to establish an international consortium supported by national funding agencies to identify important questions that most urgently need answers. Funding for taxonomists and molecular biologists needs to be secured in the long term to truly overcome the taxonomic impediment. Sampling strategies need the same global perspective as the Census to avoid falling back into competition among nations or institutions for the most attractive results.
Innovative methods will have to be adopted for the exploration of life in the abyss, for example, in situ experiments that might tell us something about the biology of abyssal organisms, and autonomous vehicles that can travel along abyssal plains to collect data over large distances and areas. The technically challenging development of suitable instruments and research with such methods will require substantial additional funding which will be granted only if the general public gets involved and educated. Societal acceptance of deep-sea research is still measured by that of astronomy. Allocating public funds to investigate other planets, stars, and even galaxies, immeasurably farther away from human reach, is questioned by few, in contrast to investigating the portion of surface of our own planet which happens to be covered with water.
Exhibitions and trade fairs related to boating and diving lately included small individual submarines for pleasure, designed to dive to about 100 m, driven by the owners themselves. Although these submarines are targeted for a very wealthy clientele, they may perhaps raise awareness for the benthic environment in a different and more direct way than anything we can offer through the media.
8.7.2. Outlook and Conclusions
The return to a more holistic perspective is perhaps a logical process following nearly a century of specialization and focus on smaller and smaller details of an ecosystem which, as we gathered more and more facts, seemed to become more and more difficult to comprehend. We may have reached a time that is right for taking a step back and looking at whole systems from different viewpoints, realizing how they all overlap and complement each other. If one could understand which factors regulate the presence of species in a given area and which factors regulate the absolute and relative abundance of these species, then one would understand much of the functioning of the ecosystem as a whole. The evaluation of biodiversity – defined as the variety and variability of genomes, populations, species, communities, and ecosystems in space and time (Heywood 1995) – continues to be a central theme in biology and conservation.
When the scientific scope of CeDAMar was planned, exclusion of continental margins, seamounts, and chemosynthetic environments was deliberate. Only through focusing on a few of the major abyssal basins of the global ocean was it possible to achieve any tangible results in the limited timeframe of the Census. Exploring the relations of the ecosystem “abyssal benthos” with neighboring systems is a logical second step to be undertaken in the future. Several habitats possibly interacting with the abyssal benthos come to mind, most obviously the continental margins (see Chapter ); on an even larger scale, an integration of water column and benthos research is a desirable goal. To be able to gain more complete insights both spatially and temporally, the abyss must be integrated into ocean observing systems.
Although the rate of discovery of new species is intimidating, it is not equally large for all organisms. Specialists do not expect much beyond 10% new species, for example, of mollusks (whereas for others such as nematodes the rate may be about 90%). Several organisms have been found to be widespread, for example, on either side of the Atlantic Ocean or in both Polar seas. Although genetic investigations have to confirm these patterns based on morphology, we may eventually come to a realistic estimate of the number of species in the abyss. “Singletons”, those species known from only one specimen, may eventually be recaptured at the original site or even elsewhere, and the recapture rate may be a good proxy for species richness.
Within the past 150 years, we have learned to look at the abyss through different lenses. The unfathomed depths turned from a mythical place inhabited, at best, by fearsome creatures waiting to attack the unwary seaman, to an integral part of our planet filled with a dazzling variety of life, well adapted to its environment and of unsuspected beauty and grace. There are still many more questions than answers. CeDAMar research has lifted some of the mysteries, and the facts are even more fascinating than the myths, to scientists as well as the general public. There is much hope among deep-sea scientists that CeDAMar, together with other deep-sea projects within the Census, acted as a spark for ongoing research in the decades to follow.
The field project CeDAMar, like the entire Census of Marine Life, would not have happened without the vision, inspiration, and continuous support of Jesse Ausubel, Sloan Foundation, and J. Frederick Grassle, Institute of Marine and Coastal Sciences, Rutgers University. National science foundations in many nations are thanked for their financial support of the research done during CeDAMar projects, and there are countless scientists and technicians, well-seasoned and young, who have to be thanked for their tireless work that produced the data. Captains and crews of many research vessels helped to collect the material on which the data are based, and heartfelt thanks are due to them as well.
|Allen, J.A. (2008) The Bivalvia of the deep Atlantic. Malacologia 50, 57–173.|
|Beaulieu, S.E. (2002) Accumulation and fate of phytodetritus on the sea floor. Oceanography and Marine Biology 40, 171–232.|
|Beesley, P.L., Ross, G.J.B. & Glasby, C.J. (2000) Polychaetes and Allies: The Southern Synthesis. CSIRO Publishing.|
|Bett, B.J., Malzone, M.G., Narayanaswamy, B.E. & Wigham, B.D. (2001) Temporal variability in phytodetritus and megabenthic activity at the seabed in the deep Northeast Atlantic. Progress in Oceanography 50, 349–368.|
|Billett, D.S.M. (1991) Deep-sea holothurians. Oceanography and Marine Biology 29, 259–317.|
|Billett, D.S.M., Bett, B.J., Jacobs, C.L., et al. (2006) Mass deposition of jellyfish in the deep Arabian Sea. Limnology and Oceanography 51, 2077–2083.|
|Billett, D.S.M., Bett, B.J., Rice, A.L., et al. (2001) Long-term change in the megabenthos of the Porcupine Abyssal Plain (NE Atlantic). Progress in Oceanography 50, 325–348.|
|Billett, D.S.M., Bett, B.J., Reid, W.D.K., et al. (2009) Long-term change in the abyssal NE Atlantic: The “Amperima Event” revisited. Deep-Sea Research II doi:10.1016/j.dsr2.2009.02.001.|
|Billett, D.S.M., Hansen, B. & Huggett, Q.J. (1985) Pelagic Holothurioidea (Echinodermata) of the northeast Atlantic. In: Echinodermata: Proceedings of the 5th International Echinoderms Conference, Galway (eds. B.F. Keegan & B.D.S. O'Connor) pp. 399–411.|
|Billett, D.S.M., Lampitt, R.S., Rice, A.L. & Mantoura, F. (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302, 520–522.|
|Boetius, A., Scheibe, S., Tselepides, A. & Thiel, H. (1996) Microbial biomass and activities in deep-sea sediments of the Eastern Mediterranean: trenches and benthic hotspots. Deep-Sea Research 43, 1439–1460.|
|Brandt, A., Brökeland, W., Choudhury, M., et al. (2007c) Deep-sea isopod biodiversity, abundance and endemism in the Atlantic sector of the Southern Ocean – results from the ANDEEP I – III expeditions. Deep-Sea Research II 54, 1760–1775.|
|Brandt, A., De Broyer, C., De Mesel, I., et al. (2007a) The deep benthos. Philosophical Transactions of the Royal Society of London B 362, 39–66.|
|Brandt, A. & Ebbe, B. (2007) ANDEEP III ANtarctic benthic DEEP-sea biodiversity: colonisation history and recent community patterns. Deep-Sea Research II 54, 1645–1904.|
|Brandt, A., Ellingsen, K.E.E., Brix, S., et al. (2005) Southern Ocean deep-sea isopod species richness (Crustacea, Malacostraca): influences of depth, latitude and longitude. Polar Biology 28, 284–289.|
|Brandt, A., Gooday, A.J., Brix S.B., et al. (2007b) The Southern Ocean deep sea: first insights into biodiversity and biogeography. Nature 447, 307–311.|
|Brandt, A. & Hilbig, B. (2004) ANDEEP (Antarctic benthic DEEP-sea biodiversity: colonization history and recent community patterns) – a tribute to Howard L. Sanders. Deep-Sea Research II 51, 1457–1919.|
|Brandt, A., Linse, K. & Schüller, M. (2009) Bathymetric distribution patterns of Southern Ocean macrofaunal taxa: Bivalvia, Gastropoda, Isopoda and Polychaeta. Deep-Sea Research I 56, 2013–2025.|
|Brökeland, W. & Raupach, M. (2008) A species complex within the isopod genus Haploniscus (Crustacea: Malacostraca) from the Antarctic deep sea. Zoological Journal of the Linnean Society 152, 655–706.|
|Brown, B. (2001) Biomass of deep-sea benthic communities: polychaetes and other invertebrates. Bulletin of Marine Science 48, 401–411.|
|Canals, M., Puig, P., Durrieu de Madron, X., et al. (2006) Flushing submarine canyons. Nature 444, 354–357.|
|Clarke, A. & Johnston, N.M. (2003) Antarctic marine benthic diversity. Oceanography and Marine Biology 41, 47–114.|
|Cross, I.A., Gebruk, A., Billett, D.S.M. & Rogacheva, A. (2009) Peniagone crozeti, a new species of elasipodid holothurian from abyssal depths off the Crozet Isles in the Southern Indian Ocean. Zootaxa 2096, 484–488.|
|Culver, S.J. & Buzas, M.A. (2000) Global latitudinal species diversity gradient in deep-sea foraminifera. Deep-Sea Research I 47, 259–275.|
|Danovaro, R., Dell'Anno, A. & Pusceddu, A. (2004) Biodiversity response to climate change in a warm deep sea. Ecology Letters 7, 821–828.|
|Danovaro, R, Gambi, C., Lampadariou, N. & Tselepides, A. (2008) Deep-sea nematode biodiversity in the Mediterranean basin: testing for longitudinal, bathymetric and energetic gradients. Ecography 31, 231–244.|
|Ellingsen, K., Brandt, A., Hilbig, B. & Linse, K. (2007) The diversity and spatial distribution of polychaetes, isopods and bivalves in the Atlantic sector of the deep Southern Ocean. Polar Biology 30, 1265–1273.|
|Etter, R.J. & Rex, M.A. (1990) Population differentiation decreases with depth in deep-sea gastropods. Deep-Sea Research 37:1251–1261.|
|Etter, R.J., Rex, M.A., Chase, M.R. & Quattro, J.M. (2005) Population differentiation decreases with depth in deep-sea bivalves. Evolution 59, 1479–1491.|
|FitzGeorge-Balfour, T., Billett, D.S.M., Wolff, G.A., et al. (2010) Phytopigments as biomarkers of selectivity in abyssal holothurians; inter-species differences in response to a changing food supply. Deep-Sea Research II doi:10.1016/j.dsr2.2010.01.013.|
|France, S.C. & Kocher, T.D. (1996) Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among deep-sea amphipods, Eurythenes gryllus. Marine Biology 126, 633–643.|
|Gage, J.D. & Tyler, P.A. (1991) Deep-Sea Biology: a Natural History of Organisms at the Deep-Sea Floor. Cambridge, UK: Cambridge University Press.|
|Gheerardyn, H. & Veit-Köhler, G. (2009) Diversity and large-scale biogeography of Paramesochridae (Copepoda, Harpacticoida) in South Atlantic Abyssal Plains and the deep Southern Ocean. Deep-Sea Research I 56, 1804–1815.|
|Ghosh, A.K. & Mukhopadhyay, R. (2000) Mineral Wealth of the Ocean. Rotterdam, the Netherlands: A.A. Balkema.|
|Ginger, M.L. et al. (2001) Organic matter assimilation and selective feeding by holothurians in the deep sea: Some observations and comments. Progress in Oceanography 50, 407–421.|
|Glover, A.G. & Smith, C.R. (2003) The deep-sea floor ecosystem: current status and prospects of anthropogenic change by the year 2025. Environmental Conservation 30, 219–241.|
|Glover, A.G., Smith, C.R., Paterson, J., et al. (2002) Polychaete species diversity in the central Pacific abyss: local and regional patterns, and relationships with productivity. Marine Ecology Progress Series 240, 157–170.|
|Gooday A.J., Kamenskaya, O.E. & Cedhagen, T. (2007) New and little-known Komokiacea (Foraminifera) from the bathyal and abyssal Weddell Sea and adjacent areas. Zoological Journal of the Linnean Society 151, 219–251.|
|Gooday, A.J., Malzone, M.G., Bett, B.J. & Lamont, P.A. (2010) Decadal-scale changes in shallow-infaunal foraminiferal assemblages at the Porcupine Abyssal Plain, NE Atlantic. Deep-Sea Research II doi:10.1016/j.dsr2.2010.01.012.|
|Grassle, J.F. & Maciolek, N.J. (1992) Deep-sea species richness: regional and local diversity estimates from quantitative bottom samples. American Naturalist 139, 313–341.|
|Gray, J.S. (2002) Species richness of marine soft sediment. Marine Ecology Progress Series 244, 285–297.|
|Hall, S. & Thatje, S. (2009) Global bottlenecks in the distribution of marine Crustacea: temperature constraints in the family Lithodidae. Journal of Biogeography, 36, 2125–2135.|
|Hansen, B. (1975) Systematics and biology of the deep-sea holothurians I. Elasipoda. Galathea Report 13, 1–262.|
|Hessler, R.R. & Sanders, H.L. (1967) Faunal diversity in the deep-sea. Deep-Sea Research 14, 65–78.|
|Heywood, V.H. (ed.) (1995) Global Biodiversity Assessment. United Nations Environment Programme. Cambridge, UK: Cambridge University Press.|
|Hughes, J.A., Smith, T., Chaillan, F., et al. (2007) Two abyssal sites in the Southern Ocean influenced by different organic matter inputs: Environmental characterization and preliminary observations on the benthic foraminifera. Deep-Sea Research II 54, 2275–2290.|
|International Seabed Authority (2008) Rationale and recommendations for the establishment of preservation reference areas for nodule mining in the Clarion-Clipperton Zone. ISBA/14/LTC/2*, Kingston, Jamaica, 12 pp.|
|International Seabed Authority (2009) Proposal for the designation of certain geographical areas in the Clarion-Clipperton Fracture Zone. ISBA/15/LTC/4, Kingston, Jamaica, 8 pp.|
|Jones, E.G., Tselepides, A., Bagley, P.M. & Priede, I.G. (2003) Bathymetric distribution of some benthic and benthopelagic species attracted to baited cameras and traps in the deep Eastern Mediterranean. Marine Ecology Progress Series 251, 75–86.|
|Kalogeropoulou, V., Bett, B.J., Gooday, A.J., et al. (2010) Temporal changes (1989–1999) in deep-sea metazoan meiofaunal assemblages on the Porcupine Abyssal Plain, NE Atlantic. Deep-Sea Research II doi:10.1016/j.dsr2.2009.02.002.|
|Kaiser, S., Barnes, D.K.A. & Brandt, A. (2007) Slope and deep-sea abundance across scales: Southern Ocean isopods show how complex the deep sea can be. Deep-Sea Research II 54, 1776–1789.|
|Lampitt, R.S., Billett, D.S.M. & Rice, A.L. (1986) The biomass of the invertebrate megabenthos from 500 to 4100 m in the North East Atlantic. Marine Biology 93, 69–81.|
|Lampitt, R.S., Salter, I., de Cuevas, B.A., et al. (2010) Long-term variability of downward particle flux in the deep Northeast Atlantic: causes and trends. Deep-Sea Research II doi:10.1016/j.dsr2.2010.01.011.|
|Lecroq, B., Gooday, A.J. & Pawlowski, J. (2009) Global genetic homogeneity in the deep-sea foraminiferan Epistominella exigua (Rotaliidae: Pseudoparrellidae). Zootaxa 2096, 23–32.|
|Malyutina, M. & Brandt, A. (2007) Diversity and zoogeography of Antarctic deep-sea Munnopsidae (Crustacea, Isopoda, Asellota). Deep-Sea Research II 54, 1790–1805.|
|McClain, C.R., Rex, M.A. & Etter, R.J. (2009) Patterns in deep-sea macroecology. In: Marine Macroecology (eds. J. Witman & K. Roy). Chicago: University of Chicago Press.|
|Miljutina, M.A., Miljutina, D.M., Mahatma, R. & Galéron, J. (2009) Deep-sea nematode assemblages of the Clarion-Clapperton Nodule Province (Tropical North-Eastern Pacific). Marine Biodiversity 40, 1–15.|
|Mincks, S.L., Dyal, P.L., Paterson, G.L.J., et al. (2009) A new species of Aurospio (Polychaeta, Spionidae) from the Antarctic shelf, with analysis of its ecology, reproductive biology and evolutionary history. Marine Ecology 30, 181–197.|
|Morgan, C.L. (2000) Resource estimates of the Clarion-Clipperton manganese nodule deposits. In: Handbook of Marine Mineral Deposits (ed. D.S. Cronan), pp. 145–170. Boca Raton, Florida: CRC Press|
|Murray, J.W. (1991) Ecology and Palaeoecology of Benthic Foraminifera. New York: Longman Scientific and Technical. 397 pp.|
|Nozawa, F., Kitazato, H., Tsuchiya, M. & Gooday, A.J. (2006) ‘Live’ benthic foraminifera at an abyssal site in the equatorial Pacific nodule province: abundance, diversity and taxonomic composition. Deep-Sea Research I 53, 1406–1422.|
|Pawlowski, J., Fahrni, J.F., Lecroq, B., et al. (2007) Bipolar gene flow in deep-sea benthic foraminifera. Molecular Ecology 16, 4089–4096.|
|Pearse, J.S., Mooi, R., Lockhart, S.J. & Brandt, A. (2009) Brooding and species diversity in the southern ocean: selection for brooders or speciation within brooding clades? In: Smithsonian at the Poles: Contributions to International Polar Year Science (eds. I. Krupnik, I.M.A. Lang & S.E. Miller) pp. 181–196. proceedings Proceedings of Smithsonian at the Poles Symposium, Smithsonian Institution, Washington, DC, 3–4 May 2007. Washington, DC: Smithsonian Institution Scholarly Press.|
|Pollard, R.T., Salter, I., Sanders, R., et al. (2009) Southern Ocean deep-water carbon export enhanced by natural iron fertilization. Nature 457, 577–580.|
|Poore, G.C.B. & Wilson, G.D.F. (1993) Marine species richness. Nature 361, 597–598.|
|Ramirez-Llodra, E., Reid, W.D.K. & Billett, D.S.M. (2005) Long-term changes in reproductive patterns of the holothurian Oneirophanta mutabilis from the Porcupine Abyssal Plain. Marine Biology 146, 683–693.|
|Raupach, M.J., Held, C. & Wägele, J.-W. (2004) Multiple colonization of the deep sea by the Asellota (Crustacea: Peracarida: Isopoda). Deep-Sea Research II 51, 1787–1795.|
|Raupach, M.J., Malyutina, M., Brandt, A. & Wägele, J.W. (2007) Molecular data reveal a highly diverse species flock within the deep-sea isopod Betamorpha fusiformis (Crustacea: Isopoda: Asellota) in the Southern Ocean. Deep-Sea Research II 54, 1820–1830.|
|Raupach, M.J., Mayer, C., Malyutina, M. & Wägele, J.-W. (2009) Multiple origins of deep-sea Asellota (Crustacea: Isopoda) from shallow waters revealed by molecular data. Proceedings of the Royal Society B 276, 799–808.|
|Raupach, M. & Wägele, J.-W. (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda) – a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarctic Science 18, 191–198.|
|Rex, M.A., Etter, R.J. & Stuart, C.T. (1997) Large-scale patterns of species diversity in the deep-sea benthos. In: Marine biodiversity (eds. R.F.G. Ormond, J.D. Gage & M.V. Angel), pp. 94–121. Cambridge, UK: Cambridge University Press.|
|Rex, M.A., McClain, C.R., Johnson, N.A., et al. (2005) A source-sink hypothesis for abyssal diversity. American Naturalist 165, 163–178.|
|Rex, M.A., Stuart, C.T. & Coyne, G. (2000) Latitudinal gradients of species richness in the deep-sea benthos of the North Atlantic. Proceedings of the National Academy of Sciences of the USA 97, 4082–4085.|
|Rex, M.A., Stuart, C.T., Hessler, R.R., et al. (1993) Global-scale latitudinal patterns of species diversity in the deep-sea benthos. Nature 365, 636–639.|
|Rex, M.A. et al. (2006) Global bathymetric patterns of standing stock and body size in the deep-sea benthos. Marine Ecology Progress Series 317, 1–8.|
|Rose, A., Seifried, S., Willen, E., et al. (2005) A method for comparing within-core alpha diversity values from repeated multicorer samplings, shown for abyssal Harpacticoida (Crustacea: Copepoda) from the Angola Basin. Organisms Diversity and Evolution 5 (Suppl. 1), 3–17.|
|Rowe, G.T. (1971) Observations on bottom currents and epibenthic populations in Hatteras Canyon. Deep-Sea Research 18, 569–581.|
|Ruhl, H.A. (2007) Abundance and size distribution dynamics of abyssal epibenthic megafauna in the northeast Pacific. Ecology 88, 1250–1262.|
|Ruhl, H.A. & Smith, K.L. (2004) Shifts in deep-sea community structure linked to climate and food supply. Science 305, 513–515.|
|Sanders, H.L., Hessler, R.R. & Hampson, G.R. (1965) An introduction to the study of deep-sea benthic faunal assemblages along the Gay Head–Bermuda transect. Deep-Sea Research 12, 845–867.|
|Sanders, H.L. & Hessler, R.R. (1969) Diversity and composition of abyssal benthos. Science 166, 1033–1034.|
|Schüller, M. & Ebbe, B. (2007) Global distributional patterns of selected deep-sea Polychaeta (Annelida) from the Southern Ocean. Deep-Sea Research II 54, 1737–1751.|
|Schüller, M., Ebbe, B. & Wägele, J.-W. (2009) Community structure and diversity of polychaetes (Annelida) in the deep Weddell Sea (Southern Ocean) and adjacent basins. Marine Biodiversity 39, 95–108.|
|Sibuet, M. & Vangriesheim, A. (2009) Deep-sea environment and biodiversity of the West African Equatorial margin. Deep-Sea Research II 56, 2156–2168.|
|Smith C.R. & Baco, A.R. (2003) Ecology of whale falls at the deep-sea floor. Oceanography and Marine Biology 41, 311–354.|
|Smith, C.R., Berelson, W., Demaster, D.J., et al. (1997) Latitudinal variations in benthic processes in the abyssal equatorial Pacific: control by biogenic particle flux. Deep-Sea Research II 44, 2295–2317.|
|Smith, C.R., De Leo, F.C., Bernardino, A.F., et al. (2008a) Abyssal food limitation, ecosystem structure and climate change. Trends in Ecology and Evolution 23, 518–528.|
|Smith, C.R. & Demopoulos, A.W.J. (2003) Ecology of the deep Pacific Ocean floor. In: Ecosystems of the World, Volume 28, Ecosystems of the Deep Ocean (ed. P.A. Tyler), pp. 179–218. Elsevier, Amsterdam.|
|Smith, C.R., Levin, L.A., Koslow, A., et al. (2008b) The near future of deep seafloor ecosystems. In: Aquatic Ecosystems: Trends and global prospects (ed. N. Polunin), pp. 334–351. Cambridge University Press.|
|Smith, C.R., Paterson, G., Lambshead, J., et al. (2008c). Biodiversity, species ranges, and gene flow in the abyssal Pacific nodule province: predicting and managing the impacts of deep seabed mining. ISA Technical Study: No.3, International Seabed Authority, Kingston, Jamaica, 38 pp.|
|Smith K.L., et al. (2006) Climate effect on food supply to depths greater than 4,000 meters in the northeast Pacific. Limnology and Oceanography 51, 166–176.|
|Smith, K.L., Ruhl, H.A., Bett, B.J., et al. (2009) Climate, carbon cycling, and deep-ocean ecosystems. Proceedings of the National Academy of Sciences of the USA 106, 19211–19218.|
|Soto, E., Paterson, G.L.J., Billett, D.S.M., et al. (2009) Temporal variability in polychaete assemblages of the abyssal NE Atlantic Ocean. Deep-Sea Research II doi:10.1016/j.dsr2.2009.02.003.|
|Storey, B.C. (1995) The role of mantle plumes in continental breakup: case histories from Gondwanaland. Nature 337, 301–308.|
|Stuart, C.T., Martinez Arbizu, P., Smith, C.R., et al. (2008) CeDAMar global database of abyssal biological sampling. Aquatic Biology 4, 143–145.|
|Stuart, C.T. & Rex, M.A. (2009) Bathymetric patterns of deep-sea gastropod species diversity in 10 basins of the Atlantic Ocean and Norwegian Sea. Marine Ecology 30, 164–180.|
|Sun, X., Corliss, B.H., Brown, C.W. & Showers, W.J. (2006) The effect of primary productivity and seasonality on the distribution of deep-sea benthic Foraminifera in the North Atlantic. Deep-Sea Research I 53: 28–47.|
|Thomas, E. & Gooday, A.J. (1996) Cenozoic deep-sea benthic foraminifers: tracers for changes in oceanic productivity? Geology 24, 355–358.|
|Thomson, M.R.A. (2004) Geological and palaeoenvironmental history of the Scotia Sea region as a basis for biological interpretation. Deep-Sea Research II 51, 1467–1487.|
|Tselepides, A. & Lampadariou, N. (2004) Deep-sea meiofaunal community structure in the Eastern Mediterranean: are trenches benthic hot spots? Deep-Sea Research I 51, 833–847.|
|Tyler, P.A. (2003) (ed.) Ecosystems of the World, Vol. 28 Ecosystems of the Deep Oceans, pp 1–569. Amsterdam: Elsevier.|
|Wigham, B.D., Hudson, I.R., Billett, D.S.M. & Wolff, G.A. (2003) Is long-term change in the abyssal Northeast Atlantic driven by qualitative changes in export flux? Evidence from selective feeding in deep-sea holothurians. Progress in Oceanography 59, 409–441.|
|Witte, U., Wenzhöfer, F., Sommer, S., et al. (2003) In situ experimental evidence of the fate of a phytodetritus pulse at the abyssal sea floor. Nature 424, 763–766.|
|Zardus, J.D., Etter, R.J., Chase, M.R., et al. (2006) Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939). Molecular Ecology 15, 639–651.|