The highest within-habitat diversity from all of these samples (slope of the curve within a single habitat) was found in the nematode communities from Håkon Mosby, followed by Gulf of Guinea (Fig. 3). In fact, the steepest slope of the curves generated from the Håkon Mosby data was found among the single-habitat group of replicate samples. These results suggest that the alpha diversity in meiofaunal communities at seeps may be greater than macrofaunal diversity, even though the nematode communities were only identified to the genus level and therefore contain an even greater diversity at the species level. The high level of variability in the slopes of the single-habitat curves for both the nematode genera (Fig. 3) and the meiofauna orders (Fig. 4) from this mud volcano is likely due to the variability in the habitat types with highly heterogeneous control and tubeworm sediments on one hand and strongly nematode-dominated center and reduced-sediment habitats on the other hand. The meiofaunal communities may be responding to small-scale heterogeneity within each habitat, and the use of broad habitat characterizations based on the visual assessment of the communities may mask the microhabitat heterogeneity to which the meiofauna respond. Indeed, nematode assemblages exhibit distinct vertical profiles in the sediment with different taxa in the surface sediments compared to the subsurface sediment fauna, pointing to species-specific distribution patterns at the millimeter to centimeter scales. Similar observations also apply to the macrofauna from CA seep sediments (Levin et al. 2003).
Figure 3. Rate of taxon accumulation across habitats. CA & OR margin macrofauna include species-level data from near-seep sediments, vesicomyid clam beds, oxygen minimum zones, bacterial mats, and background sediments. Gulf of Mexico macrofauna include species-level data from vestimentiferan tubeworm aggregations, mussel beds, and scleractinian coral habitats. Gulf of Guinea nematodes are genus-level data from seep, transition, canyon, and control sediments. Haakon Mosby mud volcano samples are also genus-level nematode meiofauna from bacterial mats, siboglinid-associated sediments from the outer rim of the volcano, and non-seep influenced sediments. The greatest relative diversity response to habitat heterogeneity was found in Gulf of Mexico habitats, and the slowest increase in the rate of species accumulation with increased habitat heterogeneity was found in the nematode fauna of the Haakon Mosby mud volcano.
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Figure 4. Rate of species accumulation across habitats for meiofaunal orders sampled from the Norwegian Margin and Gulf of Guinea. Habitats include seep sediments, siboglinid sediments, bacterial mats, canyon sediments, seep-canyon transition, and control sediments from both regions. This figure demonstrates that at higher levels of taxonomic resolution, the majority of the diversity of the community may be captured by sampling across only two of these habitat types, and adding additional habitats only slightly increases the rate at which orders are accumulated.
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When additional habitats are added to this analysis, the greatest rate of increase in the accumulation of species is found in the Gulf of Mexico habitats (Fig. 3). The high level of beta diversity among the mussel, tubeworm, and coral-associated communities is likely due to the strong differences in habitat chemistry as well as the differences in the structure of the biogenic habitats themselves (Cordes et al. 2008; Buhl-Mortensen et al. this issue). In addition, interspecific interactions (both positive and negative) among the foundation species and the communities they host will contribute to these patterns in diversity (Bergquist et al. 2003; Cordes et al. 2008). These interactions may account for the greater level of species turnover in this example where biogenic habitats exhibit higher rates of species turnover than do habitats from other systems that are primarily defined by geological habitat characteristics.
Following the Gulf of Mexico habitats, both the macrofaunal communities of the Pacific seeps and the meiofaunal nematode communities of the Gulf of Guinea exhibited similar rates of species accumulation as different habitats are added to the analysis. Gulf of Guinea nematode diversity was higher than CA and OR margin macrofaunal diversity, possibly due to the presence of an oxygen minimum zone off of CA and OR, but the slopes of the two relationships were very similar. The similarity in the size fractions of the fauna sampled and the habitat types contained in the investigations likely contributed to the similarity in these patterns.
To examine broader changes in diversity with habitat heterogeneity, the full meiofaunal datasets from Håkon Mosby and Gulf of Guinea were combined and examined at the order level (lowest level of taxonomic resolution). At this broad level, the relationship between diversity and habitat heterogeneity begins to fall off (Fig. 4). Even though these communities are from two locations separated by over 6000 km, the orders capable of colonizing deep-sea seep-related habitats appear to be limited and shared among these communities world-wide, and also appear to include other non-reducing deep-sea communities. Therefore, samples from only two or three habitats can represent a large proportion of the gamma diversity of seep meiofaunal communities at the order level.
Ecological underpinnings of the habitat heterogeneity–diversity relationship
Different sources of heterogeneity can act to shape the path of community assembly in different ways. Recent work in ecology has identified a series of theoretical models to address how communities are assembled as metacommunities and how habitat heterogeneity, as patches of distinct habitat types, might influence this process (Leibold et al. 2004). The four models, species sorting, patch dynamics, mass effect, and neutral theory, all may play a role in the assembly of seep communities, but in different ways and with different intensities.
The species sorting model describes a strong effect of niche specialization where communities are largely structured by habitat characteristics. Habitat patches are theoretically distributed along a gradient of one or more environmental factors and the species are sorted along this gradient into the habitats to which they are best adapted. This form of community assembly has been demonstrated in the clam beds surrounding point-sources of fluids in Monterey Bay, where ‘Calyptogena’ kilmeri inhabits areas of high porewater sulfide concentrations and Calyptogena pacifica (sensuKrylova & Sahling 2006) beds surround the periphery of the ‘C.’ kilmeri zone where sulfide concentrations are lower (Barry et al. 1997; Goffredi & Barry 2002). Infaunal communities of Hydrate Ridge off the coast of Oregon also show a significant response to gradients in sulfide concentration where sulfide increases from background sediments to Acharax beds, Calyptogena beds, and Beggiatoa mats (Sahling et al. 2002). These community changes were related to the dynamics of fluid flow and sulfide concentration, but are also influenced by the seep fauna themselves through sediment irrigation (Treude et al. 2003). Similar changes in clam bed-, bacterial mat-, near seep- and background sediments are reported on the California and Oregon margins (Levin et al. this issue).
Species sorting along geochemical gradients is also demonstrated in the Gulf of Mexico vestimentiferan aggregations, where the distribution of many of the associated species exhibited significant correlations, both positive and negative, with epibenthic sulfide levels (Cordes et al. 2005b). Some of these species appeared to be functionally redundant (similar trophic niches), but were found in different aggregations according to the sulfide levels (different realized niches). More broadly, this concept is demonstrated in the differences among communities sampled in mussel beds consisting of Bathymodiolus childressi with methanotrophic symbionts, tubeworm aggregations of Lamellibrachia luymesi and Seepiophila jonesi with sulfide-oxidizing symbionts, and the deep-water coral Lophelia pertusa without symbionts (Bergquist et al. 2005; Cordes et al. 2008, 2009). Theoretically, the co-occurrence of habitat patches that select for specific communities within a single seep site should lead to increased beta diversity at the site scale as observed for the Gulf of Mexico communities (Fig. 2).
Patch dynamics considers a relatively homogeneous environment where the relative importance of competition and dispersal explain the composition of the community in any one habitat patch. Regional coexistence of species is provided by a tradeoff between competitive ability and dispersal capacity. The weaker competitor may be able to colonize a patch first, but eventually the poor disperser will arrive in the patch and outcompete the first. This theory explains community dynamics where successional processes dominate. An example of this form of temporal dynamics comes from the vestimentiferan aggregations of the Gulf of Mexico. In this system, young tubeworm habitats are colonized by endemic seep species from families common to seeps around the world and are slowly replaced by species common to the surrounding benthos of the Gulf of Mexico (Bergquist et al. 2003; Cordes et al. 2005b). There is also evidence that this pattern of seep succession occurs on geologic time scales. On the Barbados Accretionary Prism, the series of diapiric structures exhibits a variety of different fluid-flow patterns and correspondingly disparate community composition in terms of the relative abundance of vesicomyid and bathymodioline bivalves (Olu et al. 1996). A similar pattern was documented on the mud volcanoes of the eastern Mediterranean where active sites exhibited high methane and particulate flux and slower-flux sites contained greater areas of carbonate crusts (Olu-Le Roy et al. 2004). The relative age of the carbonate build-ups on mound structures in the Gulf of Mexico also greatly influences the types of seep (and non-seep) communities that develop at those sites (Roberts & Carney 1997; Fisher et al. 2007).
The mass effect describes a pattern of species abundance involving source and sink populations. At large or particularly suitable habitats, the population size of a given species will be quite high. This site will serve as a source of propagules dispersing into relatively small habitats where the probability of local extinction is high, or in marginal habitats where recruitment success or adult survivorship is relatively low. A series of localized, marginal habitats could also potentially link widely distributed sources populations. These interspersed ‘sink’ populations could account for the low level of genetic divergence among widely distributed populations of bathymodiolin mussels in the Atlantic basin (Cordes et al. 2007; Olu-Le Roy et al. 2007b; Génio et al. 2008) and vestimentiferan siboglinids on the Atlantic and Pacific sides of the Isthmus of Panama (McMullin 2003). For the meiofauna, the mass effect could explain source-sink exchange between shallow-water and deep-sea reduced environments but does not seem to account for exchange between seeps or reduced environments along adjacent continental margin sites. Indeed, different seeps consist of the same orders of meiofauna (Fig. 3) but only rarely share the same dominant species; rather, these species seem to be primarily derived from more abundant assemblages in shallow-water, organic-rich sediments (Van Gaever et al. 2006, in press, this issue).
Neutral theory predicts that random effects of colonization and extinction will produce observed species distribution patterns, assuming that species and habitat patches are all similar (but not necessarily identical). Because of the relatively strong influence of habitat chemistry on community composition that has been demonstrated in numerous settings, this theory appears to be less applicable to seep ecosystems. However, this theory could apply within certain taxonomic groups if they are assumed to have a certain degree of functional redundancy and similar habitat requirements or environmental tolerances. This model could account for some of the variability in community structure seen in young tubeworm aggregations at the more isolated seep sites in the Gulf of Mexico (Cordes et al. 2006). These vestimentiferan-associated communities did not strictly adhere to the model of community succession and appeared to be a more random accumulation of a subset of the potential pool of seep-endemic species commonly inhabiting the more extensive seep sites in the region. This theory could also apply to the background species that begin to colonize a seep following the reduction in seepage along with concentrations of sulfide and methane. These are often megafaunal predators that may be taking advantage of the elevated biomass at the seeps and potentially transporting seep productivity off site (MacAvoy et al. 2003; Sellanes et al. 2008). This component of the community would be a random accumulation of background species that happened to wander into the seep site and be observed or sampled while they were there. Again, neutral theory would only apply to a subset of the community (non-endemic vagrant species) and a subset of the habitat patches (early successional stages in isolated habitats).
These four models do not represent mutually exclusive hypotheses and could all contribute to our understanding of diversity and its response to habitat heterogeneity (Gravel et al. 2006). The species sorting model appears to most accurately represent the situation found at the seeps and explains a large portion of the previously demonstrated seep species distributions, particularly for the symbiont-bearing species. The patch dynamics model could help explain the successional patterns observed at some sites and the potential for high beta diversity where there were groups of habitat patches in different stages of succession. The mass effect may apply to some areas where sufficient high-density and low-density sites are spread over a large area such as the Gulf of Mexico or the entire Atlantic Basin, but examples of this situation are more rare. The neutral theory, although seemingly diametrically opposed to the species sorting (niche) theory, may also explain the distribution patterns observed at seeps, particularly for the vagrant species (sensuCarney 1994) that colonize the seeps and potentially utilize the increased productivity at those sites. However, we note that assemblages may appear to fit the neutral theory if the appropriate space and time scales or resource dimensions causing species sorting or creating patches are not investigated.
Underlying mechanisms of the diversity response to habitat heterogeneity
If we assume that the most applicable theory of community assembly at seeps is the species sorting model, we may further examine the mechanisms by which species are sorted along environmental gradients. The mechanisms underlying the relationship between habitat heterogeneity and animal biodiversity at seeps are as complex as the seep habitats themselves. Geochemical, geological, and microbial drivers as well as biological interactions are all known to play critical roles in determining species distributions. The processes at play operate over a broad range of space and time scales from cm to many km, and from hours to MY (Fig. 5). On small scales they interact with one another to dictate biological activities as diverse as attraction to settlement, physiological tolerances, feeding mode and diet, life history, and symbioses. In addition, the abiotic factors that enable or inhibit the presence of prey, predator, competitor or symbiont will in turn affect the synecological interactions that determine animal distributions at seeps.
Much of the habitat heterogeneity that we observe at seeps, regardless of its form, is driven by the patchy availability of methane and sulfide. While the geochemical conditions and availability of reduced compounds dictate the suitability of the habitat for the C fixation activities of bacterial symbionts, and thus the nutritional condition of the host invertebrates, they also establish a physiological realm that includes sulfide-tolerant species and excludes intolerant animal species (MacDonald et al. 1990; Barry et al. 1997; Sahling et al. 2002; Levin et al. 2003; Olu et al. 1996, 1997; Olu-Le Roy et al. 2007a). Sulfide gradients appear to affect the spatial distribution of animals horizontally and vertically within the sediment column (e.g.Levin et al. 2003), and to select evolutionarily for the radiation of taxa with sulfide (and low-oxygen) tolerance or detoxification capabilities (Hourdez et al. 2002; Hourdez & Lallier 2007). Sulfide, methane, or the microbes that utilize and produce them, may provide cues for settlement of some species and act as settlement inhibitors of others (Levin et al. 2006). Reduced compounds such as methane and sulfide also fuel a free-living microbial community that provides nutrition (and possibly settlement cues) for a wide array of smaller grazing, deposit feeding and suspension feeding taxa, as well as for bacterivores that may specialize on microbes with specific metabolic pathways or morphologies (Van Dover & Fry 1994; Robinson et al. 2004).
Many of the mechanisms linking heterogeneity to diversity are facilitative. Microbial mats of sulfide oxidizers have been proposed to transform sulfide into inert, non-toxic forms, creating a more favorable microhabitat that facilitates eukaryotic organisms (Gallardo et al. 1994; Brüchert et al. 2003). In addition, microbial consortia of anaerobic methane oxidizers precipitate carbonate, which provides a complex, often extensive hard substrate habitat for seep fauna. Aggregating megafauna form biogenic bushes (tubeworms), beds (bathymodiolin mussels, vesicomyid clams, ampharetid tubes, sponges) or fields (frenulate pogonophorans) that diversify available ecological niches by providing substrate, refuge, and food to a host of small invertebrates that live parasitically, commensally as epifauna, or in loose association (Bergquist et al. 2003, 2005; Turnipseed et al. 2004; Cordes et al. 2005b, 2006). In addition, some of these taxa further act as autogenic habitat engineers through irrigation, burrowing, and symbiont uptake of sulfide, all of which modify chemical conditions in ways that may benefit the free-living chemoautotrophic microbes that feed associated invertebrates and detoxify the habitat for metazoans (Sahling et al. 2002; Treude et al. 2003; Cordes et al. 2003, 2005a; Boetius 2005). The REGAB pockmark site at 3000 m water depth in the Guinea basin near the Congo canyon is one of the few sites where the mechanism underlying the diversity response may be examined in all three size classes of fauna (Sibuet & Vangriesheim 2009). At the pockmark scale, assemblages of vesicomyid and mytilid bivalves and siboglinid tube worms are sorted along gradients in methane fluid flow and substratum variability from the center to the periphery of the pockmark. However, in the central, active area there is also a high level of smaller-scale geochemical heterogeneity driving the distribution of the symbiont-bearing taxa (Ondréas et al. 2005; Olu-Le Roy et al. 2007a). In the central area, the distribution of the foundation species largely controls the relative abundance of the associated megafauna, while larger-scale patterns are generated by gradients in fluid flow and substratum type (Olu-Le Roy et al. 2009). The relative abundance of the macrofauna and meiofauna appear to be greatly influenced by the type of biogenic habitat (Menot et al. this issue, Van Gaever et al. 2009), with the vertical distribution of the infaunal species strongly impacted by the influence of the tubeworms and mussels on the sediment biogeochemistry (Menot et al. this issue). At the seeps along the Nordic Margin, meiofauna communities also show shifts in the proportions of the dominant genera from the siboglinid fields to background sediments (Van Gaever et al. 2006, 2009). Although most of these taxa show a continuous distribution over both habitats (Figs 2 and 3), the increase in abundance suggests that some taxa are better adapted to the more reduced conditions of the siboglinid patches, while others prefer the adjacent control sediments. These investigations suggest that while there are subtle differences in the mechanism underlying the patterns, the response of diversity to habitat heterogeneity is consistent among the different size classes of fauna at seeps as well as in other habitats.