Deep-Sea Research I 57 (2010) 1573–1584 Contents lists available at ScienceDirect Deep-Sea Research I journal homepage: www.elsevier.com/locate/dsri Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA Lonny Lundsten a,n, Kyra L. Schlining a, Kaitlin Frasier b, Shannon B. Johnson a, Linda A. Kuhnz a, Julio B.J. Harvey a, Gillian Clague a, Robert C. Vrijenhoek a a Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039, USA b Scripps Institution of Oceanography, 8602 La Jolla Shores Drive, La Jolla, CA 92037, USA article info abstract Article history: Dead whale carcasses that sink to the deep seafloor introduce a massive pulse of energy capable of Received 16 April 2010 hosting dynamic communities of organisms in an otherwise food-limited environment. Through long- Received in revised form term observations of one natural and five implanted whale carcasses in Monterey Canyon, CA, this 17 September 2010 study suggests that: (1) depth and related physical conditions play a crucial role in species composition; Accepted 21 September 2010 (2) the majority of species in these communities are background deep-sea taxa; and (3) carcass Available online 8 October 2010 degradation occurs sub-decadally. Remotely operated vehicles (ROVs) equipped with studio quality Keywords: video cameras were used to survey whales during 0.8 to seven year periods, depending on the carcass. Osedax All organisms were identified to the lowest possible taxon. Community differences among whale-falls Deep-sea seemed to be most strongly related to depth and water temperature. The communities changed Succession significantly from initial establishment shortly after a carcass’ arrival at the seafloor through multiple Whale-fall years of steady degradation. The majority of species found at the whale-falls were background taxa commonly seen in Monterey Bay. While populations of species characterized as bone specialists, seep restricted, and of unknown habitat affinities were also observed, sometimes in great abundance, they contributed minimally to overall species richness. All whale carcasses, shallow and deep, exhibited sub- decadal degradation and a time-series of mosaic images at the deepest whale site illustrates the rapidity at which the carcasses degrade. & 2010 Elsevier Ltd. All rights reserved. 1. Introduction Smith and Baco, 2003; Schuller et al., 2004). These authors also suggested that vent and seep animals may use whale carcasses Whale-falls, carcasses of dead whales that sink to the seafloor, as ‘‘stepping stones,’’ bridging spatial gaps between ephemeral host thriving and dynamic communities of organisms. Each whale seep and vent habitats (Bennett et al., 1994; Baco and Smith, arriving at the seafloor represents a massive influx of energy to an 2003; Smith and Baco, 2003; Smith, 2006). Fujiwara et al. otherwise food-limited environment. Whale tissues and lipid-rich (2007) reported no overlap between whale-fall inhabitants and bones (over 60% lipids by weight) provide an energetic pulse to species found at nearby seeps and vents off the coast of Japan. the region immediately surrounding the fall (Schuller et al., 2004). Lundsten et al. (2010) report Lamellibrachia sp. living near a A 40-ton whale carcass may carry 2000–3000 kg of lipids in its whale-fall off Vancouver Island, British Columbia. Several studies skeleton alone, and represent 100–200 times the typical levels of have suggested the existence of whale-fall specialists, organisms organic carbon sinking annually to a hectare of seafloor (Smith specifically adapted to the conditions at whale carcasses (Smith et al., 2002; Smith and Baco, 2003; Smith, 2006). and Baco, 2003; Smith, 2006). Whale-fall specialists would Studies of natural and implanted whale-falls have spawned seemingly include species of the unique siboglinid genus, various theories on the structure and development of the Osedax (Rouse et al., 2004; Glover et al., 2005; Fujikura et al., communities that colonize these enriched habitats. Early research 2006; Rouse et al., 2009; Vrijenhoek et al., 2009); however, the showed the presence of hydrothermal vent and cold seep exclusive dependence upon whale bone for this genus has been organisms, although these taxa represented only a small percen- the subject of recent debate (Jones et al., 2008; Glover et al., 2008; tage of species richness (Bennett et al., 1994; Deming et al., 1997; Vrijenhoek et al., 2008). Depth has also been posited to play a Feldman et al., 1998; Smith et al., 2002; Baco and Smith, 2003; significant role in determining the overall species richness of whale-fall faunas (Goffredi et al., 2004; Fujiwara et al., 2007; Braby et al., 2007). n Corresponding author. Tel.: +1 831 775 1762; fax: +1 831 775 1620. Bennett et al. (1994) proposed a four-stage model of E-mail address: [email protected] (L. Lundsten). succession at whale-falls which was later fully developed by 0967-0637/$ - see front matter & 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2010.09.003 1574 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 Smith and Baco (2003) including: (1) a ‘‘necrophage’’ stage, where and since that study, two additional sites and three years of scavengers remove flesh from the whale carcass; (2) an observations have been included. ‘‘enrichment-opportunist’’ stage, characterized by aggregations of polychaetes and crustaceans attracted to the enriched sediments; (3) a ‘‘sulphophilic’’ stage, composed of a 2. Methods chemoautotrophic bacterial assemblage and organisms fed by these chemoautotrophs; and (4) a ‘‘reef’’ stage, inhabited by Six whale-fall sites form the basis of this study. The natural suspension feeders exploiting the remaining nutrient-depleted carcass was discovered at a relatively early stage of degradation; hard substrate. Observations on whale-fall succession patterns however, the exact date of its arrival at the seafloor is unknown suggested that carcasses persist for decades, depending on the but estimated to be six months before discovery (Goffredi et al., whale age and size (Smith et al., 2002; Smith and Baco, 2003; 2004; Schuller et al., 2004). The five implanted carcasses were Fujiwara et al., 2007). However, data from more recent studies whales that stranded along neighboring coastlines and were indicate that some of these stages may not occur at all whale-falls subsequently towed out to sea and sunk to depth using iron train- and that where stages do occur, they most likely overlap (Smith wheel anchors. All sites are located within the Monterey Canyon et al., 2002; Smith and Baco, 2003; Goffredi et al., 2004; Smith, (Fig. 1). Depths range from 382 to 2893 m (Table 1), and span the 2006; Braby et al., 2007). It also appears that succession can oxygen minimum zone (OMZ, defined by dissolved oxygen levels advance rapidly and the ultimate decomposition of the whale r0.5 ppm; Levin, 2003). Distances from bathymetric features carcass may be quick, particularly for skeletons of sub-adult such as seeps and ridges differ among sites, as do other whales which have less calcified bones and smaller lipid environmental factors including disturbance, currents, and reservoirs (Smith et al., 2002; Smith and Baco, 2003; Fujiwara carcass orientation. Additionally, the whales themselves vary in et al., 2007; Braby et al., 2007). Succession of the microbial species, age, and body size. Consequently, these sites are not communities in sediments underlying whale-falls has also been treated as replicates, but as individual instances of whale-fall demonstrated and is likely due to changes in the decompositional community development. nature of the carcass over time (Goffredi et al., 2008; Treude et al., All whale-falls were surveyed using the Monterey Bay 2009; Goffredi and Orphan, 2010). Aquarium Research Institute’s (MBARI) ROVs Tiburon, Ventana, The present analyses of one natural and five implanted whale or Doc Ricketts. These ROVs are equipped with sensors that record carcasses in Monterey Canyon, CA, allowed us to demonstrate and log environmental parameters such as geographic location, that: (1) the variation in community structure is largely attributed depth, salinity, oxygen concentration, pressure, and temperature. to depth; (2) the majority of species found at whale-falls are They have a variety of sampling capabilities and multiple video typical background deep-sea taxa; and (3) whale carcasses can cameras. Studio-quality video cameras were used to survey the degrade rapidly (e.g., sub-decadally). Because these whale-fall whale-falls and these observations were recorded to digital sites span a variety of depths and physical conditions within a videotape. Video recordings were annotated using MBARI’s Video small geographical region, they provide a unique opportunity to Annotation and Reference System (VARS, Schlining and Jacobsen compare community composition and development. An earlier Stout, 2006). Within VARS, all benthic and demersal organisms subset of the present data was published by Braby et al. (2007) were identified to the lowest possible taxon. For animals that 122°30'W 122°20'W 122°10'W 122°0'W 121°50'W 121°40'W 37°0'N 37°0'N Whale Fall Locations 382a 382p 633 36°50'N 1018 36°50'N 1820 2893 36°40'N 36°40'N 36°30'N 36°30'N 010205 Kilometers Area of Detail 122°30'W 122°20'W 122°10'W 122°0'W 121°50'W 121°40'W Fig. 1. Map of the Monterey Bay area whale study sites. The name of each whale corresponds to the depth (in m) at which it is geographically located. L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 1575 Table 1 Whale-fall characteristics by site, adapted from Braby et al. (2007). Whale site Whale 382p Whale 382a Whale 633 Whale 1018 Whale 1820 Whale 2893 Depth (m) 382 382 633 1018 1820 2893 Latitude 36.790N 36.790 N 36.802 N 36.772 N 36.708 N 36.613 N Longitude À121.887 W À121.887 W À121.994 W À122.083 W À122.105 W À122.434 W Implanted/Natural Implanted Implanted Implanted Implanted Implanted Natural Carcass length (m) 6 8 10 17 10 10 Whale species Gray Gray Gray Blue Gray Gray Avg.