Time-Series Analysis of Six Whale-Fall Communities in Monterey Canyon, California, USA

Deep-Sea Research I 57 (2010) 1573–1584

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Deep-Sea Research I

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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

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 121.887 W 121.887 W 121.994 W 122.083 W 122.105 W 122.434 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. salinity (ppm) 34.05 34.18 34.24 34.44 34.42 34.53 Avg. temperature (1C) 7.15 7.11 5.52 3.86 2.30 1.67

Avg. O2 (ml/L) 0.992 0.951 0.568 0.476 1.423 2.426 Deployment date 7 Feb., 2007 10 April, 2005 11 April, 2007 5 Oct., 2004 20 March, 2006 Unknown First monitored 4 June, 2007 5 May, 2005 17 Aug., 2007 10 Dec., 2004 23 May, 2006 6 Feb., 2002 Number of visits 3 13 5 16 6 15 Cumulative species richness (approx)a 36 66 57 68 72 90 Months at bottom 10 28 27 53 36 85

a Underestimates species richness, because some identifications are not to species level. were unknown to the authors, voucher specimens were collected the ROV oriented perpendicular to the whale carcass along a using the ROV manipulator arm, suction sampler, and push cores. parallel path using obliquely mounted video and still image For unknown species that were morphologically distinct, but not cameras. Images were gathered such that each had 50% overlap sampled, and therefore not identified to species level, a ‘tag’ name with the next image in line, and stitched and blended using was applied within the VARS database (e.g. ‘Hesionidae sp. 1’). For Photo-Mosaic in Matlab. some taxa, more than one species were identified from voucher specimens but species were indistinguishable in video. For these animals, a tag name was applied (e.g. ‘Amphipoda spp.’) and they were treated as a single ecological unit in analyses. ROV surveys 3. Results varied in length and detail, depending upon the mission, surface weather, and seafloor conditions, but aimed to include a complete 3.1. Physical characteristics video survey along both sides as well as the center of the carcass. Under optimal condition (lighting, angle, suspended particulate), The physical data revealed differences in water column charac- organisms down to 0.5 cm could be resolved using the ROV’s teristics among sites (Table 1). Salinity was similar at all sites, high definition video camera. Taxa presence/absence lists were increasing slightly from 34.05 to 34.53 ppm with the increase in compiled for each ROV dive at each whale-fall and these taxa depth. Temperature decreased from 7.15 1C at the shallowest presence/absence list were considered one sample and used for sites, to 1.67 1C at the deepest. Data also revealed the presence of further analysis. This method is appropriate for megafauna, but an oxygen minimum zone (OMZ), particularly at whales 633 and 1 cannot be used to assess micro- and infauna. Due to these 1018. O2 concentrations reached a low of 0.476 ml L at whale- 1 sampling capability limitations, many of the species captured in 1018 and a maximum of 2.426 ml L at whale-2893. previous whale-fall studies (i.e., macrofaunal polychaetes) are not represented in this work. Samples-based species accumulation curves were calculated 3.2. Community similarity and diversity from presence/absence data using ESTIMATES(Colwell, 2009). The PRIMER software package (v6, Clarke and Gorley, 2001) was used to Samples-based species accumulation curves (Fig. 2A) showed calculate the maximum potential value of Shannon Diversity, similarity (i.e., similar trajectories) between whale-fall commu-

Hmax (i.e., with perfect evenness) and these were compared using nities. None of the curves appears to have reached asymptote. analysis of variance (ANOVA). PRIMER was also used for the Analysis of variance of Hmax (Appendix G) at each whale show a following analyses on faunal composition: multidimensional significant difference in diversity between sites (F(5, 51)¼ scaling (MDS) plots and principal component analysis (PCA). For 9.514, p¼ o0.001; Fig. 2B). MDS plots, similarity matrices of Bray–Curtis coefficients were An MDS plot of the Bray–Curtis similarities between samples constructed. A combination of similarity matrices and Euclidian (Fig. 3A) produced three major groupings with a 2D stress value of distances for normalized temperature, depth, and oxygen con- 0.17. The shallower sites (whales 382a, 382p, and 633) were centration data from each whale were used for PCA. pooled, showing resemblance of 25%, excluding one outlier Taxa were classified by habitat affinity including background from whale-382a. The intermediate depth site, (whale-1018), was fauna, bone specialist, vent specialist, and unknown fauna in an somewhat segregated, but was more closely related to the three effort to determine the relative contribution of each category to shallow sites than the deeper sites. The deepest sites (whales total species richness. Here we define background fauna as 1820 and 2893) were also similar to one another (25%), but organisms that have been observed and catalogued using MBARI’s showed within site similarity of 40%. VARS database from other habitats where MBARI has conducted PCA analysis illustrated the relationship among samples and research. The VARS database contains more than 4,000,000 three environmental factors analyzed (temperature, depth, and observations. oxygen concentration, Fig. 3B). Based on this analysis, the factor Still image mosaics were created using Photo-Mosaic (Pizarro with the greatest effect on community structure is temperature, and Singh, 2003; Singh et al., 2004) and used to visualize changes which co-varies with depth. Axis ‘‘PC1,’’ most closely tied to in the whale carcasses over time. Mosaics were created using HD temperature and depth, accounts for 86.7% of variation among video frame grabs (1920 1080) or Nikon Coolpix 990 digital still samples. An additional 13.1% is accounted for by axis ‘‘PC2,’’ images (2048 1536). Images were collected by carefully ‘‘flying’’ which is correlated with O2 concentration. 1576 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584

55 Species

45 Whale 382a Whale 382p Whale 633 35 Whale 1018 Whale 1820 Whale 2893 25

15 0 2 4 6 8 10 12 14 16 Samples

4.00 Whale 382a Whale 382p Whale 633 Whale 1018 Whale 1820 Whale 2893 3.50 max H

3.00

2.50

Fig. 2. (A) Samples-based species accumulation curves using presence–absence data and calculated with EstimateS. (B) Results of ANOVA comparing mean Hmax between whale-falls. The dashed line represents the overall mean Hmax for all whale-falls, diamonds represents Hmax at each individual whale-fall; lines in each diamond correspond to the mean and upper and lower 95% conﬁdence intervals.

3.3. Habitat affinity was observed at the 2893 m site and dense populations of a bacterial mat-grazing dorvilleid species were observed at the 1820 m site. Species habitat affinity showed that at all sites and times species richness was predominantly made up from background deep-sea fauna, with few exceptions (Fig. 4; 1820 M-2, 2893 3.4. Community characterizations M-85). Because many new species have been or are being described from specimens collected during these surveys, habitat affinities for 3.4.1. Whale-382a some species are unknown; however, many of these organisms This was an 8-m long gray whale implanted April 10, 2005 may not be restricted to whale-falls. Therefore, this analysis is most at a depth of 382 m. High disturbance and turbidity due to likely conservative. Bone specialists were abundant and included recurrent sediment flows are common at this site (Table 1). The many (n¼16) species of Osedax as well as two bone-eating carcass was surveyed 13 times during 28 months. It is the only provannid gastropods (Johnson et al., in press). Seep associated one of the three shallowest sites visited earlier than four months species were observed infrequently at all sites. A vesicomyid clam post-deployment, allowing the flesh-removal stage to be directly L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 1577

Similarity 25 40

Whale 382a 382p 633 1018 1820 2893

Depth 0 PC2

O2 Temp

-1 -3 -2 -1 0 1 2 PC1

Fig. 3. (A) MDS plot of Bray–Curtis similarity indices using presence/absence data show clustering of samples by whale site, indicating depth related similarity. Stress is acceptable at 0.17. (B) Principal component analysis (PCA) relating three measured environmental factors on samples collected at each site. PC1 correlates most strongly with depth and temperature.

observed. Initial scavengers (at one month post-deployment) were post-deployment. Amphipods and the sablefish, Anoplopoma thick swarms of amphipods in higher densities than observed at fimbria, dominated initially. By 10 months, the site shifted to a the whale-382p site, as well as an abundance of hagfish (Eptatretus community composed mainly of the siboglinid polychaete, Osedax stoutii), and a sleeper shark (Somniosis pacificus). At three months ‘yellow collar’ (Vrijenhoek et al., 2009), growing on exposed post-deployment, all flesh was gone and the numbers of bone surfaces. Three species of anthozoans and an echinoid, amphipods and hagfish were greatly reduced. Over the next two Allocentrotus fragilis, were observed on the bones as were two years, diversity generally increased to a community predominantly species of decapods. A total of 36 taxa were observed. composed of bone-eating Osedax worms, anemones, the fragile urchin, Allocentrotus fragilis (Fig. 5A&B),andRathbunaster californicus (Fig. 5B). A surge of decapods and rockfish occurred 3.4.3. Whale-633 during months 19 and 20. A total of 66 different taxa were This 10-m long gray whale was implanted during April 2007 at observed. a depth of 633 m in an area of relatively low oxygen concentration (mean¼0.568 ml/L). All flesh had been removed by the first monitoring visit at four months post-deployment. We visited the 3.4.2. Whale-382p site five times during 26 months. Initial observation revealed a This 6-m long gray whale implanted during February 2007, at a wider variety of taxa than seen at the shallower sites. At four depth of 382 m just 50 m from whale-382a, was the most recent months post-deployment, extremely dense populations of amphi- of the Monterey whale-falls. It was also the smallest carcass, pods (Fig. 5C) were present along with nine taxa of bony fishes, apparently from a stillborn or recently killed calf. We conducted including Anoplopoma fimbria (present in greater numbers than at three surveys over a 10-month period. All flesh on the carcass the shallower whales), Merluccius productus,andSebastes diploproa. was gone when the site was first monitored at four months Hagfishes were present, although in low numbers, and provannid 1578 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584

382a M-1 Background fauna 382a M-3 Bone specialists 382a M-4 Seep fauna 382p M-4 Unknown 382p M-6 382a M-7 382a M-9 382a M-10 382p M-10 382a M-13 382a M-15 382a M-17 382a M-19 382a M-26 382a M-26 382a M-28

633 M-4 633 M-5 633 M-8 633 M-13 633 M-26

1018 M-2 1018 M-3 1018 M-4 1018 M-9 1018 M-13 1018 M-15 1018 M-17 1018 M-19 1018 M-21 1018 M-23 1018 M-24 1018 M-27 1018 M-34 1018 M-39 Whale carcass, Months Deployed (M-x) 1018 M-53

1820 M-2 1820 M-7 1820 M-10 1820 M-17 1820 M-21 1820 M-36

2893 M-0 2893 M-1 2893 M-8 2893 M-18 2893 M-23 2893 M-27 2893 M-31 2893 M-34 2893 M-35 2893 M-45 2893 M-47 2893 M-51 2893 M-59 2893 M-70 2893 M-85

0 5 10 15 20 25 30 35 40 45 50 Number of taxa

Fig. 4. Whale-fall taxa categorized by habitat affinity (bone, seep-wood, unknown, and background) plotted for each dive at each whale-fall on the x-axis, y-axis is number of species (n). gastropods were common. In subsequent visits, the fish species actiniarians, asteroids, and holothurians. An increase in gastropods shifted to more sedentary families (primarily Zoarcidae), and a was also recorded. Osedax showed a species shift with O. ‘orange variety of sessile and mobile invertebrates appeared, including collar’ being present initially, but replaced five months after L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 1579

Fig. 5. Megafauna at whale-falls. The number in parentheses for each image refers to the ROV platform and dive number, i.e. T993 would be ROV Tiburon dive 993; the second number refers to months on bottom or months since initial visit for whale-2893. (A) Whale-382a: Fragile urchin, Allocentrotus fragilis (T993; 9). (B) Whale-382a: Fragile urchins, Allocentrotus fragilis, Rathbunaster californicus and drift kelp on whale bones (T933; 13). (C) Whale-633: Swarms of pink and yellow amphipods (T1120; 4). (D) Whale-1018: Chionoecetes tanneri feeding on whale tissue and dense Osedax sp. on whale bone. (T776; 3). (E) Whale-1018: Dover sole, Microstomus pacificus (T916; 13). (F) Whale-1820: Blob sculpin, Psychrolutes phrictus and snubnose eelpout, Pachycara bulbiceps (T990; 2). (G) Whale-1820: Dense Osedax sp. on whale vertebrae, dense ophiuroids, and Pannychia moseleyi. (T1048; 7). (H) Whale-2893: New species of Osedax sp. and chaetopterid worms in sediment near whale carcass (T769; 34). (I) Whale- 2893: Galatheid crabs, Munidopsis spp. (T742; 31). (J) Whale-2893: Scotoplanes globosa, bacterial mat, Amage cf. arieticornuta, and a new species of Spionidae (T406; 1). (K) Whale-2893: High densities of Scotoplanes globosa and Glyphanostomum sp. (T391; 0). (L) Whale-2893: Anthosactis pearseae, Osedax frankpressi, Munidopsis spp., collected with a piece of whale bone (T742; 31). (M) Whale-2893: Pycnogonid, Colossendeis gigas, feeding upon Liponema brevicornis tentacles (T391; 0). (N) Whale-2893: Liponema brevicornis and lithodid crab (T610; 18). (O) Whale-2893: Hesionid worm, Vrijenhoekia balaenophila, with abundant Osedax frankpressi (T610; 18). 1580 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 deployment by dense populations of O. roseus. Dense populations 3.4.6. Whale-2893 of marine leaches (Hirudinea) were also observed throughout. This naturally occurring carcass was discovered nearly three A total of 57 taxa were observed. years prior to deployment of whale-1018, the first implanted carcass. The exact date of its arrival on the seafloor is unknown, but is estimated as roughly six months prior to discovery, based 3.4.4. Whale-1018 on the amount of flesh remaining and 210Pb/226Ra disequilibria This 17-m long blue whale was implanted during October (Goffredi et al., 2004; Schuller et al., 2004). Most of the flesh 2004 at a depth of 1018 m in an area with the lowest oxygen except for intestines and dense connective tissues were removed concentration for this study (mean¼0.476 ml/L). The head of this when it was found, so the earliest stages of degradation are not carcass had been removed for anatomical studies prior to our reflected in the data set. The intestinal remains disappeared eight deployment. The carcass lies in a horseshoe-shaped orientation, months later. Species richness was elevated from the outset with and is located near a steep submarine canyon wall. Flesh was exceptionally high annelid diversity and abundance. Initial taxa still present at three month post-deployment. Flesh consumers included Osedax rubiplumis, O. frankpressi, and O. ‘spiral’ (Fig. 5H), included hagfish, amphipods, and tanner crabs, Chionoecetes (Table 2), ampharetids (Glymphanostomum sp.), Phyllochaetopterus tanneri (Fig. 5D). All three taxa remained present although in sp., and dense populations of a new species of spionid. Decapods, slowly decreasing numbers until approximately 15 months post- including two species of Munidopsis (Fig. 5I) and the lithodid crab, deployment. These species were joined by O. roseus and relatively Paralomis multispina, were also abundant. A thick bacterial mat low numbers of amphipods by month three, when bone surfaces was observed near the whale’s abdominal region (Fig. 5J). Dense had become exposed. A dense bacterial mat, not observed at the aggregations of the holothurian, Scotoplanes globosa (Fig. 5K), shallower sites, developed on the sediment inside the U-shape. were noted until eight months post-discovery. This site exhibited The total area covered by the bacterial mat peaked between the highest overall species richness, with 90 taxa observed over months three and 19. This site exhibited its most taxa-diverse the course of 15 visits during 85 months. period between months nine and 19, eventually leading to a At 18 months post-discovery, a variety of anthozoans low-abundance community of rockfish, gastropods (Neptunea appeared, succeeded by an increase in echinoderms after 45 amianta and three species of provannid gastropods), and various months. Gastropod richness also increased, consisting primarily of decapods. Osedax was represented throughout, shifting from three species of abundant provannid gastropods. Rubyspira, abundant O. roseus to lower numbers of Osedax ‘orange collar’ Paralomis multispina, and Munidopsis spp. survived for numerous and Osedax ‘white collar’ that are currently undescribed. Fifteen generations, demonstrated by the accumulation of carcasses and species of bony fish (i.e., Microstomus pacificus, Fig. 5E), nine empty shells over time. Many observed taxa were not noted at the species of malacostracans, and six distinct anthozoans were other Monterey whale-falls, including a newly described ane- observed here, but none were present in high numbers. Sixteen mone, Anthosactis pearseae (Fig. 5L; Daly and Gusmao,~ 2007), visits were made over 53 months, and a total of 68 distinct taxa pycnogonids, Rubyspira spp., sea pens and several species of were observed. Munidopsis. Two species of pycnogonids, Colossendeis gigas (Fig. 5M) and C. japonica, were observed at this site feeding on Liponema brevicornis (Fig. 5M and N) anemones that had collected 3.4.5. Whale-1820 around the whale bones as well as A. pearseae living attached to This was a 10-m long gray whale implanted during March the bones (Braby et al., 2009). Fish diversity remained low 2006 at a depth of 1820 m. The lower jawbones, tongue and throughout the duration of this study. baleen were missing, probably due to predation by orcas (Orcinus The carcass itself was highly degraded after two years with the orca), when the carcass was beached. Flesh was still abundant exception of the baleen, which remained relatively intact. The when first monitored two months post-deployment. During this skull was the slowest to degrade and the most species rich region survey, dorvilleid polychaetes, lithodid crabs (Paralomis verrilli) of the whale-fall. When monitored 70 months post-discovery, and rattail fish (Coryphaenoides acrolepis) were abundant. Blob only a small, highly degraded remnant of the skull remained. sculpin, Psychrolutes phrictus and snubnose eelpout, Pachycara At this time, the site was still colonized by a diverse group of bulbiceps were also observed (Fig. 5F). Rattails were seen on all polychaetes (Fig. 5O), decapods, echinoderms, holothurians, and subsequent surveys. Bathysiphon forams, and brittle stars Osedax spp. that were living on the remnant bone fragments. (Ophiuroidea; Fig. 5G) were also abundant and remained Photo-mosaics—High-resolution photo-mosaic images of common throughout all surveys. We saw no flesh by the second whale-2893 illustrate the rapidity of whale carcass degradation visit to this site, five months post-deployment, and the exposed (Fig. 6). A relatively intact skeleton and flesh is present at bone surfaces were heavily colonized by Osedax rubiplumus discovery (Fig. 6A); 34 months later (2.5 years) the carcass is (Fig. 5G). A peak in species richness occurred 21 months post- already highly degraded with the bones becoming partially buried deployment, when 29 taxa were observed. Annelids were diverse in sediment (Fig. 6B). By 45 months, the carcass is almost (12 taxa) and abundant, and decapod diversity increased unrecognizable as a whale (Fig. 6C) and by 70 months post- markedly. A variety of bony fish frequently visited the site, discovery (almost six years) there are only a few remnants of bone although in low numbers. C. acrolepis was observed feeding on and baleen (Fig. 6D). At 82 months, very little evidence of the flesh as well as chunks of bone laden with Osedax, which soften sunken whale remains (Fig. 6E). Still images from the skull region and disintegrate the bone. The ovisacs of the bone worms are full of each whale-fall show similar trajectories of degradation at the of lecithotrophic eggs (Rouse et al., 2009), a rich energy source for time of the last survey for each site (Fig. 7). these scavengers. Overall, limited community shifts were observed during the sampling period, which has been visited relatively few times since deployment. Notable changes include 4. Discussion the appearance of bacterial mat 10 months post-deployment, and large accumulations of organic and inorganic debris, including This study reveals that time and depth related faunal changes plastic shopping bags, sea grasses, and kelp that collected around work together to facilitate the decomposition of whale carcasses on the carcass. We monitored the site six times during 36 months the seafloor. On arrival at the seafloor, carcasses host a relatively post-deployment. A total of 72 taxa were identified. low-diversity community of mobile scavengers. Through time, L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 1581

Table 2 Relative abundance of ‘bone specialist’ Osedax spp. and two provannid gastopods in 6 month bins. Rare (+), moderately abundant (++), and dense (+++) populations were observed in ROV video footage.

Months since deployment 0–6 7–12 13–18 19–24 25–36 37–42 43–48 49–54 55–60 67+

Whale-382a Osedax ‘yellow collar’ + + Osedax ‘orange collar’ + ++ + +

Whale-382p Osedax ‘yellow collar’ + +

Whale-633 Osedax roseus +++++ + Osedax ‘orange collar’ + + Osedax ‘yellow patch’ ++ ++ +

Whale-1018 Osedax roseus +++ ++ ++ ++ ++ ++ ++ Osedax ‘orange collar’ + + + + Osedax ‘yellow patch’ + + + + Osedax ‘white collar’ + Osedax ‘nude palp C’ + + + + Osedax ‘nude palp D’ + + + + Osedax ‘nude palp E’ + + + +

Whale-1820 Osedax rubiplumus + ++ + ++ ++ + Osedax frankpressi ++ ++ + Osedax roseus ++ + + Osedax ‘green palp’ + + + Osedax ‘nude palp A’ + + + + Osedax ‘nude palp D’ + + + + Rubyspira osteovora +

Whale-2898 Osedax rubiplumus ++ + ++ Osedax frankpressi + + ++ ++ ++ ++ ++ ++ + Osedax ‘spiral’ ++++ Osedax ‘nude palp B’ ++ Osedax ‘nude palp F’ + Rubyspira osteovora + +++ +++ +++ +++ +++ Rubyspira goffrediae +++

diversity increases, however, most of the increases in species factors that typically decrease with increasing depth. Frequent richness come from background taxa that are merely exploiting the disturbance is evident at whales 382a, 382p, and 633, which are abundant nutrients provided by the whale carcass. located near the head of the Monterey Canyon, an area associated In addition to temporal changes, the whale-fall communities with high sediment deposition rates and frequent turbidity flows also differed according to water depth. We hypothesize that the (Paull et al., 2003, 2005). Species richness in this study increased differences among these whale-fall communities were con- with depth, as observed by Braby et al. (2007), correlating with an strained by the physical conditions at each depth as evidenced apparent decrease in overall disturbance at the deeper sites. by ANOVA of Hmax (Fig. 2B), MDS, and PCA (Fig. 3A, B). The Most of the taxa observed at these whale-falls are common correlations of temperature and oxygen concentrations with deep-sea inhabitants of Monterey Canyon, nearby seamounts, and depth appear to be primary factors and are well known to affect the continental slope (Figs. 4 and 5). We did not assess biomass species presence and distribution in other benthic environments or species abundance in this survey, but anecdotal information (Levin and Gage, 1998; Nilsson and Rosenberg, 2000). Oxygen about the relative abundance of many species were noted here minimum zones, characterized by 40.5 ml/L of O2 tend to be (Table 2; Appendices A–F) and in previous studies (Goffredi et al., associated with lower species diversity in the deep sea (Levin and 2004; Braby et al., 2007). Some of the most abundant organisms Atkinson, 2003), but it remains unclear whether these trends appeared to be specialists, including the bone-eating Osedax worms can be extended to whale-falls implanted in Monterey Canyon and Rubyspira gastropods (Johnson et al., in preparation). Some (i.e., whales 633 and 1018; Braby et al., 2007). The longevity of the undescribed species (i.e., Spionidae at whale-2893) with unknown southern California whale carcasses reviewed in Smith (2006) habitat affinities were also abundant. Many of the flesh-removing may be due primarily to those carcasses being located within an fishes were abundant, particularly hagfish, at depths shallower anoxic basin. Recent studies have shown that deep-sea canyon than 1018 m. Several species of amphipods were also abundant, systems may be areas with elevated diversity at both large and although they could not be identified below the order level in small spatial scales due to a variety of co-occurring processes video. Initial morphological assessments from collected amphipod (Vetter et al., 2010; De Leo et al., 2010; McClain and Barry, 2010). specimens suggest the presence of a diverse amphipod assemblage Vetter and Dayton (1998) link species diversity to reduced with members of the orders and families Lysianassoidea, Melito- disturbance by currents, sedimentation, and organic enrichment, idea, Alicellidae, and Ischyroceridae. Preliminary analyses of DNA 1582 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584

Fig. 6. Still image mosaics of whale-2893 showing decomposition of the carcass through time: (A) T391, 2/6/2002, initial observation; (B) T769, 12/1/2004, 34 months since initial visit (MSIV); (C) T917, 11/8/05, 45 MSIV; (D) T1162, 12/20/2007, 70 MSIV; E: DR-10, 3/11/2009, 85 MSIV. sequence data from the nuclear coding gene Histone-3 (H3) sulfide (Goffredi et al., 2008). Bone specialists also increased at suggests that the lyssianassids are restricted to the shallower sites these sites during later stages of sampling (Fig. 4). At whale-2893, (whales 382a/p and 633). Gammarideans, however, were found dense mats of methane-oxidizing bacteria were initially visible throughout the whole depth range of this study. These initial results (Fig. 5J). However, a sulfur-reducing bacterial community was not have prompted a more detailed ecological and taxonomic study of observed and very low levels of sulfide were detected (Goffredi the amphipods which is currently in progress (J. Harvey, MBARI). et al., 2008). The presence of a ‘‘reef stage’’ consisting of suspension We observed rapid (sub-decadal) degradation at both the and filter feeders was not supported. Suspension feeding corals and shallow and the deep sites in contrast to earlier studies which sponges were observed at the deeper whales (i.e., Farrea, suggested that heavily calcified adult whale carcasses may last for Asbestopluma, Bathypathes); however, these organisms appeared many decades. Our analysis agrees with earlier studies which to have drifted down from nearby canyon walls and appeared to be suggested that the poorly calcified bones and relatively small lipid dead or dying. Living mobile (Liponema brevicornis) and sessile reserves of juvenile whales may degrade rapidly (Smith and Baco, (Hormathiidae) suspension feeders were observed in low 2003). Photo-mosaic and individual still images (Figs. 6 and 7) abundance. However, based on the rate of degradation of these visually demonstrate the rapidity at which these Monterey Canyon carcasses, a reef stage will never occur because the bones are so whale-falls degrade. The deeper sites (whales 1018, 1820, and 2893) rapidly broken down. Ultimately, the nutrient-driven opportunist have degraded in a similar fashion and timescale. The shallower sites stage may actually outlast any structurally dependant stage. The (whales 382a, 382p, and 633) have also degraded quickly, but these longest-lasting feature of all the whale-falls was the head, sites are subject to much more disturbance than the deeper sites. characterized by large, lipid-rich bones that were slow to be These carcasses are often partially buried in sediments, re-exposed, colonized by Osedax and took the most time to degrade. Further and partially buried again. The dynamic nature of canyon processes monitoring of all sites may reveal additional changes in community at these shallower sites might obscure the degradation processes, structure; however, it appears highly unlikely that any trace of the e.g., by burying carcasses (Paull et al., 2003; Paull et al., 2005; De Leo whale carcasses will remain even a decade after deployment et al., 2010; McClain and Barry, 2010). (Figs. 6 and 7). Smith and Baco (2003) first demonstrated truncated Evidence of four successional stages is lacking at these whale- and overlapping successional stages, suggesting that the age of falls. There clearly existed a necrophage stage, where flesh was the whale at death and, therefore, the calcification of bone and removed by large (hagfish, sharks) and small (amphipods, crabs, lipid reservoir contained within it, might ultimately control the and polychaetes) carrion feeders. This initial stage was followed by longevity of each stage. a multi-trophic community of mainly ‘‘enrichment/opportunists’’ Much of the motivation for this study derived from our (Smith and Baco, 2003); however, there is a great deal of overlap interests in the extraordinary diversity of Osedax bone worms between these initial stages. Any evidence of a ‘‘sulphophilic’’ stage (Rouse et al., 2004, 2009; Vrijenhoek et al., 2009). Since initial was short-lived at shallower depths, if it took place at all. At the discovery of the genus in 2002 at whale-2893, we have identified 1018 m and 1820 m sites, a ‘‘sulphophilic’’ stage was more evident 15 species of Osedax on the bones deployed in Monterey Canyon. by the presence of a thick bacterial mats and elevated levels of Relative abundance of Osedax species and bone-eating provannid L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584 1583

Fig. 7. Condition of whale carcasses at last time of sampling: (A) whale-2893 at year 7, remainder of skull region highlighted with red circle; (B) whale-1820 at year 3, remainder of skull region highlighted with red circle; (C) whale-1018 at year 4.5, skull was removed before deployment; (D) whale-633 at year 2.2 skull and jaws visible; (E) whale-382a at year 2.4, skull and jaws visible; (F) whale-382p at year 10 months, skull and jaws visible. gastropods (Table 2) revealed clear trends in both temporal change Osedax they may require bacterial symbionts to facilitate bone- and depth distribution. Succession of Osedax species was observed decomposition. A new anemone (Anthosactis pearseae), a hesionid most clearly at whale-2893. Osedax rubiplumus was the first worm polychaete (Vrijenhoekia balaenophila), and three galatheid crabs to occur in high abundance, but it was largely replaced during the (Munidopsis bracteosa, M. albatrossae and M. cascadia) have also next year by O. frankpressi. O. ‘spiral’ appeared later on baleen-laden been described from the 2893 m site (Daly and Gusmao,~ 2007; sediments near the head region. It uses long sinuous roots to devour Jones and Macpherson, 2007; Pleijel et al., 2008). Species shards of bone buried in anaerobic sediments. Early colonization by descriptions are pending for two more species of provannid O. rubiplumus and subsequent recruitment of O. frankpressi also gastropods, several new dorvellids, two additional species of occurred at whale-1820, but O. ‘spiral’ have not been observed Vrijenhoekia, a maldanid, a spionid, a new limpet, a new buccinid there. Instead, we found abundant O. roseus co-occurring with gastropod and a diversity of amphipods (Goffredi et al., 2004; O. rubiplumus at this site. O. roseus occurred abundantly in the early Rouse, Scripps Inst. Oceanogr., La Jolla, CA, pers comm.). Future stages of whale-1018, where successional changes in Osedax species studies will include new species descriptions, life history studies, were also evident. Osedax species diversity appears to be higher at and attempts to reveal the dispersal mechanisms of the specialized the deeper whale-falls, but the mid-depth whale-1018 is the most organisms, like Osedax and the newly discovered provannids that species-rich, with seven species. Sub-decadal degradation of these depend on these tiny habitat islands. As these sites progress into whale skeletons appears to be largely driven by Osedax,which their final stages of degradation, they will continue to reveal new excavate the lipid-rich bones with proliferative root-like structures insights into life and death on the deep seafloor. that host heterotrophic bacterial endosymbionts (Goffredi et al., 2004; Rouse et al., 2004). In this sense, Osedax should be considered a foundation species that controls whale-fall community structure Acknowledgements and longevity. Two new species of bone-eating provannid gastropods have We are grateful for support from the pilots of the ROVs Tiburon, been described from these whale-falls (Johnson et al., in press). Like Ventana, and Doc Ricketts and the crew of the R/Vs Western Flyer, 1584 L. Lundsten et al. / Deep-Sea Research I 57 (2010) 1573–1584

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