Unusual Benthic Fauna Associated with a Whale Fall in Monterey Canyon, California

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Unusual Benthic Fauna Associated with a Whale Fall in Monterey Canyon, California ARTICLE IN PRESS Deep-Sea Research I 51 (2004) 1295–1306 Unusual benthic fauna associated with a whale fall in Monterey Canyon, California Shana K. Goffredia,*, Charles K. Paulla, Kim Fulton-Bennetta, Luis A. Hurtadob, Robert C. Vrijenhoeka a Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 93950, USA b Center for Insect Science, Department of Ecology and Evolutionary Biology, University of Arizona, 310 Biosciences West, Tucson, AZ 85721, USA Received 13 November 2003; received in revised form 9 April 2004; accepted 20 May 2004 Abstract On February 6, 2002, we discovered an unusual assemblage of deep-sea animals associated with a well-preserved carcass of a gray whale (Eschrichtius robustus) at 2891 m depth in the axis of Monterey Canyon, California. The 9–10 m long carcass was found approximately 31 km off shore, where it settled to the bottom against the northern wall of the canyon’s sedimented floor. This carcass delivered approximately 20,000 kg of organic material to a typically food- limited seafloor. Particularly noteworthy were the low occurrence of large mobile scavengers, the large number of opportunistic deep-sea species, and an abundance of unusual polychaetes. Two of these polychaetes, a spionid and a siboglinid, are new to science. Since this discovery, we visited the whale fall on two subsequent occasions (March and October 2002) to document faunal community changes in one of the deepest large food falls known to date. r 2004 Elsevier Ltd. All rights reserved. Keywords: Whale fall; Deep-sea benthos; USA; California; Monterey; Polychaete; Organic enrichment; Abyssal zone 1. Introduction ever, can alter their metabolism, growth rate, feeding behavior, and reproduction to exploit Most deep-sea communities are limited by low episodic pulses of organic enrichment, such as food availability (Gage and Tyler, 1991). Even in animal carcasses, plant debris, and wood, as well highly productive surface waters, such as those as dissolved and particulate matter (Gage and found in Monterey Bay, California, deep-sea Tyler, 1991; Levin, 2000). Decomposing whale animals are generally adapted toa relatively low carcasses, for example, deliver large pulses of supply of carbon. Some deep-sea animals, how- organic material to the seafloor and serve as habitat islands for unique assemblages of deep-sea macrofauna (Brunn, 1957; Smith and Baco, 2003). *Corresponding author. Division of Engineering and Applied Science, 104-44 California Institute of Technology, Varying in time and space, these discrete resource Pasadena, CA 91125, USA. Tel.: +1-626-395-4108. patches are thought to contribute to habitat E-mail address: goffredi@mbari.org (S.K. Goffredi). complexity and increase biodiversity in deep-sea 0967-0637/$ - see front matter r 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2004.05.009 ARTICLE IN PRESS 1296 S.K. Goffredi et al. / Deep-Sea Research I 51 (2004) 1295–1306 environments (Grassle and Morse-Porteous, 1987; species composition, including two that we believe Butman et al., 1995b; Bacoand Smith, 2003 ). tobe new toscience, observedduring three Based on the number of whale falls discovered separate visits (at 0, 1, and 8 months after during the past several decades of deep-sea discovery). In addition, by mapping marine exploration, these habitat islands may occur mammal remains discovered in Monterey Canyon relatively frequently in time and space, especially we suggest that deposition occurs primarily within along migration corridors for at least eight large material transport conduits, thereby potentially whale species in the northeast Pacific. Smith et al. affecting the diversity and structure of benthic (1989) have estimated that hundreds of gray communities in the axes of canyons like those off whales sink to the seafloor annually within an of Monterey, California. A long-term program has area of 8 Â 105 km2 that includes Monterey Bay, been established to monitor the fate of this large California. If so, organic enrichment due to whale organic input to the benthic community. falls may play a significant role in regulating animal abundance and diversity in deep regions like Monterey Canyon. This includes enrichment 2. Materials and methods of typical deep-sea animals such as holothuroids and ophiuroids, the occurrence of opportunistic Canyon exploration, sample collection, and polychaetes and crustaceans, as well as specific videosurveillance were accomplished using the whale fall specialists. remotely operated vehicle (ROV) Tiburon, devel- Observations of natural and implanted whale oped at the Monterey Bay Aquarium Research falls along the California margin suggests that Institute. Tiburon is equipped with HMI (metallo- community succession typically progresses gen metal halide arc lamp) lighting, a suite of through three stages (Smith and Baco, 2003). (1) sensors to measure conductivity (salinity), tem- The mobile scavenger stage, comprised of about 40 perature, depth, and oxygen (CTDO—approxi- species (mostly fish and crustaceans), removes mately 2 m above the seafloor), and imaging sonar. more than 90% of the soft tissue, usually within The camera from which all video recordings were 4 months after arrival on the seafloor depending made was a high-resolution color digital camera on the size of the carcass. (2) The enrichment- (three chip Panasonic WVE550). Digital still opportunistic stage, comprised of about 20 species images were taken from the Tiburon using a (mostly polychaetes and crustaceans), may last as Coolpix 990 camera (Nikon) and a SB28 strobe long as 2 years. Finally, (3) the sulfophilic stage, light (Insight Tritech). Abundance estimates for which relies on the coupling between decomposi- Scotoplanes sp. and bacterial mat coverage areas tion of bone lipids and seawater sulfate reduction were determined via seabed photographs taken and is dominated by microbial mats and more with the Tiburon using a Coolpix camera. than 100 invertebrate species (including sulfide- Approximately 16 h of video from ROV bottom- tolerant and sulfide-dependent molluscs), may last time was recorded, annotated, and analyzed from for years and even decades depending on the size dives T391 (February 6, 2002), T406 (March 10, of the whale. 2002), and T486 (October 9, 2002). Occurrences of This paper describes a whale fall community all discernible animals were entered intoa search- found at 2891 m depth in the axis of Monterey able database with corresponding environmental Canyon, California. It is one of the deepest whale data from the CTDO sensors and observational falls discovered to date, and, thus, provides a (time, position) data. An acoustic homer beacon unique opportunity to study localized effects of was placed near the whale skull tofacilitate organic enrichment at depths that exclude many of relocation and subsequent monitoring of the site. the large mobile scavengers found at shallower Sediment push cores, bone samples, and animal whale falls. We describe changes, including loss of specimens were collected with the manipulator soft tissue from the carcass, development of large arm of the Tiburon. On board the support vessel, microbial mats, and differences in polychaete tissue samples were dissected from specimens and ARTICLE IN PRESS S.K. Goffredi et al. / Deep-Sea Research I 51 (2004) 1295–1306 1297 either frozen at À70C or preserved in 95% the 18S region (Halanych et al., 1998). Sequences ethanol, 10% formalin, or 2% cacodylate-buffered were aligned and proofread using Sequencher v 4.1 glutaraldehyde. Animal identifications were ac- (Gene Codes Corp.). All phylogenetic compar- complished via either morphological or molecular isons were performed with PAUPÃ4.0b10 (Swof- characterizations. Morphological identifications, ford, 1998). Sequence similarities (based on from both collections and video only, were made Kimura 2 parameter distances; Kimura, 1980) directly by the authors or through communica- and supporting bootstrap values (based on max- tions with taxonomic experts including G. Rouse imum parsimony and NJ analyses) are reported in (South Australian Museum), E. Southward (Mar- the text. ine Biological Association of the UK), J. Drazen (Monterey Bay Aquarium Research Institute), and the staff of the Monterey Bay Aquarium Research 3. Results Institute video annotation lab. Voucher specimens of putative new species will be held at the 3.1. Site description Monterey Bay Aquarium Research Institute pend- ing formal taxonomic descriptions. The whale fall described here was discovered Identification of the whale was determined via during Tiburon dive T391 on February 6, 2002. baleen structure and DNA sequencing of the The skeleton was situated at 2891 m depth in the mitochondrial control region. Preliminary classifi- axis of Monterey Canyon at 3636.80N/ cation of the two dominant polychaetes (annelid A 12226.00W (star; Fig. 1). The surrounding floor (siboglinid) and annelid B (spionid)) was based on of the canyon was composed of fine-grained clastic ribosomal 18S DNA sequences. The DNEASY kit sediments. Trash (mostly plastic bags and trays), (Qiagen) was used to extract total DNA from coastal macroalgae, and sea grass were observed frozen or alcohol-preserved tissues, following the near the fall, suggesting that this is an area of manufacturer’s protocol. For the whale tissues, a active sediment movement and deposition. Bottom 320 base pair fragment of the whale mitochondrial water oxygen concentrations near the fall mea- control region was amplified with primers TRO sured 97–110 mmol lÀ1, at a depth that is far below 0 0 (5 -CCT CCC TAA GAC TCA AGG AAG-3 ) the O2 minimum zone in that area (700–800 m and D (50-CCT GAA GTA AGA ACC AGA TG- depth). Bottom temperatures were between 1.65C 30)(Arnason et al., 1993) using Taq polymerase and 1.69C near the whale on all three dives. A (Promega) and the following polymerase chain limited number of bone, sediment, and animal reaction (PCR) protocol: initial denaturation at samples were collected on all three dives, primarily 94C for 5 min; 35 cycles of (94C for1 min, 55C tominimize disturbance forsubsequent time for1 min, and 72C for 2 min); and a final course observations.
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