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Macro-Ecology of Gulf
of Mexico Cold Seeps
Erik E. Cordes,1 Derk C. Bergquist,2
and Charles R. Fisher3
1
Biology Department, Temple University, Philadelphia, Pennsylvania 19122;
email: [email protected]
2
Marine Resources Research Institute, South Carolina Department of Natural Resources,
Columbia, South Carolina 29201; email: [email protected]
3
Biology Department, Pennsylvania State University, University Park, Pennsylvania 16802;
email: cfi[email protected]
Annu. Rev. Mar. Sci. 2009. 1:143–68
Key Words
First published online as a Review in Advance on
August 28, 2008
chemosynthesis, symbiosis, succession, siboglinidae, bathymodiolin, upper
Louisiana slope
The Annual Review of Marine Science is online at
marine.annualreviews.org
This article’s doi:
10.1146/annurev.marine.010908.163912
c 2009 by Annual Reviews.
Copyright All rights reserved
1941-1405/09/0115-0143$20.00
Abstract
Shortly after the discovery of chemosynthetic ecosystems at deep-sea hydrothermal vents, similar ecosystems were found at cold seeps in the Gulf of
Mexico. Over the past two decades, these sites have become model systems
for understanding the physiology of the symbiont-containing megafauna
and the ecology of seep communities worldwide. Symbiont-containing bivalves and siboglinid polychaetes dominate the communities, including five
bathymodiolin mussel species and six vestimentiferan (siboglinid polychaete)
species in the Gulf of Mexico. The mussels include the first described examples of methanotrophic symbiosis and dual methanotrophic/thiotrophic
symbiosis. Studies with the vestimentiferans have demonstrated their potential for extreme longevity and their ability to use posterior structures for
subsurface exchange of dissolved metabolites. Ecological investigations have
demonstrated that the vestimentiferans function as ecosystem engineers and
identified a community succession sequence from a specialized high-biomass
endemic community to a low-biomass community of background fauna over
the life of a hydrocarbon seep site.
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GoM: Gulf of Mexico
ULS: upper Louisiana
slope
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GC: Green Canyon
7:55
Cold seeps are common deep-water habitats on the continental slope and rise worldwide (as
reviewed 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 Aleutian
subduction zone in the eastern Pacific. In the western Pacific, some of the deepest seeps in the
world occur from Kamchatka (Mironov 2000) south past Japan to New Zealand (Lewis & Marshall
1996). In the Indian Ocean, seeps are known from the coast of Pakistan (von Rad et al. 2000) and
from recent discoveries off the coast of Indonesia and the Bay of Bengal ( J. Brooks, personal
communication). In the Atlantic, seeps occur off the coast of Brazil, near Barbados, the Blake
Ridge off the Carolinas, the Laurentian Fan, the Haakon Mosby mud volcano off the coast of
Norway (Vogt et al. 1999), the Gulf of Cadiz (Pinheiro et al. 2003), the Mediterranean, the Sea
of 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 most
well-described seep communities in the world. The presence of gas and oil in surficial sediments
on the upper continental slope off the coast of Louisiana was first discovered in gas samples from
four underwater vents (Bernard et al. 1976). Geochemical characterization of these sites followed
in 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-out
zones overlying areas impacted by salt diapirism. The descriptions of the geology of the seeps on
the upper slope coincided with the discovery of chemosynthetic communities along the Florida
Escarpment (Paull et al. 1984, Paull et al. 1985). Subsequent trawling surveys of the seeps of
the 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 been
the subject of numerous research programs that described the geology and geochemistry of the
habitat 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 with
the hope of providing a framework to guide future investigations in this model system and in other
less-known, or as-yet-unknown, seep systems. This summary comprises the current state of knowledge of the seeps of the northern GoM (Figure 1), focusing on the physiology and ecology of the
symbiotic organisms that inhabit the seeps and the diverse heterotrophic macro- and megafauna
associated with them. In the interest of space we have excludied potentially significant links to the
meiofaunal and foraminiferal communities and the rapidly expanding body of work on the microbial ecology of cold seeps. We further focus on the sites along the upper continental slope because
of 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-industry
activities at depths greater than 1000 m. Although the literature on the deeper sites is relatively
scant, it is becoming apparent that there are many basic similarities, as well as some fundamental
differences, between the deeper-living communities and those found on the upper slope. Most of
the seep sites in the northern GoM are named for the Mineral Management Service (MMS) lease
block in which the site was discovered (for example, a site named GC 140 would refer to a site
located 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 largely
driven 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 (Pindell
1985). Extensive evaporation followed, leaving behind a thick salt sheet, the Louann salt formation,
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VK 825/826
GB 535
GB 543
GB 544
GB 382
GB 424
GB 425
MC 709
GC 140
GC 185
GC 228
GC 272
GC 354
MC 798
MC 885
MC 929
MC 853
GC415
GC 204
GC286
GB 388
GC 533
0
200
400
600
800
1000
1200
1400
GC 232
GC 233
GC 234
1600
1800
2000
2200
2400
2600
2800
3000
3200
Depth contours (m)
Figure 1
Location of the known chemosynthetic communities of the upper slope (<1000 m) of the Gulf of Mexico. The area shown is delimited
by the box in the inset image of North America. Depth contours are in meters. Site labels are according to U.S. Mineral Management
Service 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 have
occurred approximately 55–50 Mya during the Paleocene and Eocene as the Caribbean plate
moved to the east across the region (Rosenfeld & Pindell 2003). By the early Miocene, approximately 21 mya, the deposition of large volumes of siliciclastic sediments onto the salt layer
began (Kennicutt et al. 1992, Sassen et al. 1994a). As these sediments accumulated they compressed 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 salt
sheet to migrate down along the continental slope and deform into vertically mobile pillars and
salt domes (Humphris 1979). Salt diapirs subsequently pierced and cracked the shale and sediment
www.annualreviews.org • Macro-Ecology of Gulf of Mexico Cold Seeps
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overburden (Brooks et al. 1987, Aharon et al. 1992), causing the migration of trapped hydrocarbons (Kennicutt et al. 1988), some of which reach the sea floor. This process of salt tectonics
dominates the geology of the northern GoM, particularly in the areas of most intense seepage on
the ULS.
As oils migrate through the sediment column, they are altered by geologic and biologic processes, which leads to variability in the abundance and types of reduced chemicals that reach the
sediment surface (Figure 2). Thermal cracking of kerogen leads to the production of petroleum
hydrocarbons and natural gas. Continued heating of these products generates smaller straightchain and aromatic hydrocarbons, organic acids, hydrocarbon gasses, and carbon dioxide (Seewald
2003). 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 (Martens
et 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 from
several 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-phase
or liquid hydrocarbons with anhydrite and gypsum contained in salt-dome cap rocks or sulfatebearing evaporites (Sassen et al. 1994b, Saunders & Thomas 1996, Röling et al. 2003). However,
the majority of the sulfide present at the sea floor in the GoM cold seeps is generated in the
shallow subsurface by the anaerobic oxidation of methane, higher hydrocarbons, and organic
material 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 supports
high-biomass microbial and animal communities at the seeps.
Individual seepage sites are located on mounds or in grabens associated with subsurface salt
structures. The relative age of a seepage source is generally related to the amount of carbonate
precipitation 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 fluid
venting often associated with sediment transport, giving rise to the term mud volcanoes for the
most active of these sites. In this setting, fluids migrate along vertical faults and can maintain
distinct 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 or
brine (Prior et al. 1989, MacDonald et al. 2000, Sassen et al. 2003, Joye et al. 2005). Sediment
instability limits or precludes the attachment of most of the seep fauna that require hard substrata
for settlement (Roberts & Neurauter 1990). Rather, the fauna of mud volcanoes is dominated by
bacterial 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).
MC: Mississippi
Canyon
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−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−→
Figure 2
Box 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 pass
through the process if they indicate a link between two state variables via a process. The darkest shade of blue represents
biogeochemical processes, medium blue includes biological interactions, and light blue includes community-level ecological processes.
DIC, dissolved inorganic carbon.
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Endemic consumers
+
Nonendemic consumers
+
+
Secondary
production
–
–
Predation
Predation
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1° Consumers
+
+
Secondary
production
1° Consumers
2° Consumers
+
+
+
2° Consumers
+
+
Recruitment
Recruitment
+
+
–
+
Methanotrophic
mussels
–
Primary
production
Symbiotic
production
+
–
+
Symbiotic
production
+
+
Growth
Young
aggregation
+
+
+
Growth
Recruitment
+
+
+
–
+
Dissolution
–
–
Non-porous
carbonates
Surficial
methane
Surficial
sulfide
+
–
–
Precipitation
–
–
Diffusion and
migration
+
+
Trapping and
accumulation
–
–
Seawater
sulfate
Diffusion and
migration
–
+
Porewater
methane
+
–
Porous crusts
and cemented
sediments
+
+
–
+
+
Hydrates
Recruitment
+
+
+
+
+
Microbial
biomass
Bed
Old
aggregation
Tubeworms
Free-living
microbes
Porewater
sulfide
+
Precipitation
Diffusion
–
+
Methanogenesis
Methane
Anaerobic
methane
oxidation
+
Porewater DIC
Calcium
carbonate
+
+
Porewater
sulfate
Sulfate
reduction
Sulfide
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Carbonate precipitation slows fluid flow and provides a stable substrate for recruitment of other
fauna (Figure 2). Authigenic carbonate precipitation is a consequence of the rise in alkalinity
and 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 bubble
streams and oil-stained sediments (Sassen et al. 1993).
Gas hydrate accumulations may also serve to mitigate the escape of gas from sediments by
forming in areas of the most active venting (MacDonald et al. 2005). Hydrates are ice-like clathrates
of methane and other gases within a water molecule lattice (Sassen et al. 2001). Hydrates form
under high-pressure and low-temperature conditions at depths between 440 and 2400 m in the
northern GoM (Sassen et al. 1999). These structures may crystallize in the pore spaces of sediments
to form small nodules, or may accumulate as massive vein-filling structures where gas migration
is most rapid (Milkov & Sassen 2003). Time-lapse photography of small sea-floor-breaching gashydrate accumulations at the Bush Hill site showed changes in hydrate morphology over the
course of a single year (MacDonald et al. 2003). Larger hydrate structures may form barriers to
seepage, collecting hydrocarbon gasses beneath them (MacDonald et al. 1994). If the gas becomes
overpressurized, a catastrophic release may result in the formation of sea floor pockmarks and
overturned carbonate blocks (Prior et al. 1989).
Mounds in intermediate stages, with continued seepage of reduced chemicals, precipitation of
carbonate substrates, and gas hydrate accumulations, often harbor well-developed chemosynthetic
communities. Bush Hill, in GC 185, is one of the best known of these sites. The small hill is
the site of carbonate accumulation on top of a conical diapir rising from a depth of 580 m to
approximately 540 m (MacDonald et al. 1989). The diapir is either a sea-floor-piercing mud
diapir (Neurauter & Bryant 1990) or a dormant mud volcano (Milkov & Sassen 2003) overlying
a 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), which
provides some indication of the general age of similar young features (Sager et al. 1999). At the
crest of the hill are oil-stained sediments, gas hydrate, bacterial mats, and active methane bubble
streams, along with numerous distinct vestimentiferan (siboglinid polychaete) aggregations and
bathymodiolin mussel beds (MacDonald et al. 2003). The distribution of mussel beds is correlated
to methane concentration in the epibenthic layer, whereas vestimentiferan tubeworm distribution
is correlated to the total amount of extractable organic matter (often in the form of oil) in the
sediments (MacDonald et al. 1989). On the western edge of this mound are hard substrata with
gorgonian (Callogorgia americana delta) and a few isolated scleractinian (Lophelia pertusa) coral
colonies (MacDonald et al. 1989).
Other well-known sites that fit this profile include the large, complex sites at GC 272 and
Garden Banks (GB) 424/425. A pair of mounds forms the site at the border between GB 424
and 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 a
large fault scarp (Kohl & Roberts 1994) on the western flank of a large mound centered in GC
273 (Sager et al. 2003). At both of these sites, soft-sediment seepage areas are dominated by beds
of vesicomyid, lucinid, and thyasirid clams (MacDonald et al. 1990a, Sassen et al. 1993, Powell
et al. 2002), whereas outcropping authigenic carbonates are often occupied by bathymodiolins
and vestimentiferans (Sassen et al. 1993, Nix et al. 1995, MacDonald et al. 2000).
As authigenic carbonate precipitation progresses, nodules and shell debris may become cemented together (Aharon et al. 1997) and thicker crusts and boulders begin to develop (Roberts
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GB: Garden Banks
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& Aharon 1994, Sager et al. 1999). At this stage, faults may become occluded and seepage slows. A
seepage site may eventually become entirely cemented over, its existence only manifest as a thick
cap of carbonate with a light δ13 C signature (Sager et al. 1999). One of the best known of these
older mounds is a site in GC 140. This site is a massive deposit of authigenic carbonate overlying
the 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 between
200 and 13 kyr old (Roberts & Aharon 1994). Continued salt migration has led to faulting on
the flanks of the mound, removing overlying sediment layers and overturning carbonate blocks,
resulting in randomly oriented carbonate outcrops (Roberts & Aharon 1994) and occasional small
gas seeps (Aharon et al. 1997, Roberts et al. 2000). The gas seeps are commonly covered with
bacterial mats (Sassen et al. 1993, Mills et al. 2004, Gilhooly et al. 2007), and microbial methane
oxidation 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 this
lease 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 authigenic
carbonate layer and large blocks of outcropping carbonate. VK 826 contains some of the most
well-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 diverse
octocoral communities. On the flanks of both mounds are large, roughly rectangular, cracked
carbonate blocks. Vestimentiferan aggregations and bacterial mats are associated with many of
these blocks where sulfide-rich fluids migrate along the subsurface channels associated with their
uplift (Cordes et al. 2006). See sidebar, Deep-Water Coral Communities.
Subsurface faulting in the areas between bathymetric highs on the sea floor may generate
additional seep sites in the form of grabens or half grabens (MacDonald et al. 1990a, Sassen
et al. 1993, MacDonald et al. 2003). Sediment slumping related to salt withdrawal may expose
gas hydrates or organic-rich sediment layers, leading to reducing conditions and additional
cold-seep habitats (Carney 1994; Sassen et al. 1999). Whereas these habitats may occasionally be
associated with free-venting methane gas emerging from the sediment surface, they are generally
more influenced by petroleum hydrocarbons (Sassen et al. 1994a). The increased abundance of
vestimentiferans over bathymodiolins at these sites is likely due to slower seepage rates of hydrocarbons, which leads to an increased amount of time for subsurface hydrocarbon degradation by
microbes coupled to the production of hydrogen sulfide (Sassen et al. 1994a, Cordes et al. 2005a).
VK: Viosca Knoll
DEEP-WATER CORAL COMMUNITIES
Chemosynthetic communities are just one of the community types that inhabit the hard-ground habitats of the Gulf
of Mexico. Once seepage of hydrocarbons and sulfide has declined, and relict seeps are represented primarily by
authigenic carbonates, deep-water corals may colonize these substrata. In 1955 a trawl in the Viosca Knoll region was
retrieved 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 of
which are solitary corals (Cairns et al. 1993). On the upper slope, L. pertusa forms the most extensive reef structures
along with the scleractinian Madrepora oculata and a number of species of gorgonian, antipatharian, and bamboo
corals (Schroeder et al. 2005). The faunal communities associated with these structures consist mainly of the general
background fauna of the Gulf of Mexico, but also contain a few species that may have specific relationships with
the 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 half
graben surrounded on three sides by steep escarpments (MacDonald et al. 2003, Milkov & Sassen
2003). 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 area
impacted by this system has resulted in extensive areas of outcropping authigenic carbonate that
provide 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 vestimentiferan
aggregations 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 at
the 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 dense
brine 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 or
no sulfide (Nix et al. 1995, MacDonald et al. 2000, Joye et al. 2005). Surface manifestation of
brine seeps may be limited to small, darkly colored depressions, or the dense seeping fluids may
accumulate in large pools and rivers along the sediment surface (MacDonald et al. 1990b). One of
the most striking brine features of the ULS is Brine Pool NR1 in GC 233 (Figure 3). This was a
pockmark likely formed from the rapid sublimation of a large volume of gas hydrate (MacDonald
et al. 1990b). The brine originates from a shallow (<500 m) subsurface salt diapir and collects in
the depression formed by the blowout event. The pool is approximately 22 m long and 11 m wide
with overflow on the southern edge of the pool (MacDonald et al. 1990b). The hypoxic brine
contains high concentrations of methane and bubbles rise from the pool. Most of the shoreline is
inhabited by a wide band of the mussel B. childressi (MacDonald et al. 1990b). Most other brine
seep sites are dominated by more diffuse surface expressions of seepage. GC 204 contains areas of
rapid fluid transport related to active salt tectonism, which results in brine and methane hydrate
in surficial sediments (Milkov & Sassen 2003) that are inhabited by beds of B. childressi. In GB
382, MC 885, and MC 929, active seepage of brines that contain elevated metal concentrations
leads 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 pool
with small mixed Bathymodiolus species mussel beds and patches of partially buried spatangoid sea
urchins around the periphery was recently discovered at 2340 m depth in Alaminos Canyon 601
(Fisher et al. 2007, Roberts et al. 2007).
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SYMBIOTIC FAUNA
Different surface expressions of seepage are associated with different types of biota depending on their physiological requirements. Two groups of megafauna with symbiotic thiotrophic
and/or methanotrophic bacteria dominate: vestimentiferan tubeworms in the polychaete family
Siboglinidae, and bivalves, including bathymodiolin mussels and multiple families of clams. The
vestimentiferan siboglinids and clams harbor microbial endosymbionts that utilize sulfide as an
energy 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 3
The shoreline of Brine Pool NR1. The interface of the dense hypersaline brine and the overlying seawater is
clearly shown, with the beds of mussel Bathymodiolus childressi along the shoreline. Photo courtesy of
Stephane Hourdez.
clams was revealed by studies of vent taxa, but was greatly expanded by investigations of seep
species. However, the majority of our knowledge of bathymodiolin physiology comes from studies of GoM species. In waters shallower than 1000 m in the GoM, three species of vestimentiferan
tubeworms, 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 of
vestimentiferans and two additional species of bathymodiolins are known. The recent exploration
of the Campeche Knolls (3000 m depth) in Mexican territorial waters of the GoM (MacDonald
et al. 2004) led to the discovery of one vestimentiferan, one bathymodiolin, one vesicomyid, and
one solemyid species whose taxonomic status remains unresolved.
Tubeworms
Vestimentiferan tubeworms were originally described as a separate phylum related to the phylum
Pogonophora ( 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 the
polychaete 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), and
an undescribed species (McMullin et al. 2003) are known. On the lower slope two undescribed
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Figure 4
Aggregations of the tubeworms Lamellibrachia luymesi and Seepiophila jonesi. Young and actively growing
aggregations are lighter in color whereas older, slower growing tubeworms are colonized by hydroids and
other epifauna and appear darker in color. Also shown in the foreground is a colony of the gorgonian
Callogorgia americana delta. Photo courtesy of Katherine Luley.
species of lamellibrachids (Brooks et al. 1990, Nelson & Fisher 2000, Cordes et al. 2007a, Roberts
et al. 2007) and Escarpia laminata are known ( Jones 1985).
All vestimentiferans lack a digestive tract as adults and rely on internal, sulfide-oxidizing bacteria
for their nutrition (Fisher 1990). The mode of transfer of nutrients to the host may involve
intracellular 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). Symbionts
are acquired de novo by each successive generation and the symbiont strain is determined both
by location and host species. For example, L. luymesi and S. jonesi on the upper slope possess very
similar symbionts, whereas E. laminata from Alaminos Canyon harbors symbionts from a different
clade 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 that
the 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 an
internal organ, the trophosome. Trophosome tissue is highly vascularized and the vascular system
contains 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, obtain
both oxygen and sulfide across the plume surface from areas where sulfide-rich hydrothermal
effluent 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 species
can obtain sufficient sulfide across the roots to fuel net autotrophy, while taking up oxygen and
carbon dioxide across the plume (Freytag et al. 2001).
Young ULS vestimentiferans settle on carbonates or other hard substrates in areas of active
seepage where sulfide is present and can presumably take up sulfide across their plumes as it is
released from the sea floor sediments. The importance of L. luymesi roots as a site for sulfide uptake
increases as surface expression of seepage subsides (Cordes et al. 2005a). Measurements of sulfide
levels among vestimentiferan tubeworm aggregations on the sea floor confirm that sulfide is only
rarely detectable around the plumes of adult L. luymesi, and when it is detectable, it is present in
low 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 immediately
beneath the large aggregations, suggesting that the majority of the sulfide requirements for older
L. 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 sulfide
were not sufficient to match the high sulfide demands calculated for even moderate-sized aggregations (Cordes et al. 2003, 2005a). The sulfide produced in seep sediments is primarily a result
of 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, occasionally 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 produced 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 average of 85% of the sulfate generated by their symbionts through epithelial channels in their roots
that may exchange sulfate for bicarbonate (Dattagupta et al. 2006). By releasing sulfate through
their roots, L. luymesi supplies an energetically favorable oxidant in deeper sediment layers. When
this is added to models of sulfide supply, the additional sulfate released through the roots was
sufficient to match the demands of even large L. luymesi aggregations in sediments rich in oil and
methane (Cordes et al. 2005a). Modeling of in situ stable isotope values and geochemical profiles
near tubeworm aggregations also implicated sulfate release by L. luymesi roots and its subsequent
oxidation in sediments beneath tubeworm aggregations (Dattagupta et al. 2008). The release of
approximately 80% of the sulfate generated by L. luymesi could maintain a steady sulfide/sulfate
ratio in root-influenced sediments, resulting in a consistent sulfide supply and the persistence of
tubeworm 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 be
more than 400 years of age and a 1.1-m S. jonesi individual was estimated to be nearly 300 years of
age. This extreme longevity is related to low mortality rates of less than 0.1% annual mortality for
L. luymesi individuals of approximately 50–60 years of age (Cordes et al. 2003). Young L. luymesi
and S. jonesi can grow at rates up to 10 and 7 cm·yr−1 , respectively, but by 50 years of age, their
growth rates slow to less than 1 and 0.5 cm·yr−1 , respectively. However, even some of the largest
L. luymesi and S. jonesi individuals measured exhibited some growth, suggesting that growth is
indeterminate 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 of
reproductive seasonality (Tyler & Young 1999). Gametes are fertilized internally; the females take
sperm 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 can
persist for three weeks (Young et al. 1996) and L. satsuma larvae for more than six weeks (Miyake
et al. 2006). This long larval stage should favor fairly broad dispersal distances and relatively high
larval exchange among widely separated populations. Studies of the population genetic structure
of L. luymesi indicate that genetic exchange occurs among populations separated by as much as
560 km, resulting in relatively little genetic differentiation among aggregations within sites or
among sites within regions of the GoM (McMullin et al. 2008). Continuous reproduction for
hundreds of years and long-range dispersal ability increase the probability that a given individual’s
larvae will encounter an appropriate location in a currently active seep site.
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Mussels
At least five species of bathymodiolin mussels with chemosynthetic and/or methanotrophic symbionts 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 fisheri
from 500 m to at least 1400 m, and Idas macdonaldi from 500 m to approximately 700 m (Gustafson
et al. 1998; Roberts et al. 2007; E.E. Cordes & C.R. Fisher, unpublished data). B. childressi from
ULS and Alaminos Canyon were originally considered to be two separate populations on the basis
of allozyme data (Craddock et al. 1995). However, analyses of combined data from two mitochondrial and six nuclear DNA markers indicate that these populations, at seeps ranging from 500 m to
more 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 and
levels 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 bacteriocytes
clustered near the outer edges of the gill filament tissues (Fisher et al. 1987), a position that likely
facilitates diffusion of methane and oxygen from the gill surface to the symbionts (Nelson & Fisher
1995). Bathymodiolins do not contain binding proteins for transport of methane or oxygen, so
diffusion is the sole mode of transport of dissolved gasses (Childress & Fisher 1992). The symbionts
obtain energy through the oxidation of methane and incorporate methane-derived carbon into
organic compounds (Childress et al. 1986, Fisher et al. 1987). Transfer of nutrients from the
symbionts to the host is largely accomplished through intracellular digestion of the symbionts
rather than translocation of metabolites (Streams et al. 1997). This symbiosis is so efficient that
B. 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), though
they appear to obtain most of their nutrition from their symbionts (Fisher & Childress 1992), as
suggested 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 (Nix
et al. 1995, Bergquist et al. 2004). At the large mussel bed of B. childressi surrounding Brine Pool
NR1 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 than
B. childressi further from the pool’s edge (Smith et al. 2000). These characteristics were correlated
with decreasing methane and increasing sulfide concentration gradients moving away from the
pool’s edge (Smith et al. 2000, Bergquist et al. 2005). Further, B. childressi transplanted from the
inner zone of the brine pool to GC234 and Bush Hill for 1 year exhibited decreased growth rates
and condition indices, whereas those transplanted from GC234 and Bush Hill to the brine pool
exhibited 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 shifted
after 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 planktotrophic 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 in
some populations may be compromised by the presence of two parasites, a eubacteria related to
Chlamydia and a trematode (Powell et al. 1999).
B. brooksi occurs at intermediate depths on the continental slope of the GoM and contains
both methanotrophic and sulfide-oxidizing gamma-proteobacteria symbionts. The two types of
symbionts 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 abundances
of the two different types of symbionts can vary in populations that inhabit different microenvironments (Fisher et al. 1993, Duperron et al. 2007a). In one study, the tissue-stable carbon isotope
values 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 (Fisher
1993). The fact that the tissue-stable carbon values were not intermediate between those expected
for bivalves that contain sulfide-oxidizing (or thiotrophic) and methanotrophic symbionts suggests
that some of the DIC produced by the methanotrophic symbionts is subsequently fixed by the
thiotrophic symbionts (Fisher 1993, Duperron et al. 2007a).
The deepest living bathymodiolin in the GoM, B. heckeri, contains symbionts with two different
morphologies in bacteriocytes that line the gill filaments (Cavanaugh et al. 1987). Recent analyses
of the 16S rRNA phylotypes of the symbionts of B. heckeri demonstrated the presence of four
phylotypes: one methanotroph, one methylotroph, and two thiotrophs (Duperron et al. 2007a). A
commensal polynoid worm, Branchipolynoe seepensis, is commonly found in this species (Pettibone
1986).
T. fisheri inhabits the base of L. luymesi aggregations and is occasionally found in beds of
B. 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 polychaete
that is morphologically very similar to Branchipolynoe symmitilida (Fisher 1993), but it is genetically
distinct from both B. symmitilida and B. seepensis (S. Hourdez, personal communication). Very little
is known of the other GoM seep mytilid, Idas macdonaldi, because it has only been documented
from a single seep site in GB 386 (Gustafson et al. 1998). Other members of the genus Idas are
associated 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 least
two species of vesicomyids (Vesicomya chordata and Calyptogena ponderosa), two species of lucinids
(Lucinoma atlantis and an undescribed species of Lucinoma), one thyasirid (Thyasira oleophila), and
an unidentified solemyid are known. All these bivalves harbor thiotrophic symbionts and exhibit a
variety of adaptations to their symbiotic lifestyle (reviewed in Fisher 1990 and Childress & Fisher
1992).
Similar to all described vesicomyids, C. ponderosa and V. cordata harbor intracellular sulfideoxidizing symbionts in bacteriocytes in greatly enlarged gills (Brooks et al. 1987). C. ponderosa and
V. 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 environmental
levels (Fisher 1996). Sulfide is taken up across the surface of the foot, which is buried in the
sediments, and oxygen is taken up through siphons extended into the water column. These clams
burrow horizontally through the sediment, leaving characteristic trails on the sea floor (Rosman
et al. 1987, Scott & Fisher 1995).
Lucinids, solemyids, and some thyasirids have a reduced gut and feeding palps and have gammaproteobacteria symbionts associated with hypertrophied gills (Distel & Felbeck 1987, Fisher 1990,
Duperron et al. 2007b). Thyasirids house their symbionts extracellularly (Southward 1986, Fisher
1990), although many thyasirids lack symbionts entirely (Dufour 2005). Nutrient transfer from
symbiont to host appears to be through intracellular digestion (Distel & Felbeck 1987), although
this has not yet been verified for all species. Environmental symbiont transmission has been shown
in L. aequizonata and all other lucinids examined to date (Gros et al. 1999). Lucinids and thyasirids
form extensive subsurface feeding tubes to acquire sulfide from deeper anoxic sediment layers
(Turner 1985, Distel & Felbeck 1987). Some lucinids are suggested to oxygenate their burrows
and mobilize the sulfide from pyrite deposits, thereby “mining” sulfide from the sediments (Dando
et al. 1994). Some thyasirids are capable of extending their foot more than 30 times the length
of the shell, potentially mining sulfides from deep anoxic layers of sediment (Dufour & Felbeck
2003). Because clams from these families live beneath the sediment surface, little is known about
their abundance at the seeps of the GoM, although extensive beds of disarticulated shells are often
encountered at seep sites (Rosman et al. 1987).
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COMMUNITY ECOLOGY
Along with the symbiont-containing species of the ULS, a total of 120 macrofaunal taxa (retained
on 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 representatives
of 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-sea
chemoautotrophy-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 persist
in 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 dominate
vent and some seep commuities, nonendemic species also occur in high abundances in ULS
seep environments. These nonendemic fauna have been classified as colonists when they occur
in greater numbers at the seeps than in the background habitats, or vagrants when they occur in
similar densities to nonseep habitats (Carney 1994). Any of these seep inhabitants may be taking
advantage of the local primary production in these deep-sea chemosynthetic habitats (Fisher
1993, MacAvoy et al. 2002, Gilhooly et al. 2007), or merely occupying the complex habitat
provided by the foundation species of tubeworms and bivalves. Below is a theoretical framework
for seep community succession based on hypotheses generated from the ULS seeps prior to the
year 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 biogenic and thermogenic methane and oil are delivered to the sediment-water interface (Sassen
et al. 1994a). As authigenic carbonates begin to precipitate, they provide the necessary hard substrate 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 Pool
NR1 (MacDonald et al. 1990b). Although these species may settle concomitantly, high methane
concentrations would favor the establishment and growth of methanotrophic mussel populations.
Bathymodiolins will not only dominate the space available, but also are capable of filter feeding
and reducing the numbers of larvae that reach the substrate (Bergquist et al. 2003a). This phenomenon may contribute to an initial phase of low levels of L. luymesi and S. jonesi recruitment
into 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 elevated
methane and sulfide concentrations. For example, the iceworm, Hesiocaeca methanicola, is able to
tolerate anoxia in excess of 96 hours (Fisher et al. 2000). An orbiniid polychaete, Methanoaricia
dendrobranchiata, can survive for days in anoxic conditions in the presence of millimolar concentrations of sulfide and contains high-affinity hemoglobins and enlarged gills that allow it take
up oxygen from very low environmental concentrations (Hourdez et al. 2002). Such adaptations
allow these and other endemic species to exploit the locally elevated microbial primary production
in 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 17
collections (Bergquist et al. 2005)] suggests that although there are advantages to the colonization
of this productive habitat, the environmental conditions present require a relatively rare set of
adaptations to tolerate exposure to seep fluid. B. childressi mussel bed associates are members of
a set of families that have been successful at seeps and vents worldwide, including the hesionid
and polynoid polychaetes, bresilid shrimp, neritoid and provannid gastropods, and the galatheid
crabs (Sibuet & Olu 1998, Tunnicliffe et al. 1998, Van Dover 2000). Although the families are
limited in number, the species-level diversity represented within these groups suggests that this
set 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 persist
for far longer (Nix et al. 1995). Often overlapping with and normally persisting past the B. childressi
mussel 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 oxidation
and carbonate precipitation rates remain high (Aharon & Fu 2000, Cordes et al. 2005a), which
promotes increased L. luymesi settlement rates over the first 10 to 30 years of vestimentiferan
aggregation development (Bergquist et al. 2002). Active recruitment coupled with low rates of
mortality 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 characterized
by 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 tubes
apparently restricts community composition and continues to favor endemic species (Cordes et al.
2005b). B. childressi remains present, along with its associated gastropod Bathynerita naticoidea and
the endemic gastropod Provanna sculpta. Other dominant endemic fauna include the polynoid
polychaetes Harmothoe sp. nov. and Branchinotogluma sp. nov. and the bresilid shrimp Alvinocaris
stactophila. The remainder of the community is largely composed of colonist fauna, including the
gastropods 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 epibenthic water are much reduced from a maximum of 4 μM in young aggregations to 0–1 μM (Cordes
et 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 of
L. luymesi roots may occlude seepage pathways (Bergquist et al. 2003a), consume sulfide before
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**
** *
*
*
**
*
**
*
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GC354
GB425
GB535
GB543
GB544
GC234
GC233
GC232 VK825
GC184 MC885
Figure 5
Succession in seep communities over time. A multidimensional scaling plot that represents the similarity in
composition among the communities associated with tubeworm aggregations and mussel beds from the
upper slope. Distance between objects is based on pairwise Bray-Curtis similarity between fourth-root
transformed 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-aggregation
communities (Bergquist et al. 2003a; Cordes et al. 2005b, 2006) are circles; the size of the circles represents
the relative age of the aggregation (older aggregations = larger circles). Different colored symbols represent
different sites according to U.S. Minerals Management Service oil lease block designations: GB is Garden
Banks, 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 deeper
sediment layers (Cordes et al. 2005a; Dattagupta et al. 2006, 2008). L. luymesi settlement rate
begins to decline owing to the monopolization of existing substrata and the reduced availability of
sulfide above the sea floor (Bergquist et al. 2002, 2003b; Cordes et al. 2003). The existing L. luymesi
population will remain viable owing to their increasing reliance on their roots for sulfide uptake
and 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 requires
exposure to methane in overlying water (Kochevar et al. 1992).
As L. luymesi growth and recruitment continues, aggregations may include hundreds to thousands of individuals (Kennicutt et al. 1995, Bergquist et al. 2002) (Figure 4). Individual aggregations may be restricted to an area of approximately 1 m2 , which is common at many sites in
the GoM (Cordes et al. 2006). Alternatively, large clusters of aggregations can form, covering
hundreds 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 release
of seep fluid from the base of the aggregations, increases the amount of tube surface area exposed
to little or no sulfide (Bergquist et al. 2003a). Once this habitat is made available, more of the
nonendemic background fauna are capable of colonizing the tubeworm aggregations. This leads
to 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 limpets
begin to take advantage of the remaining bacterial biomass in the aggregations. Lower concentrations 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 predatory Eunice sp. that forms tubes on the anterior ends of L. luymesi, results in additional reduction
of primary consumer biomass (Bergquist et al. 2003a).
As epibenthic sulfide concentrations decline further, L. luymesi recruitment finally ceases 40 to
60 years after the local seepage source and substrate were formed (Bergquist et al. 2002, Cordes
et al. 2003). Sulfide is occasionally still detectable in aggregations of this age, but only at very
low micromolar concentrations (Bergquist et al. 2003b, Cordes et al. 2006). The spherical habitat
generated by the tubeworms may be massive at this stage, with L. luymesi length normally ranging
between 85 and 120 cm at 50 years (Cordes et al. 2007b). The number of associated taxa is
positively correlated with the size of the tubeworm-generated habitat, so diversity in this stage
remains fairly high (Bergquist et al. 2003a). The aggregation containing the greatest number of
associated 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 be
composed of a mixture of endemic and nonendemic species, although shifts in community structure
are apparent. The endemic shrimp A. stactophila significantly declines in abundance as does the
endemic galatheid Munidopsis sp. 1. These species are replaced by the shrimp Periclemenes sp. and
Munidopsis sp. 2, both of which significantly increase in abundance with aggregation age. The
former species has been hypothesized to have higher tolerance to reduced chemicals and anoxic
conditions than the latter, whereas the latter are capable of outcompeting the former in more
benign 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 of
fishes, 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 and
scavengers obtain a significant amount of their nutrition from seep primary production (MacAvoy
et al. 2002, 2005). The proximity of the larger, more benign aggregations to aggregations in earlier
successional stages (Figure 4) may allow large, mobile species to forage in areas of greater prey
abundance 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. luymesi
growth 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 tubeworms
lying recumbent on their sides along the sediment surface. However, this does not necessarily
indicate that the individual vestimentiferans are in some way senescent, because their physiological
condition 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 bacteria
leads to the near elimination of the lower trophic levels (Cordes et al. 2005b). However, some
endemic species remain present in lower numbers in the later successional stages. The endemic
species 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 polychaetes
increase in abundance, perhaps taking advantage of the elevation of the tubeworm tubes to feed
in higher flow regimes above the substrate. Members of higher trophic levels also continue to
inhabit 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 habitats (Cordes et al. 2006). Tubeworm aggregations at brine seeps tend to consist of a greater
proportion of S. jonesi and are generally restricted to isolated patches. The persistence of B. childressi in somewhat older aggregations indicates that these brine-dominated sites may also contain
higher 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 aggregations
found in the western Garden Banks sites, near Brine Pool NR1 in GC 233 and in certain locations
within Mississippi Canyon and GC 354, fall into this category (Figure 5). Although the general
successional trends described above (reductions in biomass, shifts in trophic structure, etc.) are applicable 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) are
similar to those of the upper slope at higher taxonomic levels (family and above), but are quite
distinct 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 communities
found at similar depths at the seeps of Barbados and the Blake Ridge than they are to those found
on the upper slope (Cordes et al. 2007a). One of the most significant differences in community
structure with depth is the dominance of the lower trophic level by grazing gastropods on the
upper slope, and their replacement by detritivorous ophiuroids on the lower slope. The lower slope
communities are composed of fewer species in general, containing 50 taxa total and a maximum of
20 taxa in any single collection (Cordes et al. 2007a), whereas 109 taxa are known from the upper
slope 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 fauna
remains relatively constant. Distinctions appear to exist between the communities that inhabit
bathmodiolin beds and vestimentiferan aggregations, with lower diversity and higher biomass
in 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 (Bergquist
et al. 2003a), the model described for the upper slope seep system remains to be tested in the
lower slope communities. In addition to the more typical seep fauna discussed above, there are also
additional types of seep-related communities dominated by mobile sea urchins and pogonophorans
that show little affinity with the upper slope communities (Fisher et al. 2007, Roberts et al. 2007).
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ANRV396-MA01-07
SUMMARY POINTS
1. Hydrocarbon seeps in the Gulf of Mexico arise from the migration of subsurface salt
layers 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 of
bathymodiolin mussels with methane- or sulfide-oxidizing symbionts, and at least two
species of vesicomyid clams with sulfide-oxidizing symbionts are found in association
with hydrocarbon seeps in the Gulf of Mexico.
3. Mussel bed communities consist of mainly endemic species and are characterized by high
biomass and low diversity.
4. Communities that inhabit tubeworm aggregations proceed through a series of successional stages over the course of hundreds of years from high-biomass, low-diversity
communities of primarily endemic species (similar to mussel bed communities), to a
diverse mixture of endemic and nonendemic species, to a final low-diversity, low-biomass
community.
5. Successional shifts in community structure result from the decline in the concentration
of reduced chemicals in the epibenthic layers, partially resulting from the influence of
the 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 of
biogeochemical processes at the seeps is critical.
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2. Testing the succession hypothesis in a variety of settings, particularly at the deeper seeps
of 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 discoveries
of seep endemic species in coral and other hard-ground habitats.
4. Establishing connectivity (in terms of genetic exchange and community similarity) between the seeps of the Gulf of Mexico and the other chemosynthetic communities of the
Atlantic Equatorial Belt, including the Caribbean, Barbados, the Blake Ridge, Brazil, the
southern 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 this
review.
ACKNOWLEDGMENTS
The work reviewed here was supported in large part by grants and contracts from the United
States Minerals Management Service, the National Oceanic and Atmospheric Administration,
and the National Science Foundation. During the preparation of this manuscript, E.E.C. was a
member of the Organismic and Evolutionary Biology Department at Harvard University.
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Contents
Volume 1, 2009
Wally’s Quest to Understand the Ocean’s CaCO3 Cycle
W.S. Broecker p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
A Decade of Satellite Ocean Color Observations
Charles R. McClain p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p19
Chemistry of Marine Ligands and Siderophores
Julia M. Vraspir and Alison Butler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p43
Particle Aggregation
Adrian B. Burd and George A. Jackson p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p65
Marine Chemical Technology and Sensors for Marine Waters:
Potentials and Limits
Tommy S. Moore, Katherine M. Mullaugh, Rebecca R. Holyoke,
Andrew S. Madison, Mustafa Yücel, and George W. Luther, III p p p p p p p p p p p p p p p p p p p p p p p p p p p91
Centuries of Human-Driven Change in Salt Marsh Ecosystems
K. Bromberg Gedan, B.R. Silliman, and M.D. Bertness p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 117
Macro-Ecology of Gulf of Mexico Cold Seeps
Erik E. Cordes, Derk C. Bergquist, and Charles R. Fisher p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 143
Ocean Acidification: The Other CO2 Problem
Scott C. Doney, Victoria J. Fabry, Richard A. Feely, and Joan A. Kleypas p p p p p p p p p p p p p p p 169
Marine Chemical Ecology: Chemical Signals and Cues Structure
Marine Populations, Communities, and Ecosystems
Mark E. Hay p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 193
Advances in Quantifying Air-Sea Gas Exchange and Environmental
Forcing
Rik Wanninkhof, William E. Asher, David T. Ho, Colm Sweeney,
and Wade R. McGillis p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 213
vi
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Atmospheric Iron Deposition: Global Distribution, Variability,
and Human Perturbations
Natalie 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 p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 245
Contributions of Long-Term Research and Time-Series Observations
to Marine Ecology and Biogeochemistry
Hugh W. Ducklow, Scott C. Doney, and Deborah K. Steinberg p p p p p p p p p p p p p p p p p p p p p p p p p p 279
Clathrate Hydrates in Nature
Keith C. Hester and Peter G. Brewer p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 303
Hypoxia, Nitrogen, and Fisheries: Integrating Effects Across Local
and Global Landscapes
Denise L. Breitburg, Darryl W. Hondorp, Lori A. Davias, and Robert J. Diaz p p p p p p p p p 329
The Oceanic Vertical Pump Induced by Mesoscale
and Submesoscale Turbulence
Patrice Klein and Guillaume Lapeyre p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
An Inconvenient Sea Truth: Spread, Steepness, and Skewness
of Surface Slopes
Walter Munk p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 377
Loss of Sea Ice in the Arctic
Donald K. Perovich and Jacqueline A. Richter-Menge p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 417
Larval Dispersal and Marine Population Connectivity
Robert K. Cowen and Su Sponaugle p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 443
Errata
An online log of corrections to Annual Review of Marine Science articles may be found at
http://marine.annualreviews.org/errata.shtml
Contents
vii