Stable isotope variation among the mussel Bathymodiolus childressi and associated heterotrophic fauna at four cold-seep communities in the Gulf of Mexico.
Mussels (Chemical properties)
Mussels (Environmental aspects)
Heterotrophs (Chemical properties)
Heterotrophs (Environmental aspects)
Seeps (Geology) (Research)
Primary productivity (Biology) (Research)
|Publication:||Name: Journal of Shellfish Research Publisher: National Shellfisheries Association, Inc. Audience: Academic Format: Magazine/Journal Subject: Biological sciences; Zoology and wildlife conservation Copyright: COPYRIGHT 2008 National Shellfisheries Association, Inc. ISSN: 0730-8000|
|Issue:||Date: March, 2008 Source Volume: 27 Source Issue: 1|
|Topic:||Event Code: 310 Science & research|
|Product:||Product Code: 2991500 Isotopes NAICS Code: 325188 All Other Basic Inorganic Chemical Manufacturing SIC Code: 2800 CHEMICALS AND ALLIED PRODUCTS|
|Geographic:||Geographic Scope: United States Geographic Name: Gulf of Mexico Geographic Code: 1USA United States; 0GULF Gulf of Mexico|
ABSTRACT Efforts to determine the utilization of Gulf of Mexico
(GOM) chemosynthetic production by benthic predators have relied on
stable isotope differences between photosynthetic and chemosynthetic
production. Whereas the photosynthetic [[delta].sup.13]C value in GOM
surface waters is relatively uniform, chemosynthetic production may
differ in different areas depending on prevalence of thiotrophy versus
methanotrophy and inorganic carbon source. In this paper we compare the
[[delta].sup.13]C and [[delta].sup.15]N signatures of the
symbiont-containing mussel, Bathymodiolus childressi Gustafson, 1998,
from four different chemosynthetic sites to test the hypothesis that
methanotrophic production results in significant differences among them.
Bathymodiolus childressi from two areas characterized by brine seepage
and biogenic methane (GC425 and GC233) had very low [[delta].sup.15]N
(-3.7[per thousand] and -16.6[per thousand]) and [[delta].sup.13]C
(-57.5[per thousand] and -63.5[per thousand]) relative to areas with
substantial thiotrophic production (GC234 and GC185). Bathymodiolus
childressi from each chemosynthetic community had significantly
different [[delta].sup.13]C, and three of the sites also had distinct
[[delta].sup.15]N values. The [[delta].sup.13]C and [[delta].sup.15]N
signatures of hagfish (Eptatretus sp.) and giant isopods (Bathynomus
giganteus) captured from two sites showed little or no chemosyntheic
usage. Squat lobsters (Munidopsis sp.) showed heavy incorporation of
chemosyntheic production, but did not directly consume B. childressi.
KEY WORDS: Bathymodiolus childressi, stable isotopes, chemosynthesis
The continental slope in the Gulf of Mexico (GOM) supports communities of metazoans containing chemoautotrophic bacteria, comprised mostly of tubeworms (Seepiophila jonesi Gardiner, McMullin & Fisher 2001 and Lamellibrachia luymesi van der Land & Norrevang, 1975) and mussels (Bathymodiolus childressi Gustafson, 1998). These organisms harbor sulfide (tubeworms) or methane (mussels) oxidizing bacteria, which provide nutrition to their hosts. Free-living bacteria are also found at the chemosynthetic sites (also called "cold-seeps"), either in mats or as filaments on surfaces (Brooks et al. 1987, Sassen et al. 1999, MacDonald 2002). The communities also provide habitat for a host of heterotrophic invertebrates, including polychaete worms, shrimp, squat lobsters, fish, and many other organisms (Brooks et al. 1987, Kennicutt et al. 1992, MacAvoy et al. 2005). The nutrition created by the chemosynthetic bacteria is augmented by the photosynthetically fixed nutrients drifting in from the euphotic zone (Levin & Michener 2002, MacAvoy et al. 2002, MacAvoy et al. 2005, Tyler et al. 2007). The chemosynthetic production may be a significant source of nutrition to heterotrophs found there in an otherwise nutrient-poor deep ocean, (Carney 1994, Pequegnat 1983).
One method of tracing nutrient use among organisms within GOM seep environments is through stable isotope analysis (see reviews in: Kennicutt et al. 1992, Levin 2005). Photosynthetically fixed carbon and nitrogen is generally much more enriched in [sup.13]C and [sup.15]N than material derived though chemosynthesis at the cold seeps. As an organism incorporates nutrients, its isotope composition resembles the isotope signature of those materials. Therefore, if One could establish the isotope values of the photosynthetic production, chemosynthetic production, and heterotrophs from the seeps, one could estimate the importance of chemosynthetic production.
It is apparent, however, that different chemosynthetic sites in the GOM may have different carbon and nitrogen isotope signatures (although they are still different relative to photosynthetic primary production). The differences in [[delta].sup.13]C signatures correlate with the relative importance of thiotrophy versus methanotrophy among the sites. Within methanotrophic sites, signatures also differ whether the methane source is biogenic or thermogenic. If the sites have a specific isotope signature by virtue of the methods and materials that form the basis for chemosynthetic production, then the degree of heterotrophic utilization of particular sites could be quantified. Stable isotopes usually cannot determine exactly what a heterotroph has been consuming (because isotope compositions of sources may overlap), but they can be used to constrain what it has not been eating, providing insights into possible isotope ranges of food sources (Levin 2005, MacAvoy et al. 2005).
In this paper the [[delta].sup.13]C and [[delta].sup.15]N signatures of the symbiont-containing mussel, B. childressi from four different chemosynthetic sites are compared with test the hypothesis that variation in the contribution of methanotrophic production to nutrition results in significant differences in isotope content among the sites. An observation of different signatures would suggest that researchers utilizing stable isotopes to investigate chemosynthetic usage by heterotrophs should consider the signature of chemosynthetic sites near the area of capture as a better tracer signature than those further away. Additionally, the [[delta].sup.13]C and [[delta].sup.15]N signatures in heterotrophic fauna captured from two sites were examined to investigate whether those organisms used chemosynthetic production.
MATERIALS AND METHODS
Sampling was conducted during 1997, 1998, and 2002 in the Gulf of Mexico Green Canyon and Garden Banks Lease Areas on research cruises of the submersible Johnson Sea Link and the RV Edwin Link. The sites range in depth between 540 and 640 m. Sampling sites in this paper are referenced by the 4.8 x 4.8 [km.sup.2] numbered lease block in which they lie. Samples were collected from GC234 during dive numbers JSL2889 and JSL2877, from GC185 during JSL2857 and JSL2873, from GC233 during JSL2876 and JSL2870, and from GB425 during JSL2883 and JSL4053.
The GC234 site (27[degrees]44.7'N; 91[degrees]13.3'W) is at a depth of approximately 540 m. The fauna at this site is dominated by tubeworms (S. jonesi and L. luymesi) with abundant mussel (B. childressi) beds. Methane gas and oil has been observed leaking from sediments (Nix et al. 1995, Sassen et al. 1999).
The GC233 site, also called the Brine Pool or NR1 (27[degrees]43.4'N; 91[degrees]16.8'W), is at a depth of approximately 640 m. It is dominated by an anoxic brine pool arising from saline seepage along a fault (Reilly et al. 1996, Sassen et al. 1999). Methane utilizing mussels, Bathymodiolus childressi, are the dominant symbiont-bearing fauna at the site; tubeworms are scarce (Dattagupta et al. 2004, MacDonald et al. 1990). GC233 and GC234 are 5.419 km apart.
The GC185 site, Bush Hill (27[degrees]46.96'N; 91[degrees]30.46'W) lies at depths between 540-580 m. It is an active hydrocarbon seep area supporting chemoautolithotrophic communities that have been studied for various purposes for approximately 20 y. Tubeworms are the visually dominant symbiont-containing group at the site although mussels symbiotic with thiotrophic or methanotrophic bacteria (Tamu fisheri and Bathyrnodiolus childressi, respectively) also occur here. Methane and oil are actively seeping from the sediments in several places on Bush Hill, bacterial mats and carbonate outcrops are abundant, as are shallow gas hydrates (Brooks et al. 1987, Fisher 1996, Kennicutt et al. 1992, Nix et al. 1995, Sassen & MacDonald 1997, Sassen et al. 1999).
The GB425 (Garden Banks 425, mud volcano) site is an active mud volcano with high rates of discharge and is associated with a brine pool. The mud volcano has frequent eruptions of warm water (10[degrees]C or more higher than the ambient environment), and the methane-utilizing mussels, Bathymodiolus childressi, are the dominant symbiont-bearing fauna at the site. The site is characterized by abundance of barite deposits originating from brine precipitates, which appear by contact with sulfate-rich seawater (MacDonald 2002).
Little is known about the hydrocarbon seep community located in GC354, except that it is a small, "standard" upper-middle continental slope seep site, characterized by mussel and tubeworm colonies (R. Sassen, pers. comm.).
Off-site mobile predators were caught with a surface deployed Z-frame trap, 150 x 180 x 90 cm, set approximately 2 km off the location of GC354 (27[degrees]35.22' N; 91[degrees]48.34' W), in an area known from prior surveys to lack active seep communities. The Z-trap was constructed of 2.5 cm square trap mesh, equipped with two 20 cm entry mouths, and baited with menhaden in a wire bait cage to minimize consumption (MacAvoy et al. 2002). The trap was deployed for two days (June 25-27, 2002) before retrieving. Heterotrophic fauna and mussels were captured directly by the Johnson Sea Link submersible using the suction arm or scoop.
Stable Isotope Analysis
Tissue samples were dissected at sea from most animals and were frozen until shipment to the stable isotope laboratory. Some hagfish (Eptatretus sp.) were frozen on ship and dissected back at the laboratory. The tissue types sampled were muscle tissue for heterotrophic invertebrates and mantle tissue for the mussels. In the laboratory, samples were thawed, dried at 60[degrees]C for three days and homogenized by grinding in a mortar and pestle. All samples were lipid extracted by refluxing the samples in distilled dichloromethane for ~35 min (Knoff et al. 2002).
A Carlo Erba elemental analyzer coupled to a Micromass Optima isotope ratio mass spectrometer (VG/GV Micromass, Manchester, UK) was used to obtain [[delta].sup.13]C and [[delta].sup.15]N values (Fry et al. 1992, Giesemann et al. 1994).
The isotope compositions are reported relative to standard material:
[[delta].sup.x] E = [[([sup.x]E/[sup.y]E).sub.sample]/[([sup.x]E/[sup.y]E).sub.standard] - 1] x 1, 000 (1)
where E is the abundance of the element analyzed (C or N) and x is the atomic weight of the heavier isotope, and y the lighter isotope (x = 13, 15 and y = 12, 14 for C and N, respectively). The standard materials to which the samples are compared are Pee Dee Belemnite for carbon and air [N.sub.2] for nitrogen. Error in measurements was typically 0.2[per thousand].
Nonparametric tests were used for all comparisons. Mann Whitney U-tests were used for two group comparisons and Kruskal-Wallace tests were used for all multiple comparisons ([alpha] = 0.05). The Dunn procedure was used to compare specific differences among groups if Kruskal-Wallace indicated a significant difference (Rosner 1990). The Dunn procedure reduces the risk of Type 1 error inherent in multiple comparison techniques by increasing the Z-score needed to reject the null hypothesis as the number of individual groups (treatments) increases. The statistical comparisons were only made when individual groups (treatments) had an n [greater than or equal to] 3. Microsoft Excel X (Microsoft, Inc.) and JMP Start Statistics 3rd edition (SAS Institute) were used for individual statistical tests.
RESULTS AND DISCUSSION
Bathymodiolus childressi [[delta].sup.13]C Signatures
The B. childressi [[delta].sup.13]C value from the four seepage sites were all significantly different from each other (P < 0.05), with the brine seepage areas (GC233 and GB425) being more [sup.13]C-depleted than the tubeworm dominated sites (GC185 and GC234) (Table 1, Fig. 1). The bacteria with which the B. childressi are symbiotic do not fractionate methane carbon upon uptake, although free-living methanotrophs do (Brooks et al. 1987, Kennicutt et al. 1992). The B. childressi carbon signature reflects methane of different origins. Methane produced by methanogenic bacteria is highly depleted in [sup.13]C, whereas that associated with fossil hydrocarbons (thermogenic) tends to be [sup.13]C enriched (Sassen et al. 1999). It has been suggested previously that methane from GC185 is mostly of thermogenic origin, where as GC233 methane arises from biogenic sources (Sassen et al. 2003). The sites GB425 and GC234 likely have a mixture of methane from both sources, because the [sup.13]C isotope compositions found in B. childressi at these sites are intermediate to the other two. At GB425 (a brine volcano site) more [sup.13]C depleted B. childressi were observed than at GC234, suggesting biogenic methane sources dominate at brine sites. There is clearly a [[delta].sup.13]C label within the B. childressi mantle that differentiates the sites (also the case for [[delta].sup.15]N, only less dramatically). Potentially, this label could assist researchers to make more accurate estimations of the endmember signals for establishing heterotrophic usage of B. childressi tissue (and presumably, other methanotrophically fixed carbon) from the different sites. The degree of dependence that heterotrophs have on B. childressi or other chemosynthetic material may be underor over-estimated if the local carbon isotope signature is not specifically known.
Bathymodiolus childressi [[delta].sup.15]N Signatures
The B. childressi [[delta].sup.15]N values were not significantly different between GC185 and GC234. Those from GC233 and GB425 were significantly different from each other and the other two sites (Table 1, Fig. 1). Both brine seepage sites had negative [[delta].sup.15]N, which seems to be characteristic of brine areas, and GC233 had markedly lower [[delta].sup.15]N than GB425. It is likely that the [[delta].sup.15]N range reflects a dilution of the very [sup.15]N depleted ammonium values occurring at the sediment water interface (Lee & Childress 1996).
[FIGURE 1 OMITTED]
Munidopsis sp. (squat lobsters) are [sup.13]C-enriched (2[per thousand]-8[per thousand]) relative to B. childressi from the same site (GC185) (Fig. 2). The [[delta].sup.15]N values for the Munidopsis sp. were between 4[per thousand] and 9[per thousand] higher than the mussels. Whereas these [[delta].sup.13]C and [[delta].sup.15]N values suggest that some mussel tissue may have been consumed by the Munidopsis sp., the values are more enriched than would be expected for a predator on B. childressi (most reported enrichments are between 1.0[per thousand] and 1.5[per thousand] for [[delta].sup.13]C and 3[per thousand] and 3.5[per thousand] for [[delta].sup.15]N, reviewed in Lajtha & Michner 1994). Although the Munidopsis sp. are clearly not relying heavily on B. childressi, they are also not extensively relying on photosynthetic primary production, which has a [[delta].sup.13]C of -19[per thousand] to -20[per thousand] and [[delta].sup.15]N of 4[per thousand]-7[per thousand] (Fry 1983, Macko et al. 1984) in the northern Gulf of Mexico. The Munidopsis sp. are relatively small crustaceans, total length being between 3 and 5 cm when adults, including the two large chelipeds, which can be over one-half the total body length. The small decapods were likely preying on other small heterotrophs, which in turn seem to be feeding on material produced by free-living chemosynthetic bacteria (MacAvoy et al. 2005). It is likely that at these shallow seep sites (500 800 m), there is photosynthetic production drifting into the system (Tyler et al. 2007). Recent work has suggested that a seasonal pulse of photosynthetic production to these sites might coincide with the spawning of B. childressi, strongly suggesting a link between the photic zone and the seep communities on the continental shelf (Tyler et al. 2007).
[FIGURE 2 OMITTED]
Hagfish and lsopods
A large number of Bathynomus giganteus Milne Edwards, 1879 (giant isopods; n = 8) and Eptatretus sp. (hagfish; n = 39) were captured at GC354, a site similar to GC234 (R. Sassen, pers. comm.). The B. giganteus were more enriched (P = 0.013) in [sup.13]C than the hagfish (-16.5 [+ or -] 0.6[per thousand] versus -17.5 [+ or -] 0.6[per thousand], respectively) although the [[delta].sup.15]N values were not significantly different (13.5 [+ or -] 0.7[per thousand] and 13.6 [+ or -] 0.7[per thousand] for B. giganteus and Eptatretus sp. respectively). No mussels or other chemosynthetic material could be retrieved from GC354; hence the isotope range for locally derived carbon or nitrogen is not known. The biota at this site is typical of other chemosynthetic sites, being characterized by mussels and tubeworm colonies resembling by GC185 and GC234. Even without knowledge of the isotope signature of chemosynthetic material at GC354, the [[delta].sup.13]C values of the Eptatretus sp. are so elevated that it is very probable that at this location these organisms derive most of their carbon from photosynthetic material. The B. giganteus captured off of other chemosynthetic sites in a previous study also showed slightly higher [[delta].sup.13]C values relative to those reported here (GC185-15.7 [+ or -]0.1[per thousand]; n = 8), GC233 - 16.4 [+ or -] 1.2[per thousand]; n= ll) and GC234-15.7[per thousand] [+ or -]0.3; n = 2 (MacAvoyet al. 2002). The giant isopods examined here were generally between 10 cm and 16 cm total length, and were somewhat smaller than the isopods from the earlier collections, which ranged up to 48 cm total length (MacAvoy et al. 2002). The <1[per thousand] difference between earlier off-site collections and those reported here is probably because of slight differences in age-related feeding strategies, which is reflected by size differences. The [[delta].sup.15]N values for GC354 B. giganteus are approximately l[per thousand] to 1.5[per thousand] lower than those from GC185 or GC234, also suggesting slight differences in food choice (GC234 14.5 [+ or -] 0.2[per thousand]; n = 2, and GC185 14.0[per thousand] 1.1[per thousand]; n = 8), although they were elevated relative to those from GC233 (12.2 [+ or -] 5.9[per thousand], n = 6) (MacAvoy et al. 2002).
The B. childressi mussels from different hydrocarbon seep sites have different [[delta].sup.13]C and [[delta].sup.15]N values. Researchers who are using stable isotopes to determine the importance of shellfish biomass to predators that frequent seep areas need to consider the isotope signature of the local community when evaluating that importance. Small heterotrophs associated with the seep sites have lower carbon values, suggesting a chemosynthetic food source. However, the B. childressi mussels do not seem to be an important component in the small heterotrophs diet. Larger benthic predators, the Bathynomus giganteus and Eptatretus sp. derive most of their nutrition from photosynthetic sources and probably exploit chemosynthetic material only to a limited degree. This could be because of more abundant photosynthetic material at the shallow depths that these organisms were found or the inability of the predators to successfully overcome the physical defenses of seep fauna.
The authors thank Dr. Ian MacDonald of the Geochemical and Environmental Research Group, Texas A&M University and Dr. Robert Avent of the Mineral Management Service for their interest and support and their special thanks to Drs. Charles Fisher, Derk C. Bergquist, John K. Freytag, Erick Cortez, Stephane Hourdez and Erin McMullen (Penn State University) for their help on an off the ship. This research could not have been accomplished without the crews of the R.V. Edwin kink and Johnson Sea Link (Harbor Branch Oceanographic, Fort Pierce, FL). Partial support for this work was provided by Mellon funds from American University to SEM. EM was supported by a Dean's Undergraduate Research Award from American University. This work was also supported in part by subcontract L100094, $700033 and $70027 to the Mineral Management Service project RF-6899 and the Mineral Management Service, Gulf of Mexico Regional OCS office through contract #1435-01-96-CT 30813 and NSF grant OCE 0118946 to SAM.
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S. E. MACAVOY, (1) * R. S. CARNEY, (2) E. MORGAN (1) AND S. A. MACKO (3)
(1) Department of Biology, American University, Washington, District of Columbia 20016; (2) Coastal Studies Institute, Louisiana State University, Baton Rouge, Louisiana 70803; (3) Department of Environmental Sciences, University of Virginia, Charlottesville, Virginia 22903
* Corresponding author. E-mail: email@example.com
TABLE 1. [[delta].sup.13]C and [[delta].sup.15]N for Bathymodiolus childressi from the four cold-seep sites. Means, standard deviations (sd) and number of samples (N). GC233 GC185 [[delta].sup.13]C -63.5 [+ or -] -38.9 [+ or -] 2.79[per thousand] (8) 1.2[per thousand] (7) [[delta].sup.15]N -16.6 [+ or -] 2.1 [+ or -] 2.1[per thousand] (8) 1.6[per thousand] (7) GC234 GB425 [[delta].sup.13]C -43.7 [+ or -] -57.5 [+ or -] 1.5[per thousand] (6) 5.8[per thousand] (9) [[delta].sup.15]N 3.1 [+ or -] -3.7 [+ or -] 0.9[per thousand] (6) 4.1[per thousand] (9)
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