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Deep-Sea Research I 109 (2016) 27–39

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Deep-Sea Research I

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Demographic indicators of change in a deposit-feeding abyssal holothurian community (Station M, 4000 m)

Christine L. Huffard a,n, Linda A. Kuhnz a, Larissa Lemon a,b, Alana D. Sherman a, Kenneth L. Smith Jr.a

a Monterey Bay Aquarium Research Institute, Moss Landing, CA, USA b California State University Monterey Bay, Seaside, CA, USA

article info abstract

Article history: Holothurians are among the most abundant benthic megafauna at abyssal depths, and important con- Received 25 August 2015 sumers and bioturbators of organic carbon on the sea floor. Significant fluctuations in abyssal holothurian Received in revised form density are often attributed to species-specific responses to variable particulate organic carbon flux (food 9 January 2016 supply) stemming from surface ocean events. We report changes in densities of 19 holothurian species at Accepted 9 January 2016 the abyssal monitoring site Station M in the northeast Pacific, recorded during 11 remotely operated Available online 12 January 2016 vehicle surveys between Dec 2006 and Oct 2014. Body size demographics are presented for Abyssocu- Keywords: cumis abyssorum, Synallactidae sp. 1, Paelopatides confundens, Elpidia sp. A, Peniagone gracilis, Peniagone Ecology papillata, Peniagone vitrea, Peniagone sp. A, Peniagone sp. 1, and Scotoplanes globosa. Densities were lower Population biology and species evenness was higher from 2006–2009 compared to 2011–2014. Food supply of freshly- Deep-sea settled phytodetritus was exceptionally high during this latter period. Based on relationships between Echinodermata Spawning aggregation median body length and density, numerous immigration and juvenile recruitment events of multiple Body size species appeared to take place between 2011 and 2014. These patterns were dominated by elpidiids (Holothuroidea: Elasipodida: Elpidiidae), which consistently increased in density during a period of high food availability, while other groups showed inconsistent responses. We considered minimum body length to be a proxy for size at juvenile recruitment. Patterns in density clustered by this measure, which was a stronger predictor of maximum density than median and mean body length. & 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction (4000–6000 m deep; Gage and Tyler, 1991). By contrast food supply, in the form of sinking particulate organic carbon, can be The deep sea offers unique model systems for studying pat- highly limited and variable in the deep sea. Periods of undersupply terns and mechanisms associated with community change. The co- can last years to decades, and the magnitude of episodic inputs existence of different species utilizing overlapping resources often vary more inter-annually than seasonally (Lampitt et al., within the same habitat, and changes in their relative abundance 2010; Smith et al., 2013). Benthic organisms living both within and over time, have been a long-standing interest of ecologists (Pianka, on top of the sediment increase in abundance following food 1973; Menge and Sutherland, 1976). However, many key ecological pulses (Pfannkuche et al., 1999; Galéron et al., 2001). As a result, variables associated with community composition change in tra- the relative access to high quality food appears to be a key driver of community composition over time at abyssal depths (Sibuet, ditionally studied ecosystems (e.g. terrestrial or shallow-water 1985; Gage and Tyler, 1991; Gooday, 2002; Ruhl and Smith Jr., marine) are either significantly different in, or absent from, the 2004; Baillon et al., 2011; Gambi et al., 2014). deep sea. For example photoperiod, temperature, and salinity are In terms of abundance and biomass, holothurians (Echino- common determinants of local distribution (Ricketts et al., 1992) dermata: Holothuroidea) are often the dominant mobile mega- and reproductive period in shallow water invertebrates (Giese, fauna group on the abyssal sea floor [(Gage and Tyler, 1991; 1959) including holothurians (McEuen, 1988; Babcock et al., 1992), Hansen, 1975; Lauerman et al., 1996; Ohta, 1983; Ruhl, 2007; Si- but these factors do not vary considerably at abyssal depths buet, 1985) but see Durden et al. (2015a); Megafauna are defined as those animals large enough to be visible in photographs

n (Grassle et al., 1975)]. They are major consumers and bioturbators Correspondence to: Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd, Moss Landing, CA 95039, USA. of organic carbon (Ginger et al., 2001), presumably feeding as they E-mail address: [email protected] (C.L. Huffard). transit an area (Bett et al., 2001). For the entire megabenthic

http://dx.doi.org/10.1016/j.dsr.2016.01.002 0967-0637/& 2016 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 28 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 community, seafloor reworking rates have been estimated on the magnitudes of fresh phytodetritus influx observed recently at Sta. order of one to two and a half years (Bett et al., 2001; Kaufmann M, we hypothesized recent food oversupplies might have fueled and Smith, 1997), but as rapid as six weeks during a holothurian broad-scale changes in holothurian communities. We compared “boom” event (Bett et al., 2001). Surface and sub-surface deposit holothurian demographics at Sta. M from 2006–2009 to 2011– feeding holothurians can account for a majority of reworking ac- 2014 to better understand species-specific responses during the tivity, in some cases out-pacing other taxonomic assemblages by a megafauna community transition described by Kuhnz et al. (2014). factor of 9:1 (Kaufmann and Smith, 1997). When present in high Using video collected by remotely operated vehicles (ROV) we densities holothurians can rapidly deplete the quantity and quality assessed changes in density (19 species) and body length (BL) of organic material in abyssal surface sediments (Bett et al., 2001; distributions (10 species), factors which are often used to detect Ginger et al., 2001). Through consumption and repackaging, they reproductive recruitment to the sea floor and immigration events broadly influence the availability and composition of food for (Billett et al., 2001; Ramirez-Llodra et al., 2005; Ruhl, 2007; Ka- other organisms (Billett et al., 2010; MacTavish et al., 2012), which logeropoulou et al., 2010). Body size is associated with numerous can lead to cascading impacts on subsurface deposit feeders (Iken ecological factors including population density and reproductive et al., 2001), infauna (Soto et al., 2010; Thistle et al., 2008), and potential (Pianka, 1973). Species with small body size character- scavenging fishes (Bailey et al., 2006). Abrupt, large-scale changes istics and/or high fecundity are predicted to gain ecological ad- in holothurian abundances have corresponded with ecological vantages in colonizing unpredictable resources (Pianka, 1973) in- shifts impacting multiple phyla that have lasted years to possibly a cluding at abyssal depths (Billett and Hansen, 1982; Billett, 1991). decade (Billett et al., 2010; Gooday et al., 2010; Kuhnz et al., 2014; Our dataset allowed us to test whether aspects related to body size Ruhl, 2007; Ruhl and Smith Jr., 2004; Wigham et al., 2003a). Shifts were associated with the ability to attain very high densities. in abyssal holothurian communities have been traced to surface Therefore we interpreted changes in holothurian densities in light processes (Smith et al., 2008), making them potential indicators of of their body lengths. climate change impacts on deep-sea ecosystems and carbon re- Specifically, we tested the following non-mutually exclusive mineralization processes (Glover et al., 2010). hypotheses: In a habitat that can experience chronic food limitation punc- tuated by episodic pulses of essential food, those holothurian 1. Holothurian densities were higher from 2011–2014 than 2006– species that are more efficiently able to locate and utilize fresh 2009. phytodetritus are proposed to gain a competitive advantage over 2. Immigration and juvenile recruitment events involving one or those that are restricted by slower locomotion, non-selective more species were more common from 2011–2014 than 2006– feeding tentacle morphology, and/or other physiological limita- 2009. tions (Hudson et al., 2003; Iken et al., 2001; Neto et al., 2006; 3. Body size characteristics (mean, median and minimum body Wigham et al., 2003a). Abyssal holothurians consume freshly- length) correlated with patterns in density. settled phytodetritus when available, and some species might re- A. quire surface-derived phytopigments and sterols for reproduction Maximum density correlated with mean, median and mini- (Drazen et al., 2008; FitzGeorge-Balfour et al., 2010; Ginger et al., mum body length. 2001; Iken et al., 2001; Lauerman and Kaufmann, 1998). These B. nutrients can be limiting in the deep-sea (Hudson et al., 2003; Density patterns over all sampling periods clustered with the Wigham et al., 2003a). Pulses of phytodetritus to the sea floor body size characteristic that best predicted maximum density. appear to trigger opportunistic reproductive activity in numerous deep-sea echinoderms including holothurians (Tyler et al., 1982; 4. Holothurian communities differed from 2006–2009 compared Eckelbarger and Watling, 1995; Galley et al., 2008; Wigham et al., to 2011–2014 as evidenced by differences in: 2003b). High-flux events represent especially favorable conditions A. because organic material reaching the sea floor can maintain a measures of species diversity and evenness high fraction of its surface-derived nutrients (Conte et al., 1998). B. Highly mobile surface deposit feeding holothurians quickly utilize community structure. fresher surface material, leaving larger, slower subsurface deposit feeders to consume more degraded forms (Iken et al., 2001). In some cases grazing rates by a few holothurian species together can 2. Methods match deposition rates of fresh material, thereby monopolizing a limiting resource (Bett et al., 2001; Wigham et al., 2003a). This 2.1. Study site and instrumentation differential access to food can lead to interspecific differences in reproductive effort and ultimately abundance (Ramirez-Llodra At Station M (34°50′N, 123°00′W) surface water productivity et al., 2005). corresponds with lagged food supply and megafauna responses on In recent years the supply of surface-derived food, including the abyssal sea floor [4000 m; (Ruhl and Smith Jr., 2004)]. The phytodetritus, at the abyssal time series monitoring site Station M sea bed is soft sediment (silty-clay), with topographic relief (northeast Pacific, 4000 m) has exhibited high magnitude epi- o100 m over 770 km2 (Kaufmann and Smith, 1997). Food falls as sodic pulses relative to 1989–2009 (Smith et al., 2014). The first particulate organic carbon and detrital aggregates comprised pri- two decades of the time-series were dominated by periods of food marily of phytodetritus but occasionally included gelatinous ma- undersupply (Smith et al., 2013). Corresponding with recent in- terial (Smith et al., 1998, 2014). Settling location of food on the sea creases in food input, the proportional density of holothurians in floor at this station can be patchy (Lauerman et al., 1996). relation to other megafauna groups also increased, from less than Between Dec 2006 and Oct 2014, two remotely operated ve- 5% in early 2007 to nearly 50% by mid-2011; mobile surface de- hicles (ROV Tiburon and ROV Doc Ricketts) video-recorded (high- posit feeders (primarily holothurians) gained numerical dom- definition Ikegama video cameras fitted with HA10Xt.2 Fujinon inance over sessile suspension feeders, signifying a major shift in lenses) benthic transects at Sta. M (220–1830 m long; n¼11 survey the megafauna community (Kuhnz et al., 2014). periods; Table 1). Intervals between sampling periods were not Given the known and suspected links between food supply and uniform. Two parallel lasers, 29 cm apart, were projected onto the deep-sea holothurian reproduction, and the exceptionally high sea floor continuously during ROV transect recording, and used as C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 29

Table 1 generally epibenthic, but can bury in the sediment. Small in- Survey periods and seafloor transect coverage. Dive numbers starting with “T” were dividuals of this species sometimes crawl onto or under other “ ” conducted with ROV Tiburon, and those started with D were conducted with ROV objects on the sea floor, making them difficult to view and size. Doc Ricketts. Thus small or buried individuals might have been undersampled. Dive Period Area (m2) When used, terms small/smaller, and large/larger compare the relative sizes of species measured in this study, rather than body T1067 Dec-06 1120 size categories which might be in use elsewhere. T1079, T1080 Feb-07 220 T1141, T1143 Sep-07 420 D8 Feb-09 1560 2.3. Statistical analyses D230-232 May-11 1830 D321 Nov-11 1004 2.3.1. Holothurian densities from 2006–2009 versus 2011–2014 D403 Jun-12 400 Holothurian densities were calculated per species by dividing D442 Nov-12 1377 D486 Jun-13 1278 the total number of individuals (ind.) measured on each transect D581 Apr-14 1414 by the total transect area annotated for that sampling period D671-674 Oct-14 1340 (Table 1). Densities were then adjusted to ind. ha 1 to be con- sistent with other studies on holothurian density (e.g. Billett et al. (2010)). We compared densities of each species from 2011 to 2014 a scale reference for size measurements of holothurians. The ROV to their densities calculated for the years 2006–2009 respectively imaging system yielded the ability to see and measure objects at using Wilcoxon–Mann–Whitney test (StatXact-4.0.1). All scatter least 3 mm in largest dimension. This resolution is sufficient for plots of densities were created using SigmaPlot 10.0. detecting specimens at the upper size range known for pelagic juveniles of species within Elasipodida, the most abundant and 2.3.2. Indicators of immigration and juvenile recruitment diverse group of deep-sea holothurians (Hansen, 1975; Tyler et al., Recruitment involves the addition of individuals to a popula- 1985a; Gebruk et al., 1997). This method reduces the sampling bias tion, whether by immigration or reproduction (Ebert, 1983). Our of trawling, in which small individuals can be undersampled use of the term recruitment was restricted to recognizable in- (Billett et al., 2001; Durden et al., 2015b), and overall abundances dividuals that could be detected on the sea floor (Ebert, 1983). can be underestimated by up to 50% (Billett, 1991). However this Species that release brooded young [as is likely for the O. mutabilis approach is not likely to detect species that bury into the sedi- complex at Sta. M (Hansen, 1975)], or settle as juveniles from the ment. While identifications to the species level can be difficult at plankton [as in some Elasipodids (Gebruk et al., 1997)] might be very small sizes, photographic survey methods are nevertheless detectable immediately upon release or settlement. Species that preferred over trawls for assessing sizes and densities of deep-sea develop into a juvenile form after settling on the sea floor would holothurians (Billett, 1991; Bluhm and Gebruk, 1999; Rogacheva be detected only after a post-settlement lag of unknown duration. et al., 2013; Durden et al., 2015b). Our use of the term recruitment refers to juvenile recruitment, as immigration events are discussed separately. 2.2. Animal identification and sizing from ROV footage We prepared notched box plots of BL distributions for those species represented by at least 10 size measurements each for at ROV transect video footage was annotated in the Monterey Bay least three time periods. Notched box plots offered an intuitive Aquarium Research Institute's open source Video Annotation Re- and rapid means for comparing data distributions including those ference System (VARS) (Schlining and Stout, 2006) for animal that are skewed (McGill et al., 1978; Krzywinski and Altman, 2014). identification and sizing. Each holothurian in the ROV transects Box plots of BL were generated using the online tool provided by was identified to the lowest possible taxon [http://dsg.mbari.org/ (Krzywinski and Altman, 2014). Notches were defined as dsg/images/concept/Holothuroidea,(Jacobsen Stout et al., 2015)] 71.58 the interquartile range (IQR), and represented the 95% and sized following Ruhl (2007). Nineteen distinct holothurian confidence interval of each median. Distributions could be con- morphotypes (referred to here as distinct species for simplicity) sidered significantly different from each other if the notches in were distinguished, counted, and sized in ROV footage. Peniagone their box plots did not overlap (McGill et al., 1978; Krzywinski and papillata Hansen (1975), Peniagone gracilis (Ludwig, 1894) and Altman, 2014). Whiskers represented data points 41.5 IQR. This Peniagone sp. A are visually similar and could be mistaken for each method is appropriate for describing normal distributions, or non- other when very small (4 2 cm). Likewise for Peniagone vitrea normal distributions based on sample sizes greater than five Théel 1882 and Peniagone sp. 1. (McGill et al., 1978; Krzywinski and Altman, 2014). While it can be Using the measurement tool in VARS, holothurian size (BL) was difficult to interpret populations with multiple peaks (e.g. bimodal measured digitally as the distance from the anterior end (between size distributions) using this method, such distributions were very the base of the dorsal papillae if present) to the posterior end of rare in our datasets. This method allowed us greater ability to the holothurian, excluding feeding tentacles (Ruhl, 2007). Some examine size distributions than histograms, which can require a Peniagone spp. postured with the anterior end raised off the sea- minimum sample size of 30 to be considered statistically useful floor. Our measurements were based on a straight line from (Krzywinski and Altman, 2014). Letters were assigned to box plots anterior to posterior, not including slight body curvature. These to facilitate identification of significantly different groups based on lengths were obtained only for individuals that were positioned non-overlap of notches. Letters were assigned to “letter groups” in along the same horizontal plane as the laser points illuminated on ascending alphabetical order from the largest BL distribution (A) to the sea floor in ROV footage, and then were compared to the the smallest distribution (E) for each species. distance between the lasers in the same frame. This sizing meth- We identified possible immigration and juvenile recruitment odology yields low measurement errors (o1 mm), and tends to events by comparing changes in median BL distributions and underestimate sizes where error occurs (Dunlop et al., 2015). In- density over consecutive sampling periods. Median rather than dividuals were not sized if they were positioned on top of another average BL was chosen because this measure is appropriate for object or strongly contorted. In rare cases very large individuals of comparing skewed distributions (Krzywinski and Altman, 2014), Scotoplanes globosa and other species were not fully visible in a as is common for deep-sea holothurian sizes (Tyler and Billett, single video frame, precluding sizing. Abyssocucumis abyssorum is 1988). As in other studies (Ramirez-Llodra et al., 2005; Ruhl, 2007; 30 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39

Billett et al., 2010; Kalogeropoulou et al., 2010) we considered an 3. Results increase in density along with a reduction of average or median body size to indicate a recent recruitment event. We suspected 3.1. Holothurian densities from 2006–2009 versus 2011–2014 immigration might have occurred if density and median BL both increased from one survey to the next because (1) shifts toward Density of all holothurians combined ranged from a minimum 1 1 smaller size distributions would not occur if densities rose due to of 286 ind. ha in Sep 2007 to a maximum of 23,566 ind. ha in Nov 2012 (Fig. 1 and Table 2). Enypniastes sp., Psychropotes depressa immigration rather than recruitment of new young (small) in- (Théel, 1882), Holothuroidea sp. 5 and Holothuroidea sp. 6 were dividuals (e.g. Ruhl (2007)), and (2) growth alone could explain an detected in only one or two sampling periods each and were not increase in median BL, but not an increase in density as well. We analyzed further. The remaining 15 species varied in density by 1– did not analyze the relationships between density and BL dis- 4 orders of magnitude from 2006 to 2014 (Fig. 1 and Table 2). Only tribution in May 2011 because of the very large sampling gap prior A. abyssorum (Théel, 1886) and Synallactidae sp. 1 were detected in to that survey. all sampling periods. Densities were significantly higher from We considered minimum body length to be a proxy for size at 2011–2014 compared to 2006–2009 for Paelopatides confundens juvenile recruitment, the size at which juveniles could be identi- Théel, 1886, Psychropotes longicauda Théel, 1882, Elpidia sp. A,P. fied transiting the sea floor. Echinoderms surveyed at this size gracilis, P. papillata, P. vitrea, Peniagone sp. A., Peniagone sp. 1, Pe- have likely passed through post-settlement mortality (Balch and niagone sp. 2, and S. globosa (Wilcoxon–Mann–Whitney po0.05). Scheibling, 2001). This trait has been associated with survivorship, Densities were significantly lower from 2011–2014 compared to growth, and population density of other marine taxa (Cargnelli 2006–2009 for Pseudostichopus mollis Théel, 1886 (Wilcoxon– and Gross, 1996; Sogard, 1997; Searcy and Sponaugle, 2001; Ga- Mann–Whitney p¼0.05). Densities were not significantly different – – gliano et al., 2007). from 2011 2014 compared to 2006 2009 for Synallactidae sp. 1, A. abyssorum, Oneirophanta mutabilis complex, and Holothuroidea sp. – – 4 2.3.3. Body size and density 4 (Wilcoxon Mann Whitney p 0.05). Doublings (or greater in- Using StaXact 4.0.1, we calculated Spearman Rank correlation creases) of multiple species between sampling periods were coefficients to test whether maximum density correlated with common, particularly when comparing respective consecutive sampling periods between Feb 2009 and Nov 2012. Halving (or mean, median or minimum BL. We generated a 3D scatter plot of greater reductions) of densities between consecutive sampling mean, median, and minimum BL using Sigma-Plot 10.0. To ex- periods were also common, particularly when comparing densities amine differences in density patterns based on body size char- recorded between Nov 2012 and Apr 2014 (Table 2). acteristics, we used Primer-E 6 (Clarke and Warwick, 2001)to perform a cluster analysis using the SIMPER routine. This test re- 3.2. Indicators of immigration and juvenile recruitment turned levels of similarity between species based on patterns in their density distributions. The Bray–Curtis dissimilarity matrix 3.2.1. Holothurian body length distributions was based on square-root-transformed density data, with survey Details for the 10 species that could be analyzed for BL dis- dates listed as variables and species listed as samples. The mini- tributions are given below, in the same order as species listed in mum BL record for each species was then mapped onto the re- Table 2. Notched box plots are illustrated in Fig. 2. Summary sta- tuned dendrogram, with color corresponding to a size-based red– tistics for BL distributions are provided in Supplementary Table 1. blue scale. Groupings that clustered at greater than the 50% level Relationships between minimum, mean, and median BL are plot- were identified by Primer-E with colored branching. Asterisks ted in Supplementary Fig. 1. were also added to identify species known or suspected to swim in 3.2.1.1. Abyssocucumis abyssorum. A. abyssorum densities were their adult form at Sta. M based on in situ observations, designa- highest in Feb 2009 (269 ind. ha1) and lowest in Apr 2014 tion as benthopelagic in the adult form in the literature (Miller and (42 ind. ha1; Figs. 1A and 2). Small individuals were often found Pawson, 1990), or suspected (in parentheses) based on the pre- located on top of other objects or sessile organisms, such as sence of a large velum (following Rogacheva et al. (2013)). While sponge stalks. These individuals could not be measured (Dunlop many species swim facultatively when disturbed (Rogacheva et al., et al., 2015), and as such small individuals were underrepresented 2012, 2013) we were primarily interested in species which might in BL distribution summaries. For this reason, 20% or more (range swim to migrate as adults. 21–33%) of individuals could not be sized in Dec 2006, Feb 2007, Nov 2011, Nov 2012 and Apr 2014. In Feb 2009 85% of individuals 2.3.4. Holothurian community change could not be sized. BL distributions were skewed to high numbers To test whether holothurian communities differed in 2011– of small or unsized (typically small) individuals during the periods 2014 compared to 2006–2009, we calculated species diversity of relatively high density in Feb 2009, Jun 2012 and Nov 2012. BL (Shannon H′) and species evenness (Pielou's J′) for each survey of A. abyssorum ranged from 2.3 to 15.5 cm. using Primer-E. We then performed the Wilcoxon–Mann–Whitney test using StatXact-4.0 to compare groups of these measures based 3.2.1.2. Paelopatides confundens. Densities of P. confundens were 1 on surveys from 2011–2014 versus 2006–2009. Differences in highest in Oct 2014 (91 ind. ha ), and when detected, lowest in 1 community structure were assessed using non-metric multi- Feb 2009 (6 ind. ha )(Figs. 1A and 2). BL distributions were dimensional scaling (MDS) plots prepared in Primer-E based on skewed toward small individuals during surveys with relatively Bray–Curtis dissimilarity indices of square-root-transformed den- high density in Nov 2011 and Nov 2012. The period with the highest density was represented by larger rather than smaller sity data. Species were listed as variables and survey dates were individuals. P. confundens BL ranged from 2.8 to 23.3 cm. listed as samples. A cluster analysis was then performed using the SIMPER routine to return levels of similarity between sampling 3.2.1.3. Synallactidae sp. 1. Density of Synallactidae sp. 1 was rela- periods based on similarities in their holothurian density dis- tively high in Feb 2007 (182 ind. ha1) and Oct 2014 tributions. Similarity contours were overlain on the MDS plot to (172 ind. ha1), the latter period represented by an abundance of identify sampling periods that clustered at the 40% and 50% level. relatively small individuals. In May 2011 individuals were larger, C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 31

Fig. 1. Holothurian densities at Station M based on remotely operated vehicle transects at Sta. M between 2006 and 2014. Dashed red line highlights density of 1000 ind. ha1. Species represented by warm colors exceeded densities of 1000 ind. ha1 at some point during the study. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) and found at relatively low densities (Figs. 1A and 2). The lowest 2013 were in the largest size grouping (A). density documented was 10 ind. ha1, in Nov 2011. BL of Sy- nallactidae sp. 1 ranged from 2.6 to 18 cm. 3.2.1.5. Peniagone gracilis. P. gracilis was not detected during sur- veys in 2007, 2008, or 2009. Records of high densities corre- 3.2.1.4. Elpidia sp. A. Elpidia sp. A was either undetected or de- sponded with larger size distributions, particularly in May 2011 tected in moderate numbers of small individuals in 2007, 2008, (907 ind. ha1) and Jun 2012 (1150 ind. ha1; Figs. 1C and 2). The 2009, and May 2011 (0–1295 ind. ha 1; Figs. 1C and 2). Starting in two sampling periods with a population skewed toward small size Nov 2011, BL and densities were successively higher with each distributions (Nov 2012 and Apr 2014) corresponded with rela- sampling period until the highest density was recorded in Nov tively low densities (337 and 375 ind. ha1 respectively) compared 2012 (10,524 ind. ha 1), after which densities were lower with to highs. The rapid change from higher density in Jun to lower each successive sampling period. Elpidia sp. A BL ranged from density in Nov 2012 was accompanied by a change in BL dis- 0.5 to 6.9 cm. All BL distributions were the same as or differed by tribution from letter group A (largest) to letter group C (second one letter group compared to BL distribution of the previous smallest). P. gracilis BL ranged from 1 to 10.9 cm. sampling period. Individuals sampled in Feb 2007, Feb 2009, and May 2011 were in the smallest size grouping (C). Individuals 3.2.1.6. Peniagone papillata. P. papillata was detected in low num- sampled in Nov 2011 and June 2012, and Apr 2014 were in the next bers in 2007, 2008 and 2009 (0–36 ind. ha 1). Relatively high largest size grouping (B), and those sampled in Nov 2012 and June densities were recorded in May and Nov 2011 (224, 309 ind. ha1 32 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39

Table 2 Densities of holothurians (ind. ha1) recorded at Station M between Dec 2006 and Oct 2014 as calculated from ROV transects of sea floor. Those species in bold were encountered in significantly different densities in 2011–2014 compared to 2006–2009 (¼species with greater density in 2006–2009 compared to 2011–2014; þ¼ species with greater density in 2011–2014 compared to 2006–2009); †¼those known to bury; *¼those known to be capable of swimming in their adult form based on in situ observations in California, designation as benthopelagic in the adult from Miller and Pawson (1990), or suspected (in parentheses) based on the presence of a velum (following Rogacheva et al. (2013)).

Order Family Taxon Dec- Feb- Sept- Feb- May- Nov-2011 Jun-2012 Nov-2012 Jun-2013 Apr-2014 Oct-2014 2006 2007 2007 2009 2011

Dendrochirotida Cucumariidae †Abyssocucumis 125 227 95 269 84 80 175 177 180 42 104 abyssorum Aspidochirotida Synallactidae þ*Paelopatides 0 91 24 6 11 80 50 112 86 106 134 confundens Pseudostichopus 36 0 24 71 11 0 0 0 0 0 15 mollis Synallactidae sp. 1 45 182 95 38 55 10 25 67 94 71 172

Elasipodida Deimatidae Oneirophanta mutabilis 27 45 0 51 16 10 50 0 63 7 30 complex Pelagothuriidae *Enypniastes sp. 900 000 0 0 0 0 0 Psychopodidae Psychropotes depressa 000 00100 0 0 0 0 þPsychropotes 0 0 0 0 0 0 25 37 23 21 7 longicauda Elpidiidae þElpidia sp. A 0 409 0 109 1295 3436 4725 10,524 4264 141 22 þ*Peniagone gracilis 0 0 0 0 907 777 1150 337 900 375 306 þ*Peniagone 36 0 24 13 224 309 150 105 141 57 22 papillata þ*Peniagone vitrea 45 0 0 410 732 966 800 1683 1088 389 2545 þ*Peniagone sp. A 18 0 0 19 3628 4213 4200 5079 5321 5255 11,627 þ*Peniagone sp. 1 0 0 0 0 0 0 0 2917 1534 7 1142 þ(*)Peniagone sp. 2 0 0 0 19 11 159 50 202 55 57 22 þScotoplanes globosa 0 0 0 6 514 876 1300 2304 2465 1337 1246

UNK UNK Holothuroidea sp. 4 18 0 24 90 33 70 25 22 55 7 22 Holothuroidea sp. 5 0 0 0 27 13 0 0 0 0 0 0 Holothuroidea sp. 6 0 0 0 6 0 0 0 0 0 0 0 TOTAL 359 954 286 1134 7534 10,996 12,725 23,566 16,269 7872 17,416

respectively) before pre-2011 levels were recorded in Apr and Oct 3.2.1.9. Peniagone sp. 1. Peniagone sp. 1 was not detected in 2007– 2014 (57, 22 ind. ha1 respectively; Figs. 1C and 2). The largest size 2011 (Figs. 1C and 2). It was first detected in Nov 2012, with high distribution (May 2011) corresponded with the second highest densities (2917 ind. ha1) of relatively large individuals, many of density record. Body length distribution during the period with which appeared to be gravid (Fig. 3). Targeted collections with the highest density (Nov 2011) was skewed toward small individuals. ROV confirmed the presence of gametes. Moderate densities of P. papillata BL ranged from 2.5 to 19.5 cm. somewhat smaller individuals were detected in Jun 2013 (1534 ind. ha1), and large individuals in Oct 2014 3.2.1.7. Peniagone vitrea. P. vitrea was not detected, or was de- (1142 ind. ha1). Peniagone sp. 1 was detected in very low num- tected in low numbers, in 2007 and 2008 (0–45 ind. ha1; Figs. 1C bers in Apr 2014 (7 ind. ha1). Body length of Peniagone sp. and 2). Moderate densities of small individuals were detected in 1 ranged from 1.5 to 9.4 cm. Each of the three periods during Feb 2009 (410 ind. ha1). Higher densities of larger individuals which Peniagone sp. 1 was detected was represented by a sig- were recorded in May and Nov 2011, and Jun 2012 nificantly different BL distribution. (732–966 ind. ha1). A high density of small individuals was de- tected in Nov 2012 (1683 ind. ha1). Lower density (389 ind. ha1) 3.2.1.10. Scotoplanes globosa. S. globosa was not detected, or de- of small individuals was detected in Apr 2014. The highest density tected in low numbers from 2007 to 2009 (0–6 ind. ha1). In May was recorded in Oct 2014 (2545 ind. ha1), when the size demo- 2011, a moderate density of large individuals was observed graphics were large. However the very high density also included a (514 ind. ha1; Figs. 1C and 2). Successively higher densities were large number of small individuals. P. vitrea BL ranged from 1.2 to recorded during each sampling period until the highest densities 12.4 cm. were recorded in Nov 2012 and Jun 2013 (2304 and 2465 ind. ha1 respectively). Successively lower densities were then recorded 3.2.1.8. Peniagone sp. A. Peniagone sp. A was not detected, or de- reaching densities approximately equal to those recorded in Jun tected in very low numbers, in 2007, 2008 and 2009 2012 (1300 ind. ha1). Size distributions were small in Nov 2011 (0–19 ind. ha1). Moderate densities of the largest size fraction and Nov 2012, before increasing again to large sizes in Oct 2014. were detected in May 2011 (3628 ind. ha1; Figs. 1C and 2). All size distributions had high-BL outliers and no small outliers. S. Densities ranged from 3628 to 5321 individuals ha1 from May globosa BL ranged from 1.3 to 19.3 cm. 2011 through Apr 2014, with each period represented by small BL distributions. A very large number of primarily large individuals 3.2.2. Immigration and juvenile recruitment was detected in Oct 2014 (11,627 ind. ha1). Peniagone sp. A BL Numerous sampling periods in our study were associated with ranged from 0.9 to 14.5 cm. Density in Oct 2014 was double that increases in both density and BL of holothurians. We tentatively recorded in Apr 2014, a change that corresponded with an increase identified these cases as representing some form of immigration in size distribution from the smallest to the second largest. prior to Nov 2011 (Elpidia sp. A), Jun 2012 (P. gracilis), Nov 2012 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 33

Fig. 2. Density and body length (BL) distributions of holothurians encountered during remotely operated vehicle transects at Sta. M between 2006 and 2014 (density in red, notched box plots of BL in black). Box plots are shown for samples sizes of 10 or greater showing sample mean (þ), whiskers (1.5 interquartile range), and outliers (open circles). Letters by box plots identify groups significantly different from each other based on non-overlap of box plot notches. Letters signifying size distributions are in alphabetical order with group A representing the group with the largest individuals and E the smallest of each species. Small individuals of A. abyssorum were undersampled because they were frequently found on top of other objects and could not be sized. Small individual A. abyssorum were especially undersampled in Feb 2009, Nov 2011, Nov 2012 and Apr 2014 when 85%, 25%, 30% and 32% of sampled individuals could not be sized (see text). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

(Elpidia sp. A, Peniagone sp. 1), Jun 2013 (S. globosa, P. gracilis), and 2011 and Nov 2012), and P. gracilis for which Jun 2013 density was Oct 2014 (P. confundens, P. vitrea, Peniagone sp. A, and Peniagone sp. nearly three times that in Nov 2012, and BL was significantly higher. 1). The most notable examples of this pattern occurred in Elpidia sp. Two surveys in which we recorded high Peniagone sp. 1 density A, which significantly increased in BL while more than doubling in following from previously undetectable levels appeared to be ag- density twice during our study (in the 5–6monthspriortoNov gregations of gravid individuals, possibly for spawning (Fig. 3). 34 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39

Fig. 3. Peniagone sp. 1. (A) Close up and (B) wider view showing high densities of what appear to be gravid individuals in Nov 2012. Targeted collections verified the presence of ripe eggs and sperm. Red lasers in panel B are 29 cm apart. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

We identified numerous periods in which a recent juvenile might have occurred prior to Feb 2009 (A. abyssorum), Nov 2011 (S. recruitment event appeared to occur based on a concurrent in- globosa, P. papillata, Peniagone sp. A), June 2012 (A. abyssorum), crease in density and reduction of median BL. Recruitment events Nov 2012 (A. abyssorum, P. confundens, S. globosa, P. vitrea,

Fig. 4. Density patterns of holothurians encountered during remotely operated vehicle transects at Sta. M, from 2006 to 2014. (A) Scatter plot of maximum density recorded versus minimum (gray circles), mean (open circles) and median (black triangles) body length (BL). Note common log scale of axes. Colored lines were added on the y-axis for illustrative purposes to identify maximum density ranges of species that clustered by density patterns according to the SIMPER test. Line color corresponds with dendrogram branch color in panel C. (B) Clustering of holothurian species according to similarities in their density patterns across remotely operated vehicle transects at Sta. M between 2006 and 2014. Red and blue dashed lines identify clusters that are significantly similar to the degree indicated on the y-axis, according to the SIMPER test. An asterisk denotes species known (or suspected in parentheses) to swim in their adult form based on in situ observations in California or a benthopelagic designation by Miller and Pawson (1990). (C) Multidimensional scaling plot comparing holothurian density patterns by sampling period (2006–2009 black squares; 2011–2014 green squares; each square represents a separate ROV survey). Ellipsoids group data points that cluster according to the SIMPER test (40% similarity-gray lines, 50% similarity-black lines). (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 35

Peniagone sp. A), Jun 2013 (P. papillata) and Oct 2014 (Synallactidae event involved increases in densities of A. rosea, Ellipinion molle sp. 1). (Théel, 1879), P. longicauda, Oneirophanta mutabilis Théel (1879), Pseudostichopus aemulatus Solis-Marin & Billett in Solis-Marin 3.3. Body size and density et al., 2004, and Molpadiodemas villosus (Théel, 1886), and de- creases in Peniagone diaphana (Théel, 1882) (Billett et al., 2001, For the 15 holothurian species that were encountered in more 2010). than two sampling periods, maximum density was significantly The abyssal holothurian densities we observed were compar- inversely correlated with minimum BL (Spearman's ρ¼0.9159, able to those documented in other studies. Except for higher two-sided po0.0001; Fig. 4A—gray dots), mean BL (Spearman's densities of A. abyssorum (1317 ind. ha1) found at Sta. M in Jun ρ¼0.7979, two-sided p¼0.0004; Fig. 4A—open circles), and 2002, our density estimates were similar to those documented median BL (Spearman's ρ¼0.6676, two-sided p¼0.0065; Fig. 4A previously at this site using towed camera sleds (Ruhl, 2007), and —black triangles). All holothurians in our study that attained slightly higher than those found during trawl surveys of the same densities of 1000 or greater individuals ha1 had a minimum body species or congeners in the northeast Atlantic at the PAP (Billett size of 1.5 cm or smaller. et al., 2001, 2010). All but two elpidiids in our study (P. papillata Patterns in density across all sampling periods clustered by and Peniagone sp. 2) exceeded densities of 1000 ind. ha1 at some species with similar minimum BL records (Fig. 4B). Those species point, with the highest values calculated for Peniagone sp. A with minimum BL records between 0.5 and 1.5 cm formed a sig- (11,627 ind. ha1) and Elpidia sp. A (10,524 ind. ha1). Very high nificant cluster (Fig. 4C—red branching), and attained the highest densities are commonly attained by members of this family at sites maximum densities (Fig. 4A). This cluster was comprised entirely throughout the globe, with some species far surpassing densities of elpidiids. Those species with minimum BL records ranging from observed at Sta. M. The small elpidiid Amperima rosea (Perrier, 1.8–3.2 cm (Fig. 4B—blue branching) also formed a significant 1896) in the abyssal Atlantic rose from undetectable levels in 1994 cluster, and attained moderate maximum densities (Fig. 4A). Two to over 6000 ind. ha1 in 1997 as calculated using time-lapse elpidiids (P. papillata and Peniagone sp. 2) were present in this photography (Bett et al., 2001). Based on video and photographic cluster. Psychropotes longicauda and P. mollis had the largest records respectively, Kolga hyalina Danielssen and Koren, 1879 minimum BL records (3.8 cm and 6.9 cm respectively), and were [following identification in Rogacheva (2012)] frequently reaches not a part of any significant cluster (Fig. 4A and B). densities equivalent to 5000–10,000 ind. ha1 in the Norwegian- Greenland Basin (identified as Irpa abyssicola Danielssen and Ko- 3.4. Holothurian community change ren, 1879 in Gebruk et al. (2003)), and Peniagone japonica Oh- shima, 1915 has reached estimated densities of 79,070 ind. ha1 in Diversity (Shannon H′) of holothurians was not significantly Japanese waters (Ohta, 1983). Rhipidothuria racovitzai Hérouard, different from 2006–2009 versus 2011–2014 (average 1901 (then treated as Achlyonice violaecuspidata Gutt, 1990) and 1.5670.24 S.D.; Wilcoxon–Mann–Whitney U¼18.00, two-sided Elpidia glacialis Théel, 1876 in the Weddell Sea have been photo- p¼0.44). Evenness was significantly higher from 2006–2009 ver- graphed at densities equivalent to 260,000 and 320,000 ind. ha1 sus 2011–2014 (Wilcoxon–Mann–Whitney U¼28.00, two-sided respectively (Gutt and Piepenburg, 1991). Perhaps attaining the p¼0.0082; 2006–2009 Pielou’sJ′¼0.8470.07 S.D.; 2011–2014 highest known deep-sea holothurian densities, Kolga nana (Théel, Pielou’sJ′ avg.¼0.5870.10 S.D.). The relative density patterns of 1879) has reached average densities equivalent to holothurians during the 2006–2009 period differed significantly 500,000 ind. ha1 as calculated from epibenthic sledge and pho- from those documented from 2011 to 2014 based on clustering at tographic surveys in the Porcupine Seabight [treated as Kolga the 50% level (Fig. 4C). hyalina in Billett and Hansen (1982), taxonmy reassessed in Ro- gacheva (2012)]. Density estimates based on photogrammetry, epibenthic sledge, and trawl samples will differ (Billett, 1991) but 4. Discussion gross differences can still be informative. As is common among echinoderms (Uthicke et al., 2009) in- 4.1. Holothurian densities from 2006–2009 versus 2011–2014 cluding abyssal holothurians (Billett et al., 2001, 2010), boom and bust cycles were typical among holothurians at Sta. M, especially Our results suggest that a recent shift in the megafauna com- among the elpidiids. This pattern was most-clearly demonstrated munity at Sta. M (Kuhnz et al., 2014) resulted in part from re- by Elpidia sp. A, for which density was higher by an order of sponses across multiple holothurian species. Between 2006 and magnitude in Nov 2012 compared to May 2011, and then was 2009, sponges were the numerically dominant megafauna group lower by roughly an order of magnitude in each subsequent survey (Kuhnz et al., 2014). At that time, all holothurian species examined through Oct 2014, when it was detected at very low density. This here were found in relatively low densities. Following 2009, ho- species demonstrated a similar pattern previously at Sta. M (Ruhl lothurians as a group increased in density and gained numerical and Smith, 2004). We do not know whether “bust” periods re- dominance, while sponges declined in density and proportional presented mortality or emigration. Both of these processes remain abundance (Kuhnz et al., 2014). This transition involved significant poorly understood but are likely to be important components of increases in the densities of 10 out of 19 holothurian species en- holothurian population dynamics at Sta. M. In both time-lapse countered from 2011 to 2014, including all eight species within the camera images [methods described in Smith and Druffel (1998)] family Elpidiidae. Ten species increased in density between Jun and ROV video recorded at the site we have documented what and Nov 2012, a period of exceptional availability of freshly-settled might be dead holothurians on the sea floor. However individuals phytodetritus (Smith et al., 2014). We did not find a suite of ho- showing obvious signs of decay have been encountered rarely. We lothurian species that thrived in 2006–2009 but declined in 2011– have seen many Peniagone sp. A lying on their side or rolling along 2014. Only one holothurian species (P. mollis) declined in density the bottom, but we did not annotate these individuals as dead in during this transition, and was less dense from 2011–2014 com- ROV footage. They did not look compromised otherwise. Those pared to 2006–2009. These pervasive increases in holothurian individuals might have been knocked over by the bow wave of the density over a period lasting at least four years are comparable to ROV, or performing a behavior we have observed in time-lapse what has been called the “Amperima event” at the Porcupine images but cannot explain: individuals of Peniagone sp. A have Abyssal Plain (PAP), which lasted approximately three years. This been seen lying on their side for several hours and appearing dead, 36 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 but then resuming a prone position and crawling or swimming Multi-species recruitment and immigration events were away. documented during 2011–2014, but only once during 2006–2009 (one recruitment of A. abyssorum prior to Feb 2009). Throughout 4.2. Indicators of immigration and juvenile recruitment this period, Nov 2012 appears to have been the most active time for recruitment and immigration of holothurians to Sta. M, with Juvenile recruitments of multiple species appear to have oc- increases in 10 out of 19 species. This survey period followed curred during three periods in our study (prior to Nov 2011, Nov shortly after continuous, high percent-coverage depositions of 2012 and Jun 2013). All of these periods occurred between 2011 surface-derived salp detritus and phytodetritus were observed on and 2014. Small sample sizes might have contributed to our failure the sea floor, lasting from Mar–Aug 2012 (Smith et al., 2014). These to detect apparent recruitment events (or a lack thereof) between high-flux deposition events fueled the most significant period of 2006 and 2009. A. abyssorum, P. papillata, Peniagone sp. A, and S. food over-supply documented at Sta. M. since records began in globosa appear to have demonstrated more than one recruitment 1989 (Smith et al., 2013). We can only speculate that these 10 event each from 2011 to 2014, suggestive of opportunistic re- species might have responded to the same environmental cue to production or settlement by these species when food was plenti- ful. Evidence for reproductive recruitment of multiple holothurian increase their local densities: a high magnitude deposition of high fl species has been documented previously at the PAP (Billett et al., quality food to the sea oor. In conjunction with this event, density 2001, 2010), and Sta. M (Jun 1990; Ruhl, 2007). The “Amperima of Peniagone sp. A increased rapidly, lagging salp detritus percent event” involved recruitments of both A. rosea and P. longicauda cover by 14 weeks (Smith et al., 2014). This rapid increase in (Billett et al., 2010), perhaps during a shift in food composition at density was accompanied by a significant reduction of median BL the PAP (Wigham et al., 2003a). In Jun 1990 at Sta. M, a period of between Jun and Nov 2012. Based on these results we raise the moderate food supply, Elpidia sp. A (then identified as E. minu- possibility that larval settlement of Peniagone sp. A might have tissima), P. diaphana, P. vitrea, and A. abyssorum exhibited both occurred in response to these deposition events. If Peniagone sp. A lower median BL and higher densities compared to the prior recruitment stemmed from local reproduction, then an opportu- sampling period (Ruhl, 2007). nistic spawning response by Peniagone sp. A took place on a very Based on examples for which density and BL distribution were short timescale. both higher in consecutive sampling periods, we documented We recognize several sources of error that might have impacted possible immigration of six species of holothurian (Elpidia sp. A, P. our assessments of recruitment and immigration. We assumed confundens, P. gracilis, Peniagone sp. A, Peniagone sp. 1, and P. vi- only positive growth when interpreting patterns in BL. However trea), an assemblage that is skewed toward species that attained body length of individual holothurians can change significantly high maximum densities (Table 2), exhibited similar density pat- through uptake or excretion of water (Hamel et al., 1993), and terns (Fig. 4A), and had small minimum BL records (Fig. 4A and negative growth can occur during periods of non-feeding (So et al., Supplementary Table 1). For all of these species, maximum den- 2010; Hannah et al., 2012). Assimilation efficiencies can be nega- sities coincided with possible immigration events (Figs. 2 and 4C). tive in the absence of phytodetritus (Ginger et al., 2001). If nega- Furthermore adult P. gracilis, Peniagone sp. A, Peniagone sp. 1, P. tive growth occurred at Sta. M during our study then we might vitrea, and P. confundens are known to swim as adults (Table 2 and have falsely interpreted declines in median BL as resulting from Miller and Pawson, 1990). We do not know the distances from which these holothurians might have emigrated, or the degree to recruitment events. Because spatial patchiness can be common which benthopelagic species might have swum to new areas. Sta. among deep-sea holothurians, and has occurred at Sta. M (Lauer- M site is an open system without obvious boundaries to the sur- man et al., 1996), demographics surveys can be sensitive to de- rounding abyssal benthos. viations of survey location (Billett and Hansen, 1982). Calculating The idea that deep-sea holothurians might migrate and/or form densities for species that aggregate can be especially problematic spawning aggregations is not new (Billett, 1991; Ruhl, 2007). Nu- because individuals concentrate from a larger area of unknown merous echinoderms aggregate (Billett and Hansen, 1982; Gutt spatial extent [e.g. Ohta (1985) and Billett and Hansen (1982)]. and Piepenburg, 1991; Young et al., 1993) for purposes including Elsewhere megafauna spatial variation has been attributed to in- reproduction (Tyler et al., 1993). Some cold-water holothurians fluences of bottom topography on food availability (Rowe, 1971; undergo vertical depth migrations for spawning (Hamel and Billett and Hansen, 1982) and flow dynamics, which might alter Mercier, 2008). Deep-sea holothurians can exhibit patchy or ag- particulate supply and sediment characteristics (Durden et al., gregated distributions in relation to food at Sta. M (Lauerman 2015a). Body size (Billett and Hansen, 1982; Bisol et al., 1984), and et al., 1996). Distant chemical cues have been shown to assist cold- reproductive characteristics (Galley et al., 2008; Baillon et al., water echinoderms in locating food [e.g. the sea star Odontaster 2011) can also vary spatially. These aspects are not expected to validus Koehler, 1906 (Kim et al., 2007)], and inducing spawning have a significant impact on our results and conclusions. Station M (Soong et al., 2005) at the local scale. However the bathyal echi- lacks substantial relief (Kaufmann and Smith, 1997), and of the noid Stylocidaris lineata does not appear to locate food from a holothurians we documented, only Peniagone sp. 1 in Nov. 2012 distance (Young et al., 1993). To our knowledge the role of distance was strongly aggregated (Fig. 3). Spatial heterogeneity in density chemoreception in influencing deep-sea holothurian migration and dispersion of individual megafauna taxa can be significant and/or aggregation has been hypothesized (Ohta, 1985), but not over a distance of tens of kilometers at Sta. M, although near-sy- explored. The ability of some holothurians to swim has been noptic megafauna density measures from nearby sites agreed by suggested as a factor that might facilitate migrations (Billett, 1991), and the tendency of numerous species to move or orient con- an average of 70% (Lauerman et al., 1996). Our study was based on fi sistently according to currents (Ohta, 1983; Gutt and Piepenburg, benthic transects con ned to a relatively small area compared to 1991; Kaufmann and Smith, 1997; Gebruk et al., 2003; Gallo et al., earlier towed-camera sled studies at the site (Kuhnz et al., 2014). 2015) provides a possible mechanism for navigation. The empirical Finally, we assumed any spatial variation in BL and densities to be study of large-scale movements by adult holothurians represents a overshadowed by temporal variation in these aspects as found significant opportunity for further understanding of true ho- during a 16 yr time series study of BL and densities at Sta. M (Ruhl, lothurian biomass distribution, and the scale of their influence on 2007). The interannual fluctuations observed here far exceeded abyssal ecosystems. the spatial variation reported previously (Lauerman et al., 1996). C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39 37

4.3. Body size and density generation times. Some holothurians outside of Elpidiidae might be physiologically limited in their ability to produce large numbers Small body size, continuous gamete production, broadcast of eggs, as has been shown in O. mutabilis (Ramirez-Llodra et al., spawning, and a brief lecithotrophic larval stage are considered 2005), which broods its young, and psychropotids, which produce important factors allowing some deep-sea holothurians to recruit exceptionally large eggs (Hansen, 1975; Tyler et al., 1985b). Rapid opportunistically high numbers of young to the sea floor during locomotion and feeding behavior have been predicted to confer unpredictable favorable conditions (Billett and Hansen, 1982; Tyler trophic advantages to O. mutabilis exploiting detritus on the sea et al., 1985a; Billett, 1991; Gebruk et al., 2003; Hudson et al., 2003; floor (Roberts et al., 2003). These advantages did not translate to Wigham et al., 2003b; Ruhl, 2007; Billett et al., 2010; Rogacheva higher population densities of this species complex when fresh fi et al., 2012). Our results add to these ideas by showing signi cant phytodetritus was available in great quantities at Sta. M. Any inverse correlations between body size measures and maximum competitive advantage of elpidiids conferred by the characteristics densities attained. above might be short-lived, or strongly dependent on the avail- ability of fresh surface-derived nutrients. Elpidiids were found in 4.4. Holothurian community change very low or undetectable numbers when fresh phytodetritus was limiting, and they exhibited significant boom and bust cycles when At the abyssal monitoring sites Sta. M and the PAP, abrupt and it was abundant. From an evolutionary standpoint, if Elpidiidae long-lasting transitions in holothurian communities have been traced to changes in surface processes that influence the quantity, forms a monophyletic group then many traits considered amen- fl quality, timing, and distribution of phytodetritus settled on the sea able to high holothurian density on the abyssal sea oor during floor (Gage and Tyler, 1991; Billett et al., 2001; Wigham et al., boom times might have evolved once, in the most recent common 2003a; Ruhl and Smith Jr., 2004; Smith et al., 2006; Ruhl, 2007; ancestor of elpidiids. These traits would therefore represent a Ruhl et al., 2008; Billett et al., 2010). These changes have led to sample size of one in comparative studies (Garland et al., 1992). A community-wide alterations in reproductive biology, species detailed understanding of deep-sea holothurian phylogenetic re- composition, dominance, abundance, carbon burial (Ruhl, 2007; lationships is required for studies using independent contrasts Ruhl et al., 2008; FitzGeorge-Balfour et al., 2010) and possibly (Garland et al., 1992) to yield a more robust understanding of animal distribution and movements (Lauerman et al., 1996; deep-sea holothurian responses to food supply. Kaufmann and Smith, 1997). Our study lends further support to these ideas. Recent anomalous surface processes along the U.S. 4.5. Conclusions west coast (e.g. Chavez et al. (2011), Kahru et al. (2012) and Kin- tisch (2015)) have led to increases in food flux events at Sta. M We studied change in densities and BL demographics of ho- (Smith et al., 2013, 2014), and corresponded with significant and lothurians from 2006–2009 to 2011–2014, periods that took place persistent changes in holothurian assemblages. Holothurian before and after a recent shift in the megabenthic community at communities during the 2006–2009 period were significantly the abyssal time-series monitoring site Sta. M (Kuhnz et al., 2014). different from those documented between 2011 and 2014 (Fig. 4B). This latter period encompassed exceptionally high-magnitude These periods corresponded with periods of moderate and ex- fl ceptionally high food supply respectively (Smith et al., 2013, 2014). pulses of food supply to the sea oor (Smith et al., 2013, 2014). While species diversity of holothurians remained unchanged While holothurian species diversity did not change during our during our study, species evenness was significantly lower in study, these animals exhibited lower densities and higher species – – 2011–2014, as has been found previously during periods of ele- evenness during 2006 2009 than 2011 2014. Patterns indicative vated food supply at Sta. M (Ruhl, 2008). These patterns largely of juvenile recruitment and immigration by multiple species were agree with the theoretical framework outlined by Ruhl et al. (2013) exhibited multiple times when food was abundant. This pattern predicting relationships between total density, respiration rate, was dominated by species within the elasipodid family Elpidiidae, and species evenness. which were present in very low densities during 2006–2009 and We cannot evaluate our results separately from a phylogenetic very high densities during 2011–2014. Species in this group might context. The ecological patterns in our study were dominated by have exhibited opportunistic responses to unpredictable food significant increases in densities of elpidiid holothurians when supply through heightened recruitment and immigration to the food availability was very high, following from very low or un- area, perhaps facilitated by their relatively small body size and detectable densities of these species during a period of moderate small size at juvenile recruitment. supply. While two non-elpidiid species showed significant in- creases in density, other families did not similarly exhibit unan- imously higher densities in 2011–2014 compared to 2006–2009. Acknowledgments Traits conferring ecological advantages to elpidiids during periods of high food supply, and conversely those that might limit max- This research was funded by the David and Lucile Packard imum densities of other species, are likely to be phylogenetically Foundation. L.L. was supported by the Monterey Bay Aquarium constrained (Eckelbarger and Watling, 1995). The ability of elpi- Research Institute Summer Internship Program. We thank the diids to select for (Iken et al., 2001) and monopolize consumption crew of the RV Western Flyer, and the pilots of ROVs Tiburon and of fresh phytodetritus (Wigham et al., 2003a,b) through increased Doc Ricketts for their continued support. This paper was improved feeding activity during high-food flux events (e.g. Kaufmann and by the constructive comments of Henry Ruhl and three anon- Smith (1997) and Bett et al. (2001)) leads to clear ecological ad- ymous reviewers. vantages (Billett and Hansen, 1982; Billett, 1991; Billett et al., 2010). Likewise their characteristic opportunistic reproductive strategies (Galley et al., 2008) involving small egg size (Hansen, 1975; Billett and Hansen, 1982; Tyler and Billett, 1988; Wigham Appendix A. Supplementary material et al., 2003b), potentially short-duration larval stages (Wigham et al., 2003b), small body size (Gebruk et al., 2003), and potentially Supplementary data associated with this article can be found in small size at recruitment (this study) might allow for accelerated the online version at doi:10.1016/j.dsr.2016.01.002. 38 C.L. Huffard et al. / Deep-Sea Research I 109 (2016) 27–39

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