The continental margins, regarded here as the ribbon of sea floor from 200 to 4000 m water depth between the shelf and the abyss, offer some of the most variable terrain in the ocean. This relatively narrow zone, which accounts for about 15% of the seabed, exhibits extreme topographical heterogeneity, sharp environmental gradients, and tectonic activity that together create habitat for a vast assortment of biological communities (Levin et al. 2001). Canyons, vertical walls, banks, ridges, mounds, swales and gulleys criss-cross broad flat slopes (Wefer et al. 2002). Some of these features receive exceptional inputs of floodwaters, macrophytic detritus, suspended organic matter and debris from massive river inflows and long-shore transport. Others are squeezed by subduction or jolted by tectonic activity, triggering turbidity flows and forcing the efflux of reduced fluids that fuel chemosynthetic (seep) ecosystems. Multiple water masses with distinct hydrographic characteristics flow over and across the margins, often stratifying the water column like a layer cake. On some margins, naturally hypoxic waters smother the seabed at mid-bathyal depths (Helly & Levin 2004). Where flow, food, or chemical conditions are suitable, structure-forming biological assemblages thrive, generating additional heterogeneity. In combination, the margins comprise some of the most heterogeneous and dynamic real estate on the planet.
High diversity on continental margins has been recognized since the 1960s (Hessler & Sanders 1967). Many taxa typically exhibit a mid-slope diversity maximum between 1200 and 2500 m (Rex 1983; Stuart et al. 2003) and there is now evidence for high genetic as well as species diversity at these depths (Etter et al. 2005). In recent years there has been an increased emphasis on exploratory programs combining geological and biological operations, driven by the novelty and complexity of margins. Regional and local surveys allowed identification and analysis of environmental variables, benthic processes, and the scales of variability of benthic communities necessary to predict their response to deep-sea industrial activities (Sibuet & Vangriesheim 2009). An appreciation of the highly heterogeneous nature of continental margins has progressively emerged in recent decades, as multibeam bathymetric mapping in combination with submersible and ROV expeditions have revealed a wealth of canyon, seep, organic fall, bank and depositional environments on margins (Sibuet & Vangriesheim 2009; Weaver & Gunn 2009). While there is a general sense that all of this environmental complexity must influence diversity, previous efforts to examine and quantify diversity-heterogeneity relationships have been limited.
This volume is the product of both individual research efforts and synthesis activities resulting from a Census of Marine Life Continental Margin Ecosystems (COMARGE) project workshop held at Scripps Institution of Oceanography, September 7–12, 2008. The goals of the workshop were to examine the roles of habitat heterogeneity in generating and maintaining diversity on continental margins. Thirty-four scientists from 17 countries participated. They shared examples and deliberated over issues including methods for quantifying diversity-heterogeneity relationships, mechanisms underlying the relationships, relevant theory, space and time scales of relevance, consequences of these relationships for ecosystem function, and the conservation and management implications.
A series of synthesis papers explore global heterogeneity-diversity relationships for specific margin habitats including methane seeps (Cordes et al.), oxygen minimum zones (Gooday et al.) and biotic structures (Buhl-Mortensen et al.), and for specific taxonomic groups, the nematodes (Vanreusel et al.) and fishes (Priede et al.). Site-specific studies explore diversity patterns in these habitats, as well as in canyons and on open slopes. These studies bring together for the first time geographically and taxonomically diverse data sets to consider whether there are common habitat influences on patterns of diversity on margins.
Vanreusel et al. compile and analyze nematode genus diversity for soft sediments, manganese nodules, coral, seamounts, cold seeps, hydrothermal vents, canyons and trenches. They examine the extent to which habitat heterogeneity contributes significantly to total deep-sea nematode generic diversity and whether different deep-sea habitats harbor specific nematode assemblages or can be identified as hot spots of biodiversity. Most nematode genera appear to be cosmopolitan. Substrate complexity associated with coral rubble or nodule beds, biochemical gradients associated with seeps and vents, and depth gradients along the slope, all create distinct assemblages, albeit with few unique genera. However factors such as increased substrate complexity in the case of corals and nodules seem to facilitate the co-existence of a high number of genera with different modes of life, from sediment dwelling to epifauna, resulting in a higher alpha diversity.
Priede et al. describe global depth trends in diversity and size of deep-sea fishes and ask whether local heterogeneity along the margin of the temperate NE Atlantic Ocean causes deviations from the global pattern. They find globally that all three classes of fishes, the Agnatha, Chondrichyes and Osteichthyes, exhibit a general logarithmic decrease with depth in the numbers of demersal species. In contrast, along the NE Atlantic margin, trawl and baited-camera data indicate peak species richness at depths of 1100–2000 m. This diversity peak coincides with the depth of the permanent thermocline, the occurrence of Mediterranean overflow water, seasonally strong currents and resuspension of particulate matter, and high pelagic biomass impinging on the slope. Priede et al. postulate that these factors increase habitat and resource heterogeneity, thus supporting a wider range of fish species than predicted from global trends.
Animals themselves are a key source of heterogeneity on a variety of spatial scales. At the smallest scales they can provide substrate or refuge for other organisms, or they can modify the local environment to enhance flux or deposition of food particles, larvae, sediments, etc. However, animal skeletons and spicules can also form larger structures (e.g., reefs, mounds and mats) that create seafloor features at scales of 100s of metres to kilometres. Buhl-Mortensen et al. describe the biogenic habitats formed by sessile organisms on the sea floor, their effects on species diversity, and the influence of the surrounding habitat matrix. They focus on reef-forming organisms such as deep-water corals (e.g. Lophelia), gorgonians and sponges, on solitary taxa such as sea pens and glass sponges, and on large test-forming foraminifera including xenophyophores. The authors find that biotic influence varies with taxon and changes with surface structure and water depth, as well as with age and life status. Temperate, deep-water corals support fewer obligate associates than their tropical shallow-water counterparts, but exhibit high species packing, enhancing regional diversity.
On open slopes, depth often appears as an overriding correlate with changes in faunal communities (Carney 2005). However, the actual sources of depth-related habitat heterogeneity may be hydrographic in nature, associated with water-mass properties such as temperature, salinity or dissolved oxygen, or linked to organic-matter input. Narayanaswamy et al. document differences in macrofaunal composition and generic diversity associated with thermal regimes linked to different water masses in the Faroe-Shetland region of the NE Atlantic. Macrofauna on two cross-margin transects, to the north and west of Shetland, reflected different environmental influences, emphasizing the existence of considerable along-margin heterogeneity. Williams et al. report that megabenthos species composition on the Australian continental slope is shaped by an overlap of Indo-Pacific and temperate Australian faunas, with temperature, oxygen and latitude as key covariates. They propose a hierarchical system for classifying diversity correlates that encompasses biogeographic provinces associated with water masses and current regimes at larger scales, and hard or soft terrain at smaller scales. Notably, rare taxa were less readily characterized with this scheme.
Oxygen minimum zones
Oxygen minimum zones (OMZs) are low-oxygen hydrographic features that bathe the mid to upper slope on continental margins subject to intense upwelling (Helly & Levin 2004; Paulmier & Ruiz-Pino 2008). Several papers in this volume examine how OMZs influence alpha and beta diversity of benthos and how these features interact with other sources of heterogeneity on margins. A synthesis paper by Gooday et al. identifies sources of heterogeneity associated with substrata, oxygen and sulphide gradients, sediments, and organic C on margins with well-developed oxygen minimum zones. In the East Pacific and Indian Ocean they document strong effects of oxygen on alpha diversity of macrobenthos, with high beta diversity at the OMZ upper and lower boundaries. Ingole et al. focus on the western Indian margin where macrobenthos diversity is depressed at mid-slope depths within the OMZ (500–1000 m) but density and biomass are elevated at the upper boundary (100 m). Gooday et al. conclude that, although diversity is depressed within OMZs, the presence of this hydrographic feature probably enhances regional macrofaunal diversity. More information on species distributions is necessary, however, to test this conclusion.
Sellanes et al. offer a comprehensive overview of meio-, macro- and megafaunal trends in abundance and diversity along the Chile continental margin, noting how these change as a function of depth and latitude. Water masses with differing oxygen levels strongly influence all taxa, and local heterogeneity introduced by seep hardgrounds is documented for the megafauna. They show that different body-size groups have different responses, but in the lower OMZ, a water-mass interface between Equatorial Subsurface Water and Antarctic Intermediate Water serves as a hotspot for abundance and diversity.
Like the Chile margin, the continental margin of the US Pacific Northwest is overlain by an oxygen minimum zone and punctuated by methane seepage. Levin et al. examine the effects of these two sources of heterogeneity, independently and combined, on the macrobenthos. Methane seepage, and the associated microhabitats (clam beds and microbial mats), act to enhance margin diversity at the scale of habitat (tens of meters) and geographic setting (100 km), with about 50% of species being seep-endemic. However, the additional presence of an OMZ overlying the seep did not dampen diversity enhancement, as was originally predicted by the authors.
Methane seeps are increasingly recognized as major sources of heterogeneity at bathyal depths on the continental margins of all ocean basins (Sibuet & Olu 1998; Sibuet & Olu-Le Roy 2002). They can result from the enhanced burial of organic matter, the conversion of this OM to hydrocarbons (oil, asphalt, methane gas or gas hydrate), and its release or destabilization at the sea floor. The seeps themselves are highly heterogeneous, with varied fluid-flow regimes that support different structure-forming (foundation) species, which themselves give rise to habitats (e.g., bacterial mats, clam and mussel beds, pogonophoran fields, and tube-worm bushes) with many associated invertebrates (Levin 2005; Cordes et al. 2009).
Cordes et al. provide an overview of sources of heterogeneity at cold seeps and consider their influence on diversity. They develop a new approach to assessing the contribution of this remarkable heterogeneity to regional (gamma) diversity using the slope of accumulation curves generated for successively higher numbers of habitats within a region. This approach is applied to different faunal size classes and geographic settings. Diversity responses appear to be strongest at the local (alpha) level in meiofaunal communities, while for macrofaunal communities the beta-level diversity response was greater, as different types of biogenic habitats are incorporated. These patterns are considered in a metacommunity context, and are found to be consistent with species adaptation among habitats, i.e., a niche differentiation model. Van Gaever et al. examine the influence of habitat heterogeneity on seep nematode generic diversity at three spatial scales (metres, 100s of metres, 100s of kilometres). They partition gamma diversity on the Norwegian margin into alpha and beta contributions and demonstrate strong habitat (siboglinid patch, bacterial mat, reduced sediment) contributions to nematode genus diversity, with some genera exhibiting habitat-specific distributions. Menot et al. also identify strong habitat influence on macrofaunal abundance and diversity in a methane pockmark in the southern Gulf of Guinea. They highlight the fact that, although individually the siboglinid, vesicomyid and mytilid bed habitats exhibit low alpha diversity, they support different species and thus in combination contribute to high beta diversity.
Submarine canyons are widespread features on most of the ocean’s continental and island margins. Canyons differ from typical open slopes in having steep or rugged topography, multiple types of hard and soft substrate, and regions of accelerated waterflow in some cases including turbidity currents. They often act as sinks for particulate materials, including macrophytic debris, organic-rich sediments, and particle-bound pollutants, moving along shore and across shallow platforms. Canyons typically span a broad depth range from the shelf to the abyss acting as conduits of material from the coastal zone to the deep sea. Recent advances in mapping tools (multibeam sonar, ROVs, imaging systems) have revealed significant habitat heterogeneity in canyons (Schlacher et al. this volume; Tyler et al. 2009), substantially advancing understanding of how this heterogeneity influences diversity. Megabenthos studies by Ramirez-Llodra et al. reveal spatially varying assemblages in different canyon zones, but limited enhancement of densities relative to open slope environments. Ramirez-Llodra et al. examine the megabenthos composition and diversity in Blanes Canyon and the adjacent slope in the NW Mediterranean Sea. They find assemblage differences between the canyon head, wall and slope, with polychaetes dominant inside the canyon. The strong overprint of 50 years of trawling appears to have homogenized the system. These results suggest that humans can strongly alter the contributions of natural topography to margin heterogeneity. In a study of submarine canyons on oceanic islands in the Hawaiian archipelago, Vetter et al. demonstrate that the canyons exhibit enhanced megafaunal abundance and species diversity on local scales, particularly for mobile species. Numerous species are present only in canyons, not on the open slope, increasing beta diversity and supporting the hypothesis that canyons function as biodiversity hotspots and enhance regional (gamma) diversity. They conclude that on margins of islands embedded in relatively oligotrophic ocean waters, submarine canyons may provide keystone habitats. Schlacher et al. examine the biota in submarine canyons of SE Australia at upper slope depths. They find strong assemblage variations between canyons, despite evident seafloor substrate homogeneity. Bryozoan thicket and sponge distributions are linked, perhaps because the former provides attachment sites for the latter. Bottom cover of sponges is positively correlated with species richness of sponges and other biota. Because they are also sensitive to fishing disturbance, Schlacher et al. suggest that estimates of sponge and bryozoan cover could provide good proxies for diversity assessments.
Together, these studies reveal that habitat heterogeneity in canyons, created by extreme topography, diverse current regimes and substratum types, and detrital funneling, exerts a powerful influence on biotic diversity. However, recent research suggests that each canyon has unique environmental characteristics such that canyons as a group have highly variable effects on community structure and biodiversity. This variability, together with rugged terrain that makes canyons particularly difficult to study, means that we are only just beginning to understand how these important features contribute to the diversity of continental margins.
The study of continental margin heterogeneity, including its link to faunal diversity, is still in its infancy. We do know that depth and food input often show strong relationships with diversity (superseding many other environmental forces), but the mechanisms behind these relationships remain unclear. Almost nothing is known about the effects of heterogeneity on microbial diversity, although recent molecular work is providing some clues (Lecroq et al. 2009). Much of the current research is directed at the sources of heterogeneity we can perceive with our own senses. However, the coexistence of multiple species of closely related taxa in environments that appear homogeneous (e.g. siboglinids in the Gulf of Cadiz or dorvilleids at Pacific seeps) suggest that the organisms experience and partition the habitat based on sources of heterogeneity that we cannot see or detect with our current tools, or that non-equilibrium dynamics are more important than we appreciate.
The importance of understanding controls on continental margin diversity is growing as these regions experience increasing anthropogenic influence. Margins provide key ecosystem functions, such as carbon sequestration, nutrient cycling and biodiversity maintenance, as well as services that include provision of living and energy resources. Both overt activities, in the form of trawling, predator removal, energy extraction, mining and waste disposal, and more insidious climate change effects in the form of warming, deoxygenation and acidification, are likely to alter existing patterns of biodiversity and ultimately ecosystem functions (Danovaro et al. 2008; Smith et al. 2008a,b; Levin & Dayton 2009; Sibuet & Vangriesheim 2009). Understanding how both natural and human-induced sources of habitat heterogeneity shape margin communities and ecosystems is fundamental to conservation of margin resources, and to the development of indicators and proxies that can aid large-scale management practices.
The editors would like to acknowledge the Sloan Foundation and the ‘COMARGE Project of the Census of Marine Life’ as well as the Total Foundation for workshop and publication support. We also thank Lenaick Menot and Robert Carney for their significant organizational and administrative contributions to the COMARGE program and workshops. We also thank Maria Cristina Gambi for serving as oversight editor for four of the volume papers, and Jennifer Gonzalez for help with manuscript preparation and special volume administration.