macro-ecology of gulf of mexico cold seeps

ANRV396-MA01-07 ARI 4 November 2008 7:55

Macro-Ecology of Gulfof Mexico Cold SeepsErik E. Cordes,1 Derk C. Bergquist,2

and Charles R. Fisher3

1Biology Department, Temple University, Philadelphia, Pennsylvania 19122;email: [email protected] Resources Research Institute, South Carolina Department of Natural Resources,Columbia, South Carolina 29201; email: [email protected] Department, Pennsylvania State University, University Park, Pennsylvania 16802;email: [email protected]

Annu. Rev. Mar. Sci. 2009. 1:143–68

First published online as a Review in Advance onAugust 28, 2008

The Annual Review of Marine Science is online atmarine.annualreviews.org

This article’s doi:10.1146/annurev.marine.010908.163912

Copyright c© 2009 by Annual Reviews.All rights reserved

1941-1405/09/0115-0143$20.00

Key Words

chemosynthesis, symbiosis, succession, siboglinidae, bathymodiolin, upperLouisiana slope

AbstractShortly after the discovery of chemosynthetic ecosystems at deep-sea hy-drothermal vents, similar ecosystems were found at cold seeps in the Gulf ofMexico. Over the past two decades, these sites have become model systemsfor understanding the physiology of the symbiont-containing megafaunaand the ecology of seep communities worldwide. Symbiont-containing bi-valves and siboglinid polychaetes dominate the communities, including fivebathymodiolin mussel species and six vestimentiferan (siboglinid polychaete)species in the Gulf of Mexico. The mussels include the first described ex-amples of methanotrophic symbiosis and dual methanotrophic/thiotrophicsymbiosis. Studies with the vestimentiferans have demonstrated their po-tential for extreme longevity and their ability to use posterior structures forsubsurface exchange of dissolved metabolites. Ecological investigations havedemonstrated that the vestimentiferans function as ecosystem engineers andidentified a community succession sequence from a specialized high-biomassendemic community to a low-biomass community of background fauna overthe life of a hydrocarbon seep site.

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GoM: Gulf of Mexico

ULS: upper Louisianaslope

GC: Green Canyon

Cold seeps are common deep-water habitats on the continental slope and rise worldwide (asreviewed in Sibuet & Olu 1998, Tyler et al. 2003). Cold seeps occur from the coasts of Chile,Peru, and Costa Rica to southern California and Oregon and continue north to the Aleutiansubduction zone in the eastern Pacific. In the western Pacific, some of the deepest seeps in theworld occur from Kamchatka (Mironov 2000) south past Japan to New Zealand (Lewis & Marshall1996). In the Indian Ocean, seeps are known from the coast of Pakistan (von Rad et al. 2000) andfrom recent discoveries off the coast of Indonesia and the Bay of Bengal ( J. Brooks, personalcommunication). In the Atlantic, seeps occur off the coast of Brazil, near Barbados, the BlakeRidge off the Carolinas, the Laurentian Fan, the Haakon Mosby mud volcano off the coast ofNorway (Vogt et al. 1999), the Gulf of Cadiz (Pinheiro et al. 2003), the Mediterranean, the Seaof Marmara (Zitter et al. 2008), and the coasts of Angola (Olu-Le Roy et al. 2007) and Nigeria(Cordes et al. 2007a).

The hydrocarbon and saline seeps of the Gulf of Mexico (GoM) contain some of the mostwell-described seep communities in the world. The presence of gas and oil in surficial sedimentson the upper continental slope off the coast of Louisiana was first discovered in gas samples fromfour underwater vents (Bernard et al. 1976). Geochemical characterization of these sites followedin the mid-1980s with the description of petroleum, hydrocarbon gasses (Anderson et al. 1983),and methane hydrate (Brooks et al. 1984) from piston cores taken in acoustic-profile wipe-outzones overlying areas impacted by salt diapirism. The descriptions of the geology of the seeps onthe upper slope coincided with the discovery of chemosynthetic communities along the FloridaEscarpment (Paull et al. 1984, Paull et al. 1985). Subsequent trawling surveys of the seeps ofthe upper Louisiana slope (ULS) revealed similar communities composed of “vent-type” taxa(Kennicutt et al. 1985, Brooks et al. 1987). Since then, the upper slope GoM seeps have beenthe subject of numerous research programs that described the geology and geochemistry of thehabitat and the physiology and ecology of the autotrophic and heterotrophic fauna.

Here we present an overview of the macro-ecology of the well-known seeps of the GoM withthe hope of providing a framework to guide future investigations in this model system and in otherless-known, or as-yet-unknown, seep systems. This summary comprises the current state of knowl-edge of the seeps of the northern GoM (Figure 1), focusing on the physiology and ecology of thesymbiotic organisms that inhabit the seeps and the diverse heterotrophic macro- and megafaunaassociated with them. In the interest of space we have excludied potentially significant links to themeiofaunal and foraminiferal communities and the rapidly expanding body of work on the micro-bial ecology of cold seeps. We further focus on the sites along the upper continental slope becauseof the greater abundance of published information from sites in less than 1000-m water depth.Increasing support for studies of deeper sites has accompanied the increasing energy-industryactivities at depths greater than 1000 m. Although the literature on the deeper sites is relativelyscant, it is becoming apparent that there are many basic similarities, as well as some fundamentaldifferences, between the deeper-living communities and those found on the upper slope. Most ofthe seep sites in the northern GoM are named for the Mineral Management Service (MMS) leaseblock in which the site was discovered (for example, a site named GC 140 would refer to a sitelocated in block 140 in the Green Canyon lease area) and we refer to sites using these designations.

GEOLOGICAL SETTING

The widespread seepage of hydrocarbons and brines on the continental slope of the GoM is largelydriven by the process of salt tectonics. The GoM was originally formed during the late Triassic(Sassen et al. 2001), but during the middle Jurassic the opening to the Atlantic was closed (Pindell1985). Extensive evaporation followed, leaving behind a thick salt sheet, the Louann salt formation,

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VK 825/826

MC 853

MC 798MC 885

MC 929

GC 204

GC286

GC 232

GC 233

GC 234

GC 140

GC 185

GC 228

GC 272

GC 533

GC 354GB 535

GB 543

GB 544

GB 382

GB 424

GB 425

GB 388

MC 709

0 200 320030002800260024002200200018001600

Depth contours (m)

140012001000800600400

GC415

Figure 1Location of the known chemosynthetic communities of the upper slope (<1000 m) of the Gulf of Mexico. The area shown is delimitedby the box in the inset image of North America. Depth contours are in meters. Site labels are according to U.S. Mineral ManagementService oil lease block designations: GB is Garden Banks, GC is Green Canyon, MC is Mississippi Canyon, and VK is Viosca Knoll.

on the basement of the GoM (Brooks et al. 1987). Additional evaporite formation appears to haveoccurred approximately 55–50 Mya during the Paleocene and Eocene as the Caribbean platemoved to the east across the region (Rosenfeld & Pindell 2003). By the early Miocene, approx-imately 21 mya, the deposition of large volumes of siliciclastic sediments onto the salt layerbegan (Kennicutt et al. 1992, Sassen et al. 1994a). As these sediments accumulated they com-pressed and formed a thick layer of sandstone and shale over the salt basement (McGookey 1975),preventing the further migration of hydrocarbons from deeply buried Mesozoic source rocks(Kennicutt et al. 1992). Differential loading of sediments on the continental shelf caused the saltsheet to migrate down along the continental slope and deform into vertically mobile pillars andsalt domes (Humphris 1979). Salt diapirs subsequently pierced and cracked the shale and sediment

www.annualreviews.org • Macro-Ecology of Gulf of Mexico Cold Seeps 145

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MC: MississippiCanyon

overburden (Brooks et al. 1987, Aharon et al. 1992), causing the migration of trapped hydrocar-bons (Kennicutt et al. 1988), some of which reach the sea floor. This process of salt tectonicsdominates the geology of the northern GoM, particularly in the areas of most intense seepage onthe ULS.

As oils migrate through the sediment column, they are altered by geologic and biologic pro-cesses, which leads to variability in the abundance and types of reduced chemicals that reach thesediment surface (Figure 2). Thermal cracking of kerogen leads to the production of petroleumhydrocarbons and natural gas. Continued heating of these products generates smaller straight-chain and aromatic hydrocarbons, organic acids, hydrocarbon gasses, and carbon dioxide (Seewald2003). Microbial degradation of hydrocarbons generates organic acids (most commonly acetate)that may then be further metabolized into methane (Ficker et al. 1999, Kleikemper et al. 2002).Methanogenesis can also occur through the metabolism of buried organic material (Martenset al. 1991) or in shallow sediment layers through the bicarbonate-based methanogenesis pathway(Bi-MOG) (Orcutt et al. 2005).

Hydrogen sulfide is often present in the seeping fluid at the sea floor, and can originate fromseveral sources (Figure 2). Alteration of sulfur-rich hydrocarbon endmembers can produce sulfide(Kennicutt et al. 1992), as can microbial metabolism of buried organic material (Martens et al.1991, Carney 1994). Sulfide may also be derived from the interaction of dissolved gaseous-phaseor liquid hydrocarbons with anhydrite and gypsum contained in salt-dome cap rocks or sulfate-bearing evaporites (Sassen et al. 1994b, Saunders & Thomas 1996, Roling et al. 2003). However,the majority of the sulfide present at the sea floor in the GoM cold seeps is generated in theshallow subsurface by the anaerobic oxidation of methane, higher hydrocarbons, and organicmaterial using sulfate as an oxidant (Aharon & Fu 2000, Arvidson et al. 2004, Joye et al. 2004).Once sulfide and methane reach the sediment surface, they provide the energy that supportshigh-biomass microbial and animal communities at the seeps.

Individual seepage sites are located on mounds or in grabens associated with subsurface saltstructures. The relative age of a seepage source is generally related to the amount of carbonateprecipitation that has occurred at the site (Roberts & Carney 1997, Sager et al. 1999, Sager et al.2003, Fisher et al. 2007). Geologically young mound structures on the ULS exhibit active fluidventing often associated with sediment transport, giving rise to the term mud volcanoes for themost active of these sites. In this setting, fluids migrate along vertical faults and can maintaindistinct temperature anomalies as they travel to the sea floor (MacDonald et al. 2000, Joye et al.2005). The crest may consist of a large crater filled with either unconsolidated sediments orbrine (Prior et al. 1989, MacDonald et al. 2000, Sassen et al. 2003, Joye et al. 2005). Sedimentinstability limits or precludes the attachment of most of the seep fauna that require hard substratafor settlement (Roberts & Neurauter 1990). Rather, the fauna of mud volcanoes is dominated bybacterial mats and mobile chemosynthetic clams (MacDonald et al. 1990a, Powell et al. 2002),and in some instances, the mussel Bathymodiolus childressi, as observed at sites in GC 204 (Milkov& Sassen 2003) and Mississippi Canyon (MC) 709 (Sassen et al. 2004).

−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→Figure 2Box model showing the interactions among some of the ecological and biogeochemical components of upper Louisiana slope seeps.Rectangles correspond to state variables and hexagons correspond to processes. Arrows show the direction of transformation: +indicates a positive effect and − indicates a negative effect. Arrows end at a process if they indicate an effect on the process itself, or passthrough the process if they indicate a link between two state variables via a process. The darkest shade of blue representsbiogeochemical processes, medium blue includes biological interactions, and light blue includes community-level ecological processes.DIC, dissolved inorganic carbon.


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MethanogenesisAnaerobicmethaneoxidation

Porewatermethane

+ –

Diffusion andmigration

Diffusion andmigration

Surficialmethane

Hydrates

Dissolution

+

+

+

+

Methane

+

+

+

Porewater DIC

Precipitation

Non-porouscarbonates

Porous crustsand cemented

sediments

+

+

Calcium

carbonate

Porewatersulfide

Seawatersulfate

Surficialsulfide

Diffusion

Porewatersulfate

Precipitation

Trapping andaccumulation

Sulfatereduction

+

Sulfide

–

–

–

–

+

+–

+ +

1° Consumers 2° Consumers

Youngaggregation

Oldaggregation

RecruitmentRecruitment

Bed

Symbioticproduction Symbiotic

production Growth

+

+

+

+

++

Growth

Primaryproduction

+

Methanotrophic

mussels

TubewormsFree-living

microbes

+

+

+

+ +

Secondaryproduction

1° Consumers 2° Consumers

Secondaryproduction

Endemic consumers

–

++

––

+

+ +

+++

–

++

–

–

–

– –

Microbialbiomass

–

+

Predation

Recruitment

Nonendemic consumers

–

++

+

+++

Predation

–

Recruitment


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GB: Garden Banks

Carbonate precipitation slows fluid flow and provides a stable substrate for recruitment of otherfauna (Figure 2). Authigenic carbonate precipitation is a consequence of the rise in alkalinityand dissolved inorganic carbon (DIC) concentration resulting from anaerobic methane oxidation(Aharon & Fu 2000, Boetius et al. 2000). Early on, carbonates form in sediment pore spaces,reducing porosity and eventually forming small nodules, clasts, and cements (Aharon et al. 1997),as evidenced by low degrees of reflectance and backscatter in acoustic profiles (Sager et al. 1999,Sager et al. 2003). The crests of the mounds can remain active, often with visible methane bubblestreams and oil-stained sediments (Sassen et al. 1993).

Gas hydrate accumulations may also serve to mitigate the escape of gas from sediments byforming in areas of the most active venting (MacDonald et al. 2005). Hydrates are ice-like clathratesof methane and other gases within a water molecule lattice (Sassen et al. 2001). Hydrates formunder high-pressure and low-temperature conditions at depths between 440 and 2400 m in thenorthern GoM (Sassen et al. 1999). These structures may crystallize in the pore spaces of sedimentsto form small nodules, or may accumulate as massive vein-filling structures where gas migrationis most rapid (Milkov & Sassen 2003). Time-lapse photography of small sea-floor-breaching gas-hydrate accumulations at the Bush Hill site showed changes in hydrate morphology over thecourse of a single year (MacDonald et al. 2003). Larger hydrate structures may form barriers toseepage, collecting hydrocarbon gasses beneath them (MacDonald et al. 1994). If the gas becomesoverpressurized, a catastrophic release may result in the formation of sea floor pockmarks andoverturned carbonate blocks (Prior et al. 1989).

Mounds in intermediate stages, with continued seepage of reduced chemicals, precipitation ofcarbonate substrates, and gas hydrate accumulations, often harbor well-developed chemosyntheticcommunities. Bush Hill, in GC 185, is one of the best known of these sites. The small hill isthe site of carbonate accumulation on top of a conical diapir rising from a depth of 580 m toapproximately 540 m (MacDonald et al. 1989). The diapir is either a sea-floor-piercing muddiapir (Neurauter & Bryant 1990) or a dormant mud volcano (Milkov & Sassen 2003) overlyinga salt tongue that is part of a larger salt dome beneath GC 140, 184, and 185 (Sager et al. 2003).Carbonates on Bush Hill have been aged at between 3.2 and 1.4 kya (Aharon et al. 1997), whichprovides some indication of the general age of similar young features (Sager et al. 1999). At thecrest of the hill are oil-stained sediments, gas hydrate, bacterial mats, and active methane bubblestreams, along with numerous distinct vestimentiferan (siboglinid polychaete) aggregations andbathymodiolin mussel beds (MacDonald et al. 2003). The distribution of mussel beds is correlatedto methane concentration in the epibenthic layer, whereas vestimentiferan tubeworm distributionis correlated to the total amount of extractable organic matter (often in the form of oil) in thesediments (MacDonald et al. 1989). On the western edge of this mound are hard substrata withgorgonian (Callogorgia americana delta) and a few isolated scleractinian (Lophelia pertusa) coralcolonies (MacDonald et al. 1989).

Other well-known sites that fit this profile include the large, complex sites at GC 272 andGarden Banks (GB) 424/425. A pair of mounds forms the site at the border between GB 424and 425 (Sager et al. 2003), and a crater at the crest maintains a distinct temperature anomaly,up to 26.7◦C, at the sea floor (MacDonald et al. 2000, Joye et al. 2005). The GC 272 site is alarge fault scarp (Kohl & Roberts 1994) on the western flank of a large mound centered in GC273 (Sager et al. 2003). At both of these sites, soft-sediment seepage areas are dominated by bedsof vesicomyid, lucinid, and thyasirid clams (MacDonald et al. 1990a, Sassen et al. 1993, Powellet al. 2002), whereas outcropping authigenic carbonates are often occupied by bathymodiolinsand vestimentiferans (Sassen et al. 1993, Nix et al. 1995, MacDonald et al. 2000).

As authigenic carbonate precipitation progresses, nodules and shell debris may become ce-mented together (Aharon et al. 1997) and thicker crusts and boulders begin to develop (Roberts


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VK: Viosca Knoll

& Aharon 1994, Sager et al. 1999). At this stage, faults may become occluded and seepage slows. Aseepage site may eventually become entirely cemented over, its existence only manifest as a thickcap of carbonate with a light δ13C signature (Sager et al. 1999). One of the best known of theseolder mounds is a site in GC 140. This site is a massive deposit of authigenic carbonate overlyingthe main body of the salt structure that forms the mounds at GC 140, 184, and 185 (Bush Hill)(Roberts et al. 1990, Sassen et al. 1993). Carbonates at this site have been estimated to be between200 and 13 kyr old (Roberts & Aharon 1994). Continued salt migration has led to faulting onthe flanks of the mound, removing overlying sediment layers and overturning carbonate blocks,resulting in randomly oriented carbonate outcrops (Roberts & Aharon 1994) and occasional smallgas seeps (Aharon et al. 1997, Roberts et al. 2000). The gas seeps are commonly covered withbacterial mats (Sassen et al. 1993, Mills et al. 2004, Gilhooly et al. 2007), and microbial methaneoxidation results in thinner authigenic crusts cementing the larger blocks together (Roberts et al.1990, Roberts & Aharon 1994). Isolated vestimentiferans have been reported at 290 m depth in thislease block, the shallowest record for vestimentiferan tubeworms in the GoM (Roberts et al. 1990).

Two similar mounds are located at GC 354 (Kennicutt et al. 1988) and Viosca Knoll (VK)826 (MacDonald et al. 1990a). The crests of these mounds are covered with a thick authigeniccarbonate layer and large blocks of outcropping carbonate. VK 826 contains some of the mostwell-developed colonies of L. pertusa known in the GoM (Schroeder et al. 2005, Cordes et al.2008). Less extensive hard coral structures are present at GC 354, and this site harbors diverseoctocoral communities. On the flanks of both mounds are large, roughly rectangular, crackedcarbonate blocks. Vestimentiferan aggregations and bacterial mats are associated with many ofthese blocks where sulfide-rich fluids migrate along the subsurface channels associated with theiruplift (Cordes et al. 2006). See sidebar, Deep-Water Coral Communities.

Subsurface faulting in the areas between bathymetric highs on the sea floor may generateadditional seep sites in the form of grabens or half grabens (MacDonald et al. 1990a, Sassenet al. 1993, MacDonald et al. 2003). Sediment slumping related to salt withdrawal may exposegas hydrates or organic-rich sediment layers, leading to reducing conditions and additionalcold-seep habitats (Carney 1994; Sassen et al. 1999). Whereas these habitats may occasionally beassociated with free-venting methane gas emerging from the sediment surface, they are generallymore influenced by petroleum hydrocarbons (Sassen et al. 1994a). The increased abundance ofvestimentiferans over bathymodiolins at these sites is likely due to slower seepage rates of hydro-carbons, which leads to an increased amount of time for subsurface hydrocarbon degradation bymicrobes coupled to the production of hydrogen sulfide (Sassen et al. 1994a, Cordes et al. 2005a).

DEEP-WATER CORAL COMMUNITIES

Chemosynthetic communities are just one of the community types that inhabit the hard-ground habitats of the Gulfof Mexico. Once seepage of hydrocarbons and sulfide has declined, and relict seeps are represented primarily byauthigenic carbonates, deep-water corals may colonize these substrata. In 1955 a trawl in the Viosca Knoll region wasretrieved that contained approximately 150 kg of the colonial scleractinian Lophelia pertusa (Moore & Bulis 1960).In the Gulf of Mexico, 63 species of azoozanthellate scleractinians have been reported in total, the majority ofwhich are solitary corals (Cairns et al. 1993). On the upper slope, L. pertusa forms the most extensive reef structuresalong with the scleractinian Madrepora oculata and a number of species of gorgonian, antipatharian, and bamboocorals (Schroeder et al. 2005). The faunal communities associated with these structures consist mainly of the generalbackground fauna of the Gulf of Mexico, but also contain a few species that may have specific relationships withthe corals and a few species that are common to both coral and seep habitats (Cordes et al. 2008).


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An example of this kind of system is in the GC 234 lease block, one of the most well-developed,extensive areas of seep communities on the ULS (Kennicutt et al. 1988, MacDonald et al. 1990a).GC 234 lies on top of a fault scarp that runs roughly east-to-west (Sager et al. 2003) to form a halfgraben surrounded on three sides by steep escarpments (MacDonald et al. 2003, Milkov & Sassen2003). Several faults cutting through the area have resulted in numerous discrete seepage sites(Sager et al. 1999) and outcropping vein-filling gas hydrates (Sassen et al. 1999). The broad areaimpacted by this system has resulted in extensive areas of outcropping authigenic carbonate thatprovide ample substrata for the development of chemosynthetic communities (MacDonald et al.1990a, Bergquist et al. 2003a, MacDonald et al. 2003) as well as gorgonian and L. pertusa colonies(Cordes et al. 2008). A number of distinct bathymodiolin beds and contiguous vestimentiferanaggregations cover hundreds of square meters (MacDonald et al. 1990a, 2003; Bergquist et al. 2002,2003a). This fault scarp extends into adjacent lease blocks (Sager et al. 2003) and re-emerges atthe sediment surface at GC 232 to form an additional rich but smaller chemosynthetic community(Cordes et al. 2005b, 2006).

If the salt structures that cause sediment faulting are in relatively shallow subsurface layers,dissolution of the evaporite by overlying seawater may occur, resulting in the formation of densebrine with salinities up to 130 ppt (MacDonald et al. 1990b, Aharon et al. 1992, Joye et al. 2005).Brines often contain high concentrations of methane and other hydrocarbon gasses, but little orno sulfide (Nix et al. 1995, MacDonald et al. 2000, Joye et al. 2005). Surface manifestation ofbrine seeps may be limited to small, darkly colored depressions, or the dense seeping fluids mayaccumulate in large pools and rivers along the sediment surface (MacDonald et al. 1990b). One ofthe most striking brine features of the ULS is Brine Pool NR1 in GC 233 (Figure 3). This was apockmark likely formed from the rapid sublimation of a large volume of gas hydrate (MacDonaldet al. 1990b). The brine originates from a shallow (<500 m) subsurface salt diapir and collects inthe depression formed by the blowout event. The pool is approximately 22 m long and 11 m widewith overflow on the southern edge of the pool (MacDonald et al. 1990b). The hypoxic brinecontains high concentrations of methane and bubbles rise from the pool. Most of the shoreline isinhabited by a wide band of the mussel B. childressi (MacDonald et al. 1990b). Most other brineseep sites are dominated by more diffuse surface expressions of seepage. GC 204 contains areas ofrapid fluid transport related to active salt tectonism, which results in brine and methane hydratein surficial sediments (Milkov & Sassen 2003) that are inhabited by beds of B. childressi. In GB382, MC 885, and MC 929, active seepage of brines that contain elevated metal concentrationsleads to the formation of barite chimneys in addition to anhydrite and carbonate crusts (Fu et al.1994, Roberts & Aharon 1994). Isolated B. childressi mussel beds often surround small (1–2 m2)mud volcanoes at these sites (Fu et al. 1994, Kohl & Roberts 1994). Another large brine poolwith small mixed Bathymodiolus species mussel beds and patches of partially buried spatangoid seaurchins around the periphery was recently discovered at 2340 m depth in Alaminos Canyon 601(Fisher et al. 2007, Roberts et al. 2007).

SYMBIOTIC FAUNA

Different surface expressions of seepage are associated with different types of biota depend-ing on their physiological requirements. Two groups of megafauna with symbiotic thiotrophicand/or methanotrophic bacteria dominate: vestimentiferan tubeworms in the polychaete familySiboglinidae, and bivalves, including bathymodiolin mussels and multiple families of clams. Thevestimentiferan siboglinids and clams harbor microbial endosymbionts that utilize sulfide as anenergy source, whereas different species of bathymodiolin mussels harbor either methanotrophic,thiotrophic, or both types of symbionts. The basic physiology of vestimentiferans and symbiotic


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Figure 3The shoreline of Brine Pool NR1. The interface of the dense hypersaline brine and the overlying seawater isclearly shown, with the beds of mussel Bathymodiolus childressi along the shoreline. Photo courtesy ofStephane Hourdez.

clams was revealed by studies of vent taxa, but was greatly expanded by investigations of seepspecies. However, the majority of our knowledge of bathymodiolin physiology comes from stud-ies of GoM species. In waters shallower than 1000 m in the GoM, three species of vestimentiferantubeworms, three species of bathymodiolin mussels, and at least six species of lucinid, thyasirid,solemyid, and vesicomyid clams are known. On the lower slope at least an additional three species ofvestimentiferans and two additional species of bathymodiolins are known. The recent explorationof the Campeche Knolls (3000 m depth) in Mexican territorial waters of the GoM (MacDonaldet al. 2004) led to the discovery of one vestimentiferan, one bathymodiolin, one vesicomyid, andone solemyid species whose taxonomic status remains unresolved.

Tubeworms

Vestimentiferan tubeworms were originally described as a separate phylum related to the phylumPogonophora ( Jones 1985). More recent genetic analyses have placed these two groups together,with the symbiont-containing whale-bone specialist Osedax spp. in the family Siboglinidae in thepolychaete order Sabellida (Black et al. 1997, McHugh 1997, Rouse 2001, Rouse et al. 2004).On the upper slope of the GoM (Figure 4), one species of lamellibrachid, Lamellibrachia luymesi(Gardiner & Hourdez 2003), two species of escarpids, Seepiophila jonesi (Gardiner et al. 2001), andan undescribed species (McMullin et al. 2003) are known. On the lower slope two undescribed


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Figure 4Aggregations of the tubeworms Lamellibrachia luymesi and Seepiophila jonesi. Young and actively growingaggregations are lighter in color whereas older, slower growing tubeworms are colonized by hydroids andother epifauna and appear darker in color. Also shown in the foreground is a colony of the gorgonianCallogorgia americana delta. Photo courtesy of Katherine Luley.

species of lamellibrachids (Brooks et al. 1990, Nelson & Fisher 2000, Cordes et al. 2007a, Robertset al. 2007) and Escarpia laminata are known ( Jones 1985).

All vestimentiferans lack a digestive tract as adults and rely on internal, sulfide-oxidizing bacteriafor their nutrition (Fisher 1990). The mode of transfer of nutrients to the host may involveintracellular digestion of symbionts (Bosch & Grasse 1984), release of metabolites by the symbionts(Felbeck & Jarchow 1998, Bright et al. 2000), or both processes (Bright & Sorgo 2003). Symbiontsare acquired de novo by each successive generation and the symbiont strain is determined bothby location and host species. For example, L. luymesi and S. jonesi on the upper slope possess verysimilar symbionts, whereas E. laminata from Alaminos Canyon harbors symbionts from a differentclade than E. laminata from the Florida Escarpment (Nelson & Fisher 2000, McMullin et al. 2003,Thornhill et al. 2008). There is evidence from juveniles of one or more vent vestimentiferans thatthe symbionts are taken up by early juvenile stages across the body wall (Nussbaumer et al. 2006),although this has not been tested in seep siboglinids.

The symbionts are intracellular within host bacteriocytes, which in turn are housed in aninternal organ, the trophosome. Trophosome tissue is highly vascularized and the vascular systemcontains hemoglobins capable of reversibly binding both oxygen and sulfide (Arp & Childress 1981,Jones 1985, Flores et al. 2005). Hydrothermal vent tubeworms, such as Riftia pachyptila, obtainboth oxygen and sulfide across the plume surface from areas where sulfide-rich hydrothermaleffluent actively mixes with oxygenated ambient sea water (Arp et al. 1987). Conversely, adult


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L. luymesi acquires sulfide from porewater sources using a posterior extension of its body and tube,the root ( Julian et al. 1999, Freytag et al. 2001). Laboratory studies have shown that this speciescan obtain sufficient sulfide across the roots to fuel net autotrophy, while taking up oxygen andcarbon dioxide across the plume (Freytag et al. 2001).

Young ULS vestimentiferans settle on carbonates or other hard substrates in areas of activeseepage where sulfide is present and can presumably take up sulfide across their plumes as it isreleased from the sea floor sediments. The importance of L. luymesi roots as a site for sulfide uptakeincreases as surface expression of seepage subsides (Cordes et al. 2005a). Measurements of sulfidelevels among vestimentiferan tubeworm aggregations on the sea floor confirm that sulfide is onlyrarely detectable around the plumes of adult L. luymesi, and when it is detectable, it is present inlow micromolar concentrations (Freytag et al. 2001; Bergquist et al. 2003b; Cordes et al. 2005b,2006). However, millimolar concentrations of sulfide are present in pore waters immediatelybeneath the large aggregations, suggesting that the majority of the sulfide requirements for olderL. luymesi individuals are met by subsurface sulfide pools ( Julian et al. 1999, Bergquist et al. 2003b,Dattagupta et al. 2008).

In models of sulfide supply to L. luymesi aggregations, the previously known sources of sulfidewere not sufficient to match the high sulfide demands calculated for even moderate-sized aggre-gations (Cordes et al. 2003, 2005a). The sulfide produced in seep sediments is primarily a resultof anaerobic methane oxidation by microbial consortia (Boetius et al. 2000, Orcutt et al. 2005);the sulfate reduction rates at ULS seeps are among the highest rates ever measured, occasion-ally exceeding 3.5 μmol·cm−3·d−1 (Aharon & Fu 2000, Arvidson et al. 2004, Orcutt et al. 2005,Roberts et al. 2007). The additional sulfide needed by the L. luymesi aggregations could be pro-duced through reduction of the sulfate generated by the symbionts of L. luymesi ( Julian et al. 1999,Freytag et al. 2001). In a series of laboratory experiments, L. luymesi individuals released an aver-age of 85% of the sulfate generated by their symbionts through epithelial channels in their rootsthat may exchange sulfate for bicarbonate (Dattagupta et al. 2006). By releasing sulfate throughtheir roots, L. luymesi supplies an energetically favorable oxidant in deeper sediment layers. Whenthis is added to models of sulfide supply, the additional sulfate released through the roots wassufficient to match the demands of even large L. luymesi aggregations in sediments rich in oil andmethane (Cordes et al. 2005a). Modeling of in situ stable isotope values and geochemical profilesnear tubeworm aggregations also implicated sulfate release by L. luymesi roots and its subsequentoxidation in sediments beneath tubeworm aggregations (Dattagupta et al. 2008). The release ofapproximately 80% of the sulfate generated by L. luymesi could maintain a steady sulfide/sulfateratio in root-influenced sediments, resulting in a consistent sulfide supply and the persistence oftubeworm aggregations over their extremely long lifespan (Cordes et al. 2005a, Dattagupta et al.2008).

The seep tubeworms are among the most long-lived, noncolonial animals known (Fisher et al.1997, Bergquist et al. 2000, Cordes et al. 2007b). A 2.8-m L. luymesi individual was estimated to bemore than 400 years of age and a 1.1-m S. jonesi individual was estimated to be nearly 300 years ofage. This extreme longevity is related to low mortality rates of less than 0.1% annual mortality forL. luymesi individuals of approximately 50–60 years of age (Cordes et al. 2003). Young L. luymesiand S. jonesi can grow at rates up to 10 and 7 cm·yr−1, respectively, but by 50 years of age, theirgrowth rates slow to less than 1 and 0.5 cm·yr−1, respectively. However, even some of the largestL. luymesi and S. jonesi individuals measured exhibited some growth, suggesting that growth isindeterminate in these species (Bergquist et al. 2000, Cordes et al. 2007b).

L. luymesi appears to remain fecund throughout its adult lifespan and exhibits no evidence ofreproductive seasonality (Tyler & Young 1999). Gametes are fertilized internally; the females takesperm bundles into the oviducts and release fertilized embryos (Hilario et al. 2005). Lecithotrophic


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trochophore larvae are positively buoyant initially and in laboratory studies L. luymesi larvae canpersist for three weeks (Young et al. 1996) and L. satsuma larvae for more than six weeks (Miyakeet al. 2006). This long larval stage should favor fairly broad dispersal distances and relatively highlarval exchange among widely separated populations. Studies of the population genetic structureof L. luymesi indicate that genetic exchange occurs among populations separated by as much as560 km, resulting in relatively little genetic differentiation among aggregations within sites oramong sites within regions of the GoM (McMullin et al. 2008). Continuous reproduction forhundreds of years and long-range dispersal ability increase the probability that a given individual’slarvae will encounter an appropriate location in a currently active seep site.

Mussels

At least five species of bathymodiolin mussels with chemosynthetic and/or methanotrophic sym-bionts exist in the GoM: Bathymodiolus childressi from the ULS down to at least 2300-m depth,B. brooksi from approximately 1080 m to 3300 m, B. heckeri from 2200 m to 3300 m, Tamu fisherifrom 500 m to at least 1400 m, and Idas macdonaldi from 500 m to approximately 700 m (Gustafsonet al. 1998; Roberts et al. 2007; E.E. Cordes & C.R. Fisher, unpublished data). B. childressi fromULS and Alaminos Canyon were originally considered to be two separate populations on the basisof allozyme data (Craddock et al. 1995). However, analyses of combined data from two mitochon-drial and six nuclear DNA markers indicate that these populations, at seeps ranging from 500 m tomore than 2200 m depth, represent a continuous interbreeding population (Carney et al. 2006).

Bathymodiolin mussels that inhabit vents and seeps exhibit a wide variety of symbiont types andlevels of symbiont integration. Of the bathymodiolins of the GoM, B. childressi is the best studied(Figure 3). This species harbors type I methanotrophic gamma-proteobacteria in bacteriocytesclustered near the outer edges of the gill filament tissues (Fisher et al. 1987), a position that likelyfacilitates diffusion of methane and oxygen from the gill surface to the symbionts (Nelson & Fisher1995). Bathymodiolins do not contain binding proteins for transport of methane or oxygen, sodiffusion is the sole mode of transport of dissolved gasses (Childress & Fisher 1992). The symbiontsobtain energy through the oxidation of methane and incorporate methane-derived carbon intoorganic compounds (Childress et al. 1986, Fisher et al. 1987). Transfer of nutrients from thesymbionts to the host is largely accomplished through intracellular digestion of the symbiontsrather than translocation of metabolites (Streams et al. 1997). This symbiosis is so efficient thatB. childressi are capable of growing with methane as their sole carbon and energy source (Cary et al.1988). B. childressi is also capable of filter feeding (Page et al. 1990, Pile & Young 1999), thoughthey appear to obtain most of their nutrition from their symbionts (Fisher & Childress 1992), assuggested by the presence of hypertrophied gills, reduced digestive tracts (Gustafson et al. 1998),and light carbon stable isotopic signatures (–40 to –70 range) (Childress et al. 1986, Brooks et al.1987, Dattagupta et al. 2004).

B. childressi physiological condition is strongly correlated with environmental conditions (Nixet al. 1995, Bergquist et al. 2004). At the large mussel bed of B. childressi surrounding Brine PoolNR1 in GC 233, the mussels near the edge of the pool exhibited significantly higher growth rates,condition index (measured by ash-free dry weight to shell volume ratio), and glycogen content thanB. childressi further from the pool’s edge (Smith et al. 2000). These characteristics were correlatedwith decreasing methane and increasing sulfide concentration gradients moving away from thepool’s edge (Smith et al. 2000, Bergquist et al. 2005). Further, B. childressi transplanted from theinner zone of the brine pool to GC234 and Bush Hill for 1 year exhibited decreased growth ratesand condition indices, whereas those transplanted from GC234 and Bush Hill to the brine poolexhibited improved condition and increased growth rates (Bergquist et al. 2004, Dattagupta et al.


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2004). Tissue carbon and nitrogen stable isotopic values of transplanted B. childressi also shiftedafter one year to more closely reflect that of their new neighbors and new methane sources,suggesting a metabolic tissue replacement rate between 34% and 56% per year (Dattagupta et al.2004).

B. childressi is dioecious, exhibits synchronous, periodic gametogenesis, and produces a plank-totrophic larval stage capable of wide dispersal (Eckelbarger & Young 1999, Tyler & Young 1999,Tyler et al. 2007). This periodic cycle and the overall reproductive capacity of B. childressi insome populations may be compromised by the presence of two parasites, a eubacteria related toChlamydia and a trematode (Powell et al. 1999).

B. brooksi occurs at intermediate depths on the continental slope of the GoM and containsboth methanotrophic and sulfide-oxidizing gamma-proteobacteria symbionts. The two types ofsymbionts may occur within the same cell and often within the same vacuole (Fisher et al. 1993,Duperron et al. 2007a). B. brooksi inhabit a wide range of microhabitats, and the relative abundancesof the two different types of symbionts can vary in populations that inhabit different microenvi-ronments (Fisher et al. 1993, Duperron et al. 2007a). In one study, the tissue-stable carbon isotopevalues of B. brooksi were more negative (−48.8 ± 1.7) than those found in B. childressi (−43.9 ±1.8), which harbors only methanotrophic symbionts, collected from the same mussel bed (Fisher1993). The fact that the tissue-stable carbon values were not intermediate between those expectedfor bivalves that contain sulfide-oxidizing (or thiotrophic) and methanotrophic symbionts suggeststhat some of the DIC produced by the methanotrophic symbionts is subsequently fixed by thethiotrophic symbionts (Fisher 1993, Duperron et al. 2007a).

The deepest living bathymodiolin in the GoM, B. heckeri, contains symbionts with two differentmorphologies in bacteriocytes that line the gill filaments (Cavanaugh et al. 1987). Recent analysesof the 16S rRNA phylotypes of the symbionts of B. heckeri demonstrated the presence of fourphylotypes: one methanotroph, one methylotroph, and two thiotrophs (Duperron et al. 2007a). Acommensal polynoid worm, Branchipolynoe seepensis, is commonly found in this species (Pettibone1986).

T. fisheri inhabits the base of L. luymesi aggregations and is occasionally found in beds ofB. childressi (Fisher 1993, Cordes et al. 2005b). T. fisheri contains sulfide-oxidizing symbionts(Fisher 1993) in extracellular gill pockets. T. fisheri also harbors a commensal polynoid polychaetethat is morphologically very similar to Branchipolynoe symmitilida (Fisher 1993), but it is geneticallydistinct from both B. symmitilida and B. seepensis (S. Hourdez, personal communication). Very littleis known of the other GoM seep mytilid, Idas macdonaldi, because it has only been documentedfrom a single seep site in GB 386 (Gustafson et al. 1998). Other members of the genus Idas areassociated with the sulfide-rich deep-water habitats of wood falls and whale carcasses (Distel et al.2000).

Other Bivalves

Clams from four families are found associated with seeps in the GoM. On the ULS, at leasttwo species of vesicomyids (Vesicomya chordata and Calyptogena ponderosa), two species of lucinids(Lucinoma atlantis and an undescribed species of Lucinoma), one thyasirid (Thyasira oleophila), andan unidentified solemyid are known. All these bivalves harbor thiotrophic symbionts and exhibit avariety of adaptations to their symbiotic lifestyle (reviewed in Fisher 1990 and Childress & Fisher1992).

Similar to all described vesicomyids, C. ponderosa and V. cordata harbor intracellular sulfide-oxidizing symbionts in bacteriocytes in greatly enlarged gills (Brooks et al. 1987). C. ponderosa andV. cordata contain abundant extracellular hemoglobin in a closed circulatory system (Scott & Fisher


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1995), which is capable of concentrating sulfide 2 to 3 orders of magnitude above environmentallevels (Fisher 1996). Sulfide is taken up across the surface of the foot, which is buried in thesediments, and oxygen is taken up through siphons extended into the water column. These clamsburrow horizontally through the sediment, leaving characteristic trails on the sea floor (Rosmanet al. 1987, Scott & Fisher 1995).

Lucinids, solemyids, and some thyasirids have a reduced gut and feeding palps and have gamma-proteobacteria symbionts associated with hypertrophied gills (Distel & Felbeck 1987, Fisher 1990,Duperron et al. 2007b). Thyasirids house their symbionts extracellularly (Southward 1986, Fisher1990), although many thyasirids lack symbionts entirely (Dufour 2005). Nutrient transfer fromsymbiont to host appears to be through intracellular digestion (Distel & Felbeck 1987), althoughthis has not yet been verified for all species. Environmental symbiont transmission has been shownin L. aequizonata and all other lucinids examined to date (Gros et al. 1999). Lucinids and thyasiridsform extensive subsurface feeding tubes to acquire sulfide from deeper anoxic sediment layers(Turner 1985, Distel & Felbeck 1987). Some lucinids are suggested to oxygenate their burrowsand mobilize the sulfide from pyrite deposits, thereby “mining” sulfide from the sediments (Dandoet al. 1994). Some thyasirids are capable of extending their foot more than 30 times the lengthof the shell, potentially mining sulfides from deep anoxic layers of sediment (Dufour & Felbeck2003). Because clams from these families live beneath the sediment surface, little is known abouttheir abundance at the seeps of the GoM, although extensive beds of disarticulated shells are oftenencountered at seep sites (Rosman et al. 1987).

COMMUNITY ECOLOGY

Along with the symbiont-containing species of the ULS, a total of 120 macrofaunal taxa (retainedon a 2 mm sieve) have been collected with tubeworm aggregations and mussels (Carney 1994;Bergquist et al. 2003a; Cordes et al. 2005b, 2006). Many of these taxa are representativesof those found at cold seeps and hydrothermal vents worldwide (Tunnicliffe 1991, Sibuet &Olu 1998). A large proportion of the taxa found at vents and seeps is endemic to deep-seachemoautotrophy-based ecosystems. It is commonly believed, and occasionally demonstrated,that endemic seep and vent taxa have developed a suite of adaptations that allow them to persistin an otherwise exclusionary environment of high environmental toxicity (Tunnicliffe et al. 1998,Fisher et al. 2000, Van Dover 2000, Hourdez et al. 2002). Whereas endemic species dominatevent and some seep commuities, nonendemic species also occur in high abundances in ULSseep environments. These nonendemic fauna have been classified as colonists when they occurin greater numbers at the seeps than in the background habitats, or vagrants when they occur insimilar densities to nonseep habitats (Carney 1994). Any of these seep inhabitants may be takingadvantage of the local primary production in these deep-sea chemosynthetic habitats (Fisher1993, MacAvoy et al. 2002, Gilhooly et al. 2007), or merely occupying the complex habitatprovided by the foundation species of tubeworms and bivalves. Below is a theoretical frameworkfor seep community succession based on hypotheses generated from the ULS seeps prior to theyear 2000 and tested in a series of subsequent studies.

Model of Upper Louisiana Slope Seep Ecology

Early in the evolution of a seepage source, the seepage rate is high and large amounts of bio-genic and thermogenic methane and oil are delivered to the sediment-water interface (Sassenet al. 1994a). As authigenic carbonates begin to precipitate, they provide the necessary hard sub-strate for settlement of vestimentiferans and mussels (Tyler & Young 1999), although extensive


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mussel beds may form in areas without substantial carbonate deposition such as the Brine PoolNR1 (MacDonald et al. 1990b). Although these species may settle concomitantly, high methaneconcentrations would favor the establishment and growth of methanotrophic mussel populations.Bathymodiolins will not only dominate the space available, but also are capable of filter feedingand reducing the numbers of larvae that reach the substrate (Bergquist et al. 2003a). This phe-nomenon may contribute to an initial phase of low levels of L. luymesi and S. jonesi recruitmentinto B. childressi–dominated young seepage sites.

The associated community of B. childressi mussel beds is dominated by a few endemic species(Carney 1994, Bergquist et al. 2005). Some of these endemic species tolerate hypoxia and elevatedmethane and sulfide concentrations. For example, the iceworm, Hesiocaeca methanicola, is able totolerate anoxia in excess of 96 hours (Fisher et al. 2000). An orbiniid polychaete, Methanoariciadendrobranchiata, can survive for days in anoxic conditions in the presence of millimolar concen-trations of sulfide and contains high-affinity hemoglobins and enlarged gills that allow it takeup oxygen from very low environmental concentrations (Hourdez et al. 2002). Such adaptationsallow these and other endemic species to exploit the locally elevated microbial primary productionin a habitat where environmental toxicity likely excludes many predators (Bergquist et al. 2003a,Cordes et al. 2005b).

The limited diversity of the B. childressi-associated community [a total of 19 species in 17collections (Bergquist et al. 2005)] suggests that although there are advantages to the colonizationof this productive habitat, the environmental conditions present require a relatively rare set ofadaptations to tolerate exposure to seep fluid. B. childressi mussel bed associates are members ofa set of families that have been successful at seeps and vents worldwide, including the hesionidand polynoid polychaetes, bresilid shrimp, neritoid and provannid gastropods, and the galatheidcrabs (Sibuet & Olu 1998, Tunnicliffe et al. 1998, Van Dover 2000). Although the families arelimited in number, the species-level diversity represented within these groups suggests that thisset of adaptations may allow for rapid divergence once these habitats are colonized.

B. childressi individuals may live for as long as 100–150 years, whereas mussel beds may persistfor far longer (Nix et al. 1995). Often overlapping with and normally persisting past the B. childressimussel bed successional stage are young tubeworm aggregations consisting of L. luymesi, S. jonesi,and the rare undescribed escarpid (Figure 5). During this period, anaerobic methane oxidationand carbonate precipitation rates remain high (Aharon & Fu 2000, Cordes et al. 2005a), whichpromotes increased L. luymesi settlement rates over the first 10 to 30 years of vestimentiferanaggregation development (Bergquist et al. 2002). Active recruitment coupled with low rates ofmortality in young L. luymesi and S. jonesi results in rapid increases in population size (Cordes et al.2003). The environment surrounding vestimentiferan aggregations in this stage is characterizedby relatively high concentrations of reduced chemicals in the epibenthic water (Freytag et al.2001, Bergquist et al. 2003b, Cordes et al. 2006). The abundance of sulfide among L. luymesi tubesapparently restricts community composition and continues to favor endemic species (Cordes et al.2005b). B. childressi remains present, along with its associated gastropod Bathynerita naticoidea andthe endemic gastropod Provanna sculpta. Other dominant endemic fauna include the polynoidpolychaetes Harmothoe sp. nov. and Branchinotogluma sp. nov. and the bresilid shrimp Alvinocarisstactophila. The remainder of the community is largely composed of colonist fauna, including thegastropods Cancellaria rosewateri and Cataegis meroglypta and the sipunculid Phascolosoma turnerae.

When L. luymesi aggregations reach 20 to 30 years of age, sulfide concentrations in the epiben-thic water are much reduced from a maximum of 4 μM in young aggregations to 0–1 μM (Cordeset al. 2005b). Declines in seepage rate result from ongoing carbonate precipitation (Sassen et al.1994a) as well as the influence of L. luymesi on the local biogeochemistry. The subsurface mass ofL. luymesi roots may occlude seepage pathways (Bergquist et al. 2003a), consume sulfide before


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** *

*

***

*

*

**

*

*

VK825

MC885

GC354GB425

GB535GB543

GB544

GC234

GC233

GC232GC184

Figure 5Succession in seep communities over time. A multidimensional scaling plot that represents the similarity incomposition among the communities associated with tubeworm aggregations and mussel beds from theupper slope. Distance between objects is based on pairwise Bray-Curtis similarity between fourth-roottransformed species abundances where similar communities are located close to each other in the ordination.Mussel-bed communities (Bergquist et al. 2005) are denoted with asterisks and tubeworm-aggregationcommunities (Bergquist et al. 2003a; Cordes et al. 2005b, 2006) are circles; the size of the circles representsthe relative age of the aggregation (older aggregations = larger circles). Different colored symbols representdifferent sites according to U.S. Minerals Management Service oil lease block designations: GB is GardenBanks, GC is Green Canyon, MC is Mississippi Canyon, and VK is Viosca Knoll.

it reaches the sea floor, and release sulfate that may shift the site of sulfate reduction to deepersediment layers (Cordes et al. 2005a; Dattagupta et al. 2006, 2008). L. luymesi settlement ratebegins to decline owing to the monopolization of existing substrata and the reduced availability ofsulfide above the sea floor (Bergquist et al. 2002, 2003b; Cordes et al. 2003). The existing L. luymesipopulation will remain viable owing to their increasing reliance on their roots for sulfide uptakeand their ability to fuel pore water sulfide production by releasing sulfate through their roots.Conversely, populations of B. childressi will decline because this methanotrophic mussel requiresexposure to methane in overlying water (Kochevar et al. 1992).

As L. luymesi growth and recruitment continues, aggregations may include hundreds to thou-sands of individuals (Kennicutt et al. 1995, Bergquist et al. 2002) (Figure 4). Individual aggre-gations may be restricted to an area of approximately 1 m2, which is common at many sites inthe GoM (Cordes et al. 2006). Alternatively, large clusters of aggregations can form, coveringhundreds of m2, such as are found in GC 234 and GC 232 (MacDonald et al. 1990a, 2003).

The continued growth of L. luymesi and S. jonesi, in conjunction with reductions in the releaseof seep fluid from the base of the aggregations, increases the amount of tube surface area exposedto little or no sulfide (Bergquist et al. 2003a). Once this habitat is made available, more of thenonendemic background fauna are capable of colonizing the tubeworm aggregations. This leadsto a more diverse community than is found in mussel beds or very young tubeworm aggregations(Carney 1994; Bergquist et al. 2003a, 2005; Cordes et al. 2005b). Amphipods, chitons, and limpetsbegin to take advantage of the remaining bacterial biomass in the aggregations. Lower concentra-tions of sulfide and methane also lead to reductions in free-living microbial primary productivity,which leads to declines in the overall biomass of the associated community (Bergquist et al. 2003a,


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Cordes et al. 2005b). The onset of colonization by taxa in higher trophic levels, such as the preda-tory Eunice sp. that forms tubes on the anterior ends of L. luymesi, results in additional reductionof primary consumer biomass (Bergquist et al. 2003a).

As epibenthic sulfide concentrations decline further, L. luymesi recruitment finally ceases 40 to60 years after the local seepage source and substrate were formed (Bergquist et al. 2002, Cordeset al. 2003). Sulfide is occasionally still detectable in aggregations of this age, but only at verylow micromolar concentrations (Bergquist et al. 2003b, Cordes et al. 2006). The spherical habitatgenerated by the tubeworms may be massive at this stage, with L. luymesi length normally rangingbetween 85 and 120 cm at 50 years (Cordes et al. 2007b). The number of associated taxa ispositively correlated with the size of the tubeworm-generated habitat, so diversity in this stageremains fairly high (Bergquist et al. 2003a). The aggregation containing the greatest number ofassociated taxa documented (47) was in this stage, and was one of the largest aggregations collected(726 tubeworms, 4.3 m2 tube surface area) (Cordes et al. 2006).

The community that inhabits L. luymesi and S. jonesi aggregations in this stage continues to becomposed of a mixture of endemic and nonendemic species, although shifts in community structureare apparent. The endemic shrimp A. stactophila significantly declines in abundance as does theendemic galatheid Munidopsis sp. 1. These species are replaced by the shrimp Periclemenes sp. andMunidopsis sp. 2, both of which significantly increase in abundance with aggregation age. Theformer species has been hypothesized to have higher tolerance to reduced chemicals and anoxicconditions than the latter, whereas the latter are capable of outcompeting the former in morebenign habitat conditions (Cordes et al. 2005b). The majid crabs Rochinia crassa and R. tanneri,the giant isopod Bathynomus giganteus, the seastar Sclerasterias tanneri, as well as a number offishes, including synaphobranchid eels and the hagfish Eptatretus sp., appear in older aggregations(Carney 1994, Cordes et al. 2005b). Many individuals of these vagrant secondary consumers andscavengers obtain a significant amount of their nutrition from seep primary production (MacAvoyet al. 2002, 2005). The proximity of the larger, more benign aggregations to aggregations in earliersuccessional stages (Figure 4) may allow large, mobile species to forage in areas of greater preyabundance without remaining in the toxic environment for extended periods of time.

This final successional stage may persist for hundreds of years with continued slow L. luymesigrowth and low or undetectable concentrations of reduced chemicals in the epibenthic layer.Eventually, continued L. luymesi growth leads to basketing of the aggregations, with the tubewormslying recumbent on their sides along the sediment surface. However, this does not necessarilyindicate that the individual vestimentiferans are in some way senescent, because their physiologicalcondition does not appear to decline in this stage (Bergquist et al. 2003b).

In the oldest L. luymesi aggregations, a lack of chemosynthetic production by free-living bacterialeads to the near elimination of the lower trophic levels (Cordes et al. 2005b). However, someendemic species remain present in lower numbers in the later successional stages. The endemicspecies are normally scavenging or predatory species, including Munidopsis sp. 1, Harmothoe sp. nov.and Branchinotogluma sp. nov. Filter-feeding organisms such as hydroids and serpulid polychaetesincrease in abundance, perhaps taking advantage of the elevation of the tubeworm tubes to feedin higher flow regimes above the substrate. Members of higher trophic levels also continue toinhabit the aggregations and likely forage over the surrounding sea floor and within adjacent,more productive aggregations (Cordes et al. 2005b).

This linear progression through successional stages is not always consistent in different habi-tats (Cordes et al. 2006). Tubeworm aggregations at brine seeps tend to consist of a greaterproportion of S. jonesi and are generally restricted to isolated patches. The persistence of B. chil-dressi in somewhat older aggregations indicates that these brine-dominated sites may also containhigher methane concentrations in the epibenthic layer. Sulfide concentrations are also higher than


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expected in some older aggregations, above 1 μM in some cases and as high as 4 μM in one sample(Cordes et al. 2006), leading to the persistence of endemic heterotrophic fauna. The aggregationsfound in the western Garden Banks sites, near Brine Pool NR1 in GC 233 and in certain locationswithin Mississippi Canyon and GC 354, fall into this category (Figure 5). Although the generalsuccessional trends described above (reductions in biomass, shifts in trophic structure, etc.) are ap-plicable to most sites, their trajectory through the successional sequence can be somewhat altered.

The seep foundation species and associated communities of the lower slope (>1000 m) aresimilar to those of the upper slope at higher taxonomic levels (family and above), but are quitedistinct at the species level (Brooks et al. 1990, Cordes et al. 2007a, Fisher et al. 2007, Roberts et al.2007). The composition of the lower slope communities is actually more similar to the communitiesfound at similar depths at the seeps of Barbados and the Blake Ridge than they are to those foundon the upper slope (Cordes et al. 2007a). One of the most significant differences in communitystructure with depth is the dominance of the lower trophic level by grazing gastropods on theupper slope, and their replacement by detritivorous ophiuroids on the lower slope. The lower slopecommunities are composed of fewer species in general, containing 50 taxa total and a maximum of20 taxa in any single collection (Cordes et al. 2007a), whereas 109 taxa are known from the upperslope and a maximum of 47 taxa were collected within a single L. luymesi and S. jonesi aggregation(Cordes et al. 2006). Although diversity declines as depth increases, the density of associated faunaremains relatively constant. Distinctions appear to exist between the communities that inhabitbathmodiolin beds and vestimentiferan aggregations, with lower diversity and higher biomassin lower slope mussel beds than lower slope vestimentiferan aggregations (Cordes et al. 2007a).Although this finding mirrors the successional trend of the upper slope communities (Bergquistet al. 2003a), the model described for the upper slope seep system remains to be tested in thelower slope communities. In addition to the more typical seep fauna discussed above, there are alsoadditional types of seep-related communities dominated by mobile sea urchins and pogonophoransthat show little affinity with the upper slope communities (Fisher et al. 2007, Roberts et al. 2007).

SUMMARY POINTS

1. Hydrocarbon seeps in the Gulf of Mexico arise from the migration of subsurface saltlayers and can occur in various stages that correspond to a gradient in fluid flux rates.

2. Six species of siboglinid tubeworms with sulfide-oxidizing symbionts, five species ofbathymodiolin mussels with methane- or sulfide-oxidizing symbionts, and at least twospecies of vesicomyid clams with sulfide-oxidizing symbionts are found in associationwith hydrocarbon seeps in the Gulf of Mexico.

3. Mussel bed communities consist of mainly endemic species and are characterized by highbiomass and low diversity.

4. Communities that inhabit tubeworm aggregations proceed through a series of succes-sional stages over the course of hundreds of years from high-biomass, low-diversitycommunities of primarily endemic species (similar to mussel bed communities), to adiverse mixture of endemic and nonendemic species, to a final low-diversity, low-biomasscommunity.

5. Successional shifts in community structure result from the decline in the concentrationof reduced chemicals in the epibenthic layers, partially resulting from the influence ofthe siboglinid tubeworms on the biogeochemistry of the seeps.


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FUTURE ISSUES

1. Establishing the link between the microbial and metazoan communities in terms ofbiogeochemical processes at the seeps is critical.

2. Testing the succession hypothesis in a variety of settings, particularly at the deeper seepsof the Gulf of Mexico where there are other foundation species of tubeworms and mussels,is essential.

3. We must resolve the degree of endemism of the seep fauna in light of recent discoveriesof seep endemic species in coral and other hard-ground habitats.

4. Establishing connectivity (in terms of genetic exchange and community similarity) be-tween the seeps of the Gulf of Mexico and the other chemosynthetic communities of theAtlantic Equatorial Belt, including the Caribbean, Barbados, the Blake Ridge, Brazil, thesouthern Mid-Atlantic Ridge, and the African Margin, is necessary.

DISCLOSURE STATEMENT

The authors are not aware of any biases that might be perceived as affecting the objectivity of thisreview.

ACKNOWLEDGMENTS

The work reviewed here was supported in large part by grants and contracts from the UnitedStates Minerals Management Service, the National Oceanic and Atmospheric Administration,and the National Science Foundation. During the preparation of this manuscript, E.E.C. was amember of the Organismic and Evolutionary Biology Department at Harvard University.

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Annual Review ofMarine Science

Volume 1, 2009

Contents

Wally’s Quest to Understand the Ocean’s CaCO3 CycleW.S. Broecker � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

A Decade of Satellite Ocean Color ObservationsCharles R. McClain � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �19

Chemistry of Marine Ligands and SiderophoresJulia M. Vraspir and Alison Butler � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �43

Particle AggregationAdrian B. Burd and George A. Jackson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �65

Marine Chemical Technology and Sensors for Marine Waters:Potentials and LimitsTommy S. Moore, Katherine M. Mullaugh, Rebecca R. Holyoke,Andrew S. Madison, Mustafa Yucel, and George W. Luther, III � � � � � � � � � � � � � � � � � � � � � � � � � � �91

Centuries of Human-Driven Change in Salt Marsh EcosystemsK. Bromberg Gedan, B.R. Silliman, and M.D. Bertness � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 117

Macro-Ecology of Gulf of Mexico Cold SeepsErik E. Cordes, Derk C. Bergquist, and Charles R. Fisher � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 143

Ocean Acidification: The Other CO2 ProblemScott C. Doney, Victoria J. Fabry, Richard A. Feely, and Joan A. Kleypas � � � � � � � � � � � � � � � 169

Marine Chemical Ecology: Chemical Signals and Cues StructureMarine Populations, Communities, and EcosystemsMark E. Hay � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 193

Advances in Quantifying Air-Sea Gas Exchange and EnvironmentalForcingRik Wanninkhof, William E. Asher, David T. Ho, Colm Sweeney,

and Wade R. McGillis � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 213

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Atmospheric Iron Deposition: Global Distribution, Variability,and Human PerturbationsNatalie M. Mahowald, Sebastian Engelstaedter, Chao Luo, Andrea Sealy,

Paulo Artaxo, Claudia Benitez-Nelson, Sophie Bonnet, Ying Chen, Patrick Y. Chuang,David D. Cohen, Francois Dulac, Barak Herut, Anne M. Johansen, Nilgun Kubilay,Remi Losno, Willy Maenhaut, Adina Paytan, Joseph M. Prospero,Lindsey M. Shank, and Ronald L. Siefert � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 245

Contributions of Long-Term Research and Time-Series Observationsto Marine Ecology and BiogeochemistryHugh W. Ducklow, Scott C. Doney, and Deborah K. Steinberg � � � � � � � � � � � � � � � � � � � � � � � � � � 279

Clathrate Hydrates in NatureKeith C. Hester and Peter G. Brewer � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 303

Hypoxia, Nitrogen, and Fisheries: Integrating Effects Across Localand Global LandscapesDenise L. Breitburg, Darryl W. Hondorp, Lori A. Davias, and Robert J. Diaz � � � � � � � � � 329

The Oceanic Vertical Pump Induced by Mesoscaleand Submesoscale TurbulencePatrice Klein and Guillaume Lapeyre � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 351

An Inconvenient Sea Truth: Spread, Steepness, and Skewnessof Surface SlopesWalter Munk � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 377

Loss of Sea Ice in the ArcticDonald K. Perovich and Jacqueline A. Richter-Menge � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 417

Larval Dispersal and Marine Population ConnectivityRobert K. Cowen and Su Sponaugle � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 443

Errata

An online log of corrections to Annual Review of Marine Science articles may be found athttp://marine.annualreviews.org/errata.shtml

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macro-ecology of gulf of mexico cold seeps

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