MARINE ECOLOGY PROGRESS SERIES Vol. 293: 99–108, 2005 Published June 2 Mar Ecol Prog Ser Variations in seep mussel bed communities along physical and chemical environmental gradients Derk C. Bergquist1, 3,*, Clint Fleckenstein1, Julie Knisel1, Brett Begley1, Ian R. MacDonald2, Charles R. Fisher1 1Department of Biology, Pennsylvania State University, 208 Mueller Laboratory, University Park, Pennsylvania 16802, USA 2Physical and Life Sciences Department, Texas A&M University — Corpus Christi, 6300 Ocean Dr. ST320, Corpus Christi, Texas 78412, USA 3Present address: Department of Zoology, University of Florida, 223 Bartram Hall, Gainesville, Florida 32611-8525, USA ABSTRACT: This study examined the faunal communities associated with beds of the hydrocarbon seep mussel Bathymodiolus childressi in the Gulf of Mexico and the relationships between these communities and local environmental characteristics. Mussels, their associated fauna and accompa- nying water chemistry parameters were collected at 17 locations across 4 hydrocarbon seep sites. A total of 19 species, mostly seep endemics, were identified. Species richness and fauna density were significantly and negatively correlated with methane concentration and were significantly and posi- tively correlated with oxygen concentration. Canonical Correspondence Analysis (CCA) separated polychaetes, alvinocarid shrimp and gastropods along gradients of methane and oxygen concentra- tions. Polychaetes and alvinocarid shrimp tended towards lower oxygen and higher methane concen- trations and gastropods tended towards higher oxygen and lower methane. The larger-sized preda- ceous gastropods and decapods were associated with lower sulfide and higher oxygen concentrations. The proportion of the community comprising of endemic species was significantly and positively correlated with mussel biomass and shell surface area. Other measures of habitat com- plexity (mussel density, shell surface area and biomass) explained little of the variation in the associ- ated faunal communities. The results suggest that oxygen and methane availabilities play a substan- tial role in structuring these communities with several dominant seep heterotrophs partitioning resources among different microenvironments. KEY WORDS: Benthic community · Chemical gradient · Habitat complexity · Bathymodiolus childressi · Cold seep Resale or republication not permitted without written consent of the publisher INTRODUCTION symbionts for nutrition, typically dominate vent and seep communities (Childress & Fisher 1992). The Hydrothermal vents and cold seeps host high- physical structures created by these symbiont- density communities that contrast sharply with the bearing invertebrates in turn provide habitat for a surrounding sparsely populated deep-sea floor (Tun- diverse array of heterotrophic fauna including gas- nicliffe 1991, Sibuet & Olu 1998). Production, driven tropods, polychaetes, decapods, and fish (Sarrazin & by bacterial chemoautotrophy, provides the nutrition Juniper 1999, Van Dover & Trask 2000, Bergquist et necessary to support the high biomass associated al. 2003). with vent and seep systems (Fisher 1996). Sessile At cold hydrocarbon seeps on the upper Louisiana invertebrates, such as vestimentiferan tubeworms, slope (ULS) of the Gulf of Mexico, the mussel Bathy- bathymodiolid mussels and vesicomyid clams that modiolus childressi represents one of the most are dependent upon chemoautotrophic bacterial numerous and widespread of the symbiont-bearing, *Email: [email protected] © Inter-Research 2005 · www.int-res.com 100 Mar Ecol Prog Ser 293: 99–108, 2005 structure-forming invertebrates. B. childressi obtains MATERIALS AND METHODS the bulk of its nutrition from methanotrophic sym- bionts housed within its gills (Childress et al. 1986, Site descriptions. During July and August of 1995 Cary et al. 1988, Streams et al. 1997) and inhabits and 1997, mussel beds were sampled at 4 geographi- areas of relatively vigorous seepage (Nix et al. 1995). cally distinct sites within the Minerals Management These habitats are generally characterized by high Service (MMS) Green Canyon and Garden Banks leas- methane concentrations, low oxygen concentrations, ing blocks on the ULS of the Gulf of Mexico (Fig. 1). and occasionally abundant crude oil and hydrogen Two sites characterized by pooled hypersaline fluids sulfide (Smith et al. 2000, Bergquist et al. 2004). that were saturated with methane were designated However, the chemical environments and character- ‘brine’ sites, and 2 sites characterized by an abun- istics of the resident mussels tend to differ substan- dance of hydrocarbons in sediments near the seafloor tially among different seep sites and mussel beds were designated ‘petroleum’ sites. The first brine site, within a seep site. Mussel beds located in areas dom- Brine Pool NR1 (BP), was located at 27° 43’ 24” N , inated by petroleum seepage (MacDonald 1998) tend 91° 16’ 30” W and at a depth of 650 m within the MMS to be characterized by low methane and high sulfide Green Canyon leasing block 233. The site was charac- concentrations, abundant crude oil, and mussels with terized by a single large pool of brine 22 m in length a relatively slow growth rate and poor physiological and 11 m wide, with salinity levels of 120 g kg–1. The condition (Nix et al. 1995, Bergquist et al. 2004). pool was surrounded by a single continuous mussel Mussel beds located in seep sites dominated by brine bed (Bathymodiolus childressi), varying in width from (MacDonald 1998) tend to be characterized by higher 3 to 7 m and covering an area of ~540 m2 (MacDonald methane and lower sulfide concentrations, little et al. 1990). The mussel bed was divided into 2 visibly crude oil and by mussels with a relatively faster distinct zones: inner and outer. The inner edge was growth rate and better physiological condition (Smith characterized by an abundance of smaller mussels at et al. 2000, Bergquist et al. 2004). Within seep sites, high densities. The outer edge was predominately all these characteristics tend to vary substantially large individuals occurring at lower densities with among mussel beds and can vary among different numerous disarticulated shells (Smith et al. 2000). portions of a single mussel bed. For example, at one The second brine site (GB) was located at 27° 37’ N , well studied brine-dominated site (Brine Pool NR 1), 92° 11’ W and at a depth of ~670 m within the MMS a single large mussel bed encircles a pool of super- Garden Banks leasing block 425 (MacDonald et al. saturated brine (MacDonald et al. 1990). The inner 2000). This site supported a patchy distribution of edge of the mussel bed is broadly characterized by high-density mussel beds, with very few vestimentifer- high methane and low sulfide concentrations, sup- ans. Unlike BP, this site did not have a distinct, well- porting smaller mussels with a fast growth rate. The developed brine pool but was characterized by brine outer edge of the mussel bed is characterized by saturated (133 g kg–1), almost liquid sediments (Mac- lower methane and higher sulfide concentrations, Donald 1998). supporting larger mussels with a slower growth rate The first petroleum site, Bush Hill (BH) was located (Smith et al. 2000). Thus, the shell matrices of B. at 27° 47’ N , 91° 30’ 24” W at a depth of 540 to 580 m at childressi beds represent a wide range of habitat characteristics, but the relationships between the res- ident fauna and the physical, biological and chemical characteristics of these mussel beds have not been examined. Carney (1995) reported that the fauna associated with beds of Bathymodiolus childressi are dominated by detritivorous gastropods, polychaetes and crus- taceans and tend to be homogenous in composition among different mussel beds even those separated by tens of kilometers. Unfortunately, the collections in that study were not quantitative and accompany- ing environmental characteristics were not deter- mined. The goals of the current study are: (1) to characterize the communities associated with beds of B. childressi on the ULS, and (2) to determine whether these communities vary with local environ- Fig. 1. Locations of the 4 study sites on the upper Louisiana mental characteristics. slope (ULS) of the Gulf of Mexico Bergquist et al.: Cold seep mussel bed communities 101 the border of the MMS Green Canyon leasing blocks was observed by a scientist in the submersible and 184 and 185 (Brooks et al. 1989, MacDonald et al. documented using a video camera. 1989). The main portion of BH (~10 000 m2) supported In total, 17 collections were made using this method- a large number of vestimentiferan tubeworm assem- ology. One collection was made at each of the 4 differ- blages and numerous mussel beds ranging in size from ent mussel beds at BH (1997), 1 at each of 2 different 1 to 20 m2. Additional scattered mussel beds and tube- mussel beds at GC (1997), 1 at a single mussel bed at worm clumps were found in the 120 000 m2 area sur- GB (1997) and 10 from the single continuous mussel rounding the main site. The second petroleum site bed at BP (6 in 1995 and 4 in 1997). At BP in 1995, 2 col- (GC) was located at 27° 44.7’ N , 91° 13.3’ W, at a depth lections were made along the inner edge, 2 along the of ~540 m within the MMS Green Canyon leasing outer edge and 2 in the middle of the single large mus- block 234 (Brooks et al. 1989). Seep fauna at GC sel bed encircling the pool of brine. In 1997, the cor- occured over an area of several square kilometers, and ners of the square ‘ring’ forced the mussels and their the central portion of this site supported an abundance associated fauna beneath the surface of the underlying of very large vestimentiferan aggregations and numer- brine, compromising our ability to collect all of the ous mussel beds. Actively bubbling methane has com- organisms. As a result of this, we have only reported monly been observed in these mussel beds and much the habitat and community characteristics for these 4 of the sediment was oil stained. Methane hydrates collections and have not included them in the formal breached the seafloor in several locations at both of analyses.