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The natural diet of a hexactinellid sponge: Benthic–pelagic coupling in a deep-sea microbial food web
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Deep-Sea Research I 53 (2006) 1148–1156 www.elsevier.com/locate/dsr
The natural diet of a hexactinellid sponge: Benthic–pelagic coupling in a deep-sea microbial food web Adele J. Pilea,, Craig M. Youngb,c a
School of Biological Sciences (A08), University of Sydney, Sydney, NSW 2006, Australia b Harbor Branch Oceanographic Institution, Fort Pierce, FL 23062, USA c Oregon Institute of Marine Biology, 63466 Boat Basin Drive Charleston, OR 97420, USA
Received 21 July 2005; received in revised form 23 March 2006; accepted 26 March 2006 Available online 13 June 2006
Abstract Dense communities of shallow-water suspension feeders are known to sidestep the microbial loop by grazing on ultraplankton at its base. We quantified the diet, rates of water processing, and abundance of the deep-sea hexactinellid sponge Sericolophus hawaiicus, and found that, like their demosponge relatives in shallow water, hexactinellids are a significant sink for ultraplankton. S. hawaiicus forms a dense bed of sponges on the Big Island of Hawaii between 360 and 460 m depth, with a mean density of 4.7 sponges m2. Grazing of S. hawaiicus on ultraplankton was quantified from in situ samples using flow cytometry, and was found to be unselective. Rates of water processing were determined with dye visualization and ranged from 1.62 to 3.57 cm s1, resulting in a processing rate of 7.972.4 ml sponge1 s1. The large amount of water processed by these benthic suspension feeders results in the transfer of approximately 55 mg carbon and 7.3 mg N d1 m2 from the water column to the benthos. The magnitude of this flux places S. hawaiicus squarely within the functional group of organisms that link the pelagic microbial food web to the benthos. r 2006 Elsevier Ltd. All rights reserved. Keywords: Hexactinellid; Ultraplankton; Suspension feeding
1. Introduction Benthic suspension feeders in shallow marine ecosystems are capable of transferring large quantities of material from the overlying water column to the sea floor. For example, dense communities dominated by bivalves and corals can remove a large proportion of the particles larger than 5 mm from the water column (Glynn, 1973; Sorokin, 1973; Peterson and Black, 1987). The microbial commuCorresponding author.
E-mail address: [email protected] (A.J. Pile). 0967-0637/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2006.03.008
nity, which is now known to play a key role in planktonic food webs, is also an important source of food to benthic communities (Azam et al., 1983; Ayukai, 1995; reviewed by Gili and Coma, 1998). Hexactinellid or glass sponges are among the most common megafaunal organisms at bathyal and abyssal depths throughout the world’s oceans (Tabachnick, 1994). Dense bands of hexactinellids are dominant features of the continental slopes off Europe (Rice et al., 1990), Morocco (Barthel et al., 1996), and the Antarctic (Barthel et al., 1991). Aspects of physiology (Mackei et al., 1983; Leys, 1995; Leys and Mackie, 1997; Leys and Lauzon,
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1998) and reproduction (Boury-Ensault et al., 1999) have been studied in a few hexactinellids that extend up to SCUBA depths; but overall, we know very little about the physiology, reproduction, or ecological relationships of the common hexactinellids at bathyal depths. Like their demosponge relatives (Reiswig, 1971; Pile et al., 1996, 1997; Ribes et al., 1999), hexactinellids may use ultraplankton as their primary food source (Reiswig, 1990; Wyeth et al., 1996). Because modern hexactinellids live mostly below the euphotic zone, in a region where bacterioplankton and protozoans are the most common midwater organisms, bacterivory would be an appropriate strategy. We have recently discovered a dense and discrete band of hexactinellid sponges between 360 and 460 m depths off Kona, Hawaii. A recently described species, Sericolophus hawaiicus (Tabachnick and Levi, 2000), dominated this assemblage. S. hawaiicus has the general shape of an arum lily, with the proximal end of the organism anchored in the sediment by a thick rope of very long (up to 50 cm) glass spicules (Fig. 1A). The distal portion is
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bilaterally symmetrical with the body folded outward, the exhalent surface forming a shallow, expanded concavity (rather than the lining of an internal chamber, which is typical for most sponges), and the inhalent side forming an umbrella-like feeding surface. In the population we studied, virtually all individuals were oriented into the prevailing current. Details of orientation and spatial distribution will be described in a separate paper. The discrete vertical distribution of this species is dramatic, and we undertook the present study on feeding mechanisms as a step toward determining the potential cause of this distribution. Specifically, we investigated whether ultraplankton are an important food source for these sponges.
2. Materials and methods Sponge-mediated carbon and nitrogen fluxes were estimated conservatively by a modified version of the general model for organism-mediated flux (Pile
Figure 1. Drawings of Sericolophus hawaiicus, the sucker, and its use. (A) Drawing depicting the exhalent surface of S. hawaiicus with an expanded oscular area where water exits the sponge. There is a fine net over the oscular area, presumably to prevent debris from entering the aquiferous system. (B) Photograph of the sucker in position after having taken simultaneous water sample from the exhalent pocket of the sponge and near by ambient water. (C) Diagram of the sucker.
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et al., 1996): organismmediated flux Dwatercolumn property ¼ vol: processed ðvol: processed=pumping unitÞ time number of pumping units , m2
ð1Þ
where the water-column property is the cell count of ultraplankton, volume processed is in l, and pumping unit is one full-sized S. hawaiicus. This model requires the collection of three kinds of information at similar temporal and spatial scales; (1) sponge retention of ultraplankton (measured by comparing upstream and downstream ultraplankton abundance by flow cytometry), (2) instantaneous sponge pumping rate (measured by dye transit through the sponge), and (3) sponge abundance (determined by quantitative analysis of video transects). The in situ work was accomplished with Pisces V submersible on the leeward slope of the Mauna Loa volcano, off Kona, Hawaii (190 32.6421 N 150 0.2151W), between 30 November and 8 December 2001. 2.1. Retention of ultraplankton by sponges Paired water samples (n ¼ 20) were collected simultaneously from the exhalent current and the ambient water upstream with a portable device, which we referred to as ‘‘the sucker’’ (Figs. 1B and C). The sucker is a two-pronged fork made of welded aluminum pipe that holds a spring-loaded 5ml syringe at the end of each prong. One manipulator arm was used to carefully position one of the syringes within the exhalent pocket of the sponge, with the other syringe immediately upcurrent on the opposite side of the sponge. A pin pulled by the second manipulator arm released the springs, causing water to be drawn quickly and simultaneously into both syringes. Syringes were rinsed with 10% p-formaldehyde prior to the dive and 0.01 ml remained in the very tip of each syringe to preserve the samples in situ after collection. Upon returning to the surface, samples were preserved for flow cytometry according to standard protocols (Pile et al., 1996). Four paired samples, the maximum that could be carried on the submersible, were collected on 1, 2, 3, 7, and 8 December 2001.
Ultraplankton populations were quantified with a Becton Dickson FACSCalibur flow cytometer at The Centaury Institute, Sydney, Australia, following the techniques of Marie et al. (1997). Yellowgreen fluorescent microspheres (0.95 mm diameter beads, Molecular Probes) were added to each sample at a final concentration of 239 beads 50 ml1 as both an indicator of volume processed and as an internal reference. Samples were run such that the event rate was below 1000 cells s1 to avoid coincidence, and the duration of the run was determined by gating on the beads. Runs ceased when bead count was 239. Orange fluorescence (from phycoerythrin), red fluorescence (from chlorophyll), and green fluorescence (from DNA stained with SYBR Green) were collected through band-pass interference filters at 650, 585, and 530 nm, respectively. The five measured parameters (forward- and rightangle light scatter (FALS and RALS), orange, red, and green fluorescence) were recorded on fourdecade logarithmic scales, sorted in list mode, and analyzed with CYTOWIN, a custom-designed software (Vaulot, 1989). After processing, nine paired samples were found to contain sponge cells or sediment, possibly indicating improper placement of the syringes by the manipulator arm. In order to assure conservative estimates of food consumption, we removed these potentially artefactual samples from the data set. Ultraplankton populations were identified to four general cell types: bacteria, Prochlorococcus sp., Synechococcus-type cyanobacteria, and phototrophic eukaryotes 43 mm. Cell types were visually confirmed, and mean cell diameters were measured (n ¼ 50) by epifluorescence microscopy after staining with Hoechsts 33342 (final concentration 0.45 mg ml1). Differences between cell counts from upstream and exhalent current water (n ¼ 11) of each type of ultraplankton were analyzed by paired t-tests with a Bonferroni-transformed experimentwise a of 0.01 to determine the effect of S. hawaiicus on ultraplankton (Zar, 1984). The mean feeding efficiency for each sponge was calculated as ((mean cell count ambientmean cell count exhalent)/mean cell count ambient) 100 for each type of ultraplankton (Pile et al., 1996). Differences in retention efficiencies between types of ultraplankton were tested with analysis of variance models after homogeneity of variance was checked by Levine’s test (Zar, 1984). A conservative estimate of ultraplankton food consumed was obtained by converting the mean number of ultraplankton cells removed to an
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equivalent mass of C and N. For heterotrophic bacteria, we used a cell-to-carbon conversion factor of 20 fg C cell1 with a C/N ratio of 3.5 (Wheeler and Kirchman, 1986). For the photosynthetic prokaryotes, Prochlorococcus sp. and Synechococcus-type cyanobacteria, we used a cell conversion factor for carbon of 46 and 470 fg cell1 (Campbell et al., 1994; Bertilsson et al., 2003) and for nitrogen of 9.4 and 35 fg cell1 (Bertilsson et al., 2003). Carbon and nitrogen conversions for photosynthetic eukaryotes o3 mm were calculated based on the mean biovolume (5.13 mm3), where pg C cell1 is equal to 0.109 V0.991 and pg N cell1 is equal to 0.0172 V1.023 (Montagnes et al., 1994). These conversion factors have been used for cells with mean diameters that are equal to or greater than those found during this study (Ducklow et al., 1993). We are aware of the limitations of such calculations and have presented the consumption and flux data in such a way that the values can be recalculated, should better conversion values for these cell types become available. We would like to know if S. hawaiicus grazes selectively on any components of the plankton community. Selectivity indices require an estimate of the probability that a particle in a given size category will be retained by the filtering apparatus and ingested (Vanderploeg and Scavia, 1979). This is generally calculated empirically from microscopic measurements of the filtering apparatus, but such measurements are unavailable for S. hawaiicus. Therefore, to determine if S. hawaiicus grazes selectively on any portion of the plankton community, the percentage of carbon in the diet of the sponges was compared to the percentage of carbon in the plankton using a Kolmogorov–Smirnov twosample test (Pile et al., 1996). 2.2. Instantaneous sponge pumping rate Excurrent flow velocity was measured with dyerelease experiments conducted on five S. hawaiicus. Fluorescein dye was released from a 50-ml syringe on the upstream side of the sponge. Dye plumes issuing from the oral surface of the sponge were videotaped with a Sony digital video camera mounted on the submersible in a plane perpendicular to the orientation of the sponge. Two parallel lasers were mounted on the camera, 15.25 cm apart for scale. Velocity of the current was determined using frame-by-frame video analysis following the techniques of Savarese et al. (1997).
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Volume flux was empirically calculated as Q ¼ uA, where Q is the volume flow (ml s1), u is velocity (cm s1), and A is the oscular area (cm2). The multiple oscula are positioned mostly in the center indentation of the sponge (Fig. 1). The area of this indentation was measured from the videotape. Examination of preserved specimens indicates that nearly 50% of the area consists of oscular openings, but we made our estimates more conservative by assuming that only one-third of the indentation area would serve as oscular area. Our estimate of volume processed is based on a plugflow model, in which the velocity profile of the exhalent current is rectangular rather than a laminar pipe flow with a parabolic velocity profile. This model is appropriate for the shape of the exhalent current in ascidians (Fiala-Medioni, 1973, 1978), and most likely for sponges as well (Savarese et al., 1997). As we had no data on the temporal patterns of feeding in this species, we assumed conservatively that the sponges process water at the measured instantaneous rates for only 12 h d1 (Pile et al., 1996). Tropical, boreal, and temperate demosponges can have variable water-processing rates over a diel cycle (Reiswig, 1974; Pile et al., 1996, 2003; Savarese et al., 1997). Comparisons of instantaneous rate measurements with longer records indicate that the volume processed calculated from a 12-h instantaneous rate is comparable to the volume processed computed from a 24-h pumping record (Pile, unpublished data). 2.3. Sponge abundance Density of S. hawaiicus within its discrete zone of high density was determined from 12 horizontal video transects by the Pisces V submersible and RCV 150 ROV. All animals in every contiguous video field (n450 in each transect) were counted, and field sizes were calibrated by parallel laser dots. 3. Results 3.1. Sponge retention of ultraplankton Sponges significantly reduced the abundance of all types of ultraplankton (Fig. 2). Concentrations of bacteria (Student’s paired t-test t10 ¼ 9:75), Prochlorococcus sp. (Student’s paired t-test t10 ¼ 5:68), Synechococcus-type cyanobacteria (Student’s paired t-test t10 ¼ 8:44), and photosynthetic eukaryotes o3 mm (Student’s paired t-test
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streams from the oscula within the exhalent pocket of the sponge. The velocity of the exhalent current from exhalent pocket ranged from 1.62 to 3.57 cm s1 with an average velocity of 2.23(70.77 s.d.) cm s1. The average volume processed by large S. hawaiicus was 7.94(72.44) ml sponge1 s1.
7 ambient exhalent
6
Mean 105 cells ml-1
5 4
3.3. Sponge abundance 3 2 1 0
(A)
Bacteria
Prochlorococcus Synechococcus
Picoeucaryotes
Mean retention efficiency (%)
100
80
60
40
3.4. Sponge-mediated fluxes
20
This dense bed of S. hawaiicus is responsible for a flux of at least 55 mg C d1 m2 and 7.3 mg N d1 m2 from the water column (Table 1). Most of the carbon (64%) and much of the nitrogen (36%) is supplied by Synechococcus-type cyanobacteria, even though these make up only about 10% of the ultraplankton population by number. Bacteria, which are the numerical dominants of the ultraplankton, are nitrogen rich and constitute the other major contributor to the nitrogen flux. Prochlorococcus sp. makes lesser contributions to the carbon and nitrogen flux than the other two prokaryotes. Compared to the contribution of prokaryotes, carbon and nitrogen fluxes of photosynthetic eukaryotes o3 mm are minor, contributing only 8% of the total carbon and 9% of the total nitrogen flux. These fluxes are not statistically different from the ratio of carbon and nitrogen available within the water-column community (Kolmogorov–Smirnov two-sample test, D4;4 ¼ 32, po0:01), indicating that S. hawaiicus does not graze selectively.
0 Bacteria
(B)
The sponges were found primarily in areas of sediment between fingers of basaltic rock that ran down the slope perpendicular to the island. Sponge densities were calculated only for the sedimented areas; the rocky fingers, where sponges were rare, were not included since they did not represent part of the sponge habitat. Large S. hawaiicus occurred at a mean density of 4.7(70.36 s.d.) sponges m2. Although there were also small sponges in some quadrats, these were not included in the estimate, because we had no empirical data on pumping rates or removal of ultraplankton by animals of this size.
Prochlorococcus Synechococcus
Picoeucaryotes
Type of ultraplankton
Figure 2. Effect of Sericolophus hawaiicus on ultraplankton: (A) concentration of each type of ultraplankton in the ambient water and water from the exhalent surface of the hexactinellid sponge S. hawaiicus, and (B) feeding efficiencies. (a) Mean cell concentrations of ambient water and water from the exhalent surface. All sponges significantly reduced concentrations of all types of ultraplankton. White bars denote ambient water (n ¼ 11) and black bars denote water from the exhalent surface (n ¼ 11), while the error bars are one s.d. (b) Polled feeding efficiencies of all the sponges (n ¼ 11) on ultraplankton. There were no statistical differences between the efficiencies and error bars are one s.d.
t10 ¼ 16:21) in water collected from the exhalent pocket were significantly lower than ambient concentrations. There were no differences among the retention efficiencies of the various kinds of ultraplankton (ANOVA, F 3;43 ¼ 0:191, p ¼ 0:906), which ranged from 47% for bacteria to 54% for autotrophic eukaryotes o3 mm. 3.2. Instantaneous pumping rates of sponges Even when large clouds of dye were released over a sponge, dye was only seen exiting in well-defined
4. Discussion As is typical for shallow-water demosponges, the bathyal hexactinellid S. hawaiicus feeds on ultraplankton. This is not unexpected, as laboratory studies (Wyeth et al., 1996) and field sampling
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Table 1 Mean flux of the various types of ultraplankton by Sericolophus hawaiicus Cell type
Prokaryotes Bacteria Prochlorococcus sp. Synechococcus sp. Eukaryotes Autotrophic eukaryotes o3 mm Total
Mean 103 cells available (ml1)
Mean 103 cells retained (ml1)
Carbon flux (mg C day1 m2)
Nitrogen flux (mg N day1 m2)
464 (72) 111 (17) 62 (10)
309 (71) 76 (17) 47 (11)
10.0 (18) 6.0 (10) 35.0 (64)
2.8 (39) 1.2 (16) 2.6 (36)
8 (1)
5 (1)
4.0 (8) 55
0.7 (9) 7.3
Standard cell-to-carbon conversion factors were used to empirically calculate carbon and nitrogen values. Values in parentheses represent the percentage of the total available.
(Reiswig, 1990) of much shallower hexactinellid sponges in the sounds and fjords of British Columbia, Canada, suggested that bacteria are a likely food item for this group. However, the present study is the first investigation of the natural diet of a hexactinellid sponge. Like shallow-water demosponges, S. hawaiicus appear to graze unselectively on ultraplankton (Reiswig, 1971; Pile et al., 1996, 1997). Retention efficiencies of these hexactinellids are lower than those of demosponges that have been investigated. Demosponges typically have retention efficiencies between 95% and 99% on all types of ultraplankton (Reiswig, 1971; Pile et al., 1996, 1997). We measured retention efficiencies between 47% and 54% for S. hawaiicus on the same types of plankton by similar analytical techniques. The three types of phototrophic ultraplankton we found in the diet of S. hawaiicus would not normally be expected at the depth where these sponge populations occur, because of low light levels and slow sinking rates. In some regions, phototrophic ultraplankton are carried to similar depths by the decaying fecal pellets of grazing salps (Lochte and Turley, 1988; Graf, 1989; Pfannkuche and Lochte, 1993). However, we believe that the deep occurrence of phototrophic ultraplankton off Kona can be explained by the interaction of several oceanographic processes. First, phototrophic ultraplankton occur at relatively great depths in Hawaiian waters because of the unusual clarity of the water. The chlorophyll maximum surrounding the Hawaiian Islands is generally below 100 m, and the Synechococcus and Prochlorococcus maxima may be as deep as 150 m, with cells found as deep as 200 m (Campbell and Vaulot, 1993). Second, there is
a consistent downwelling current at the depth of the sponges directly off Kona. We have observed this prevailing downslope current repeatedly during sponge dives, and its prevalence is revealed by the consistent upslope orientation of virtually all planar cnidarians as well as the hexactinellid sponges themselves. It appears likely that the phototrophic ultraplankton are carried downward at surface abundances by the water masses that are deflected downward at this point of the Kona Coast. These omnivorous sponges graze nonselectively on ultraplankton, consuming both heterotrophic and phototrophic organisms. In general, the lower C:N ratio of heterotrophs makes them excellent sources of nitrogen (Geider and LaRoche, 2002; Bertilsson et al., 2003), whereas the larger phototrophs are better sources of carbon. Clearly, the nutritional composition of ultraplankton will change seasonally. In other deep-sea sponges, this variation may drive seasonal reproduction (Witte, 1996). Water-processing rates by S. hawaiicus are within the range measured for shallow-water demosponges. Freshwater sponges in Lake Baikal have instantaneous pumping velocities between 0.2 and 3.3 cm s1 (Savarese et al., 1997). Mycale lingua, a boreal marine demosponge species, has an instantaneous velocity of 14.0 cm s1, whereas the range for three species of tropical marine demosponges is 7.3–14.6 cm s1 (Reiswig, 1974; Pile et al., 1996). In shallow-water systems, sponge communities may be capable of completely filtering the overlying water column on a daily basis (Reiswig, 1974; Pile et al., 1997). As hexactinellid sponge communities are limited to greater depths, it is highly unlikely that they will impact the entire overlying water column,
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but they can have a substantial impact on the concentration of plankton in the benthic boundary layer (Buss and Jackson, 1981; Peterson and Black, 1987; Pile et al., 1997). The large amount of ultraplankton removed by S. hawaiicus makes this species an important component of the functional group that links the pelagic microbial food web to the benthos. The number of macroinvertebrates that have been shown to sidestep the microbial loop and directly utilize the base of the microbial food web as a primary food source is evergrowing, and currently includes demosponges, ascidians, soft corals, and bivalves (see review by Gili and Coma, 1998). We are aware of only one other deep-sea organism that has been shown empirically to retain ultraplankton, the cold seep mussel Bathymodiolus childressi (Pile and Young, 1999). However, suspension feeders are not uncommon at slope and abyssal depths, particularly in areas of accelerated flow such as rocks and seamounts, so it is likely that many deepsea demosponges, bivalves, and ascidians graze on ultraplankton. Dense macroinvertebrate communities dominated by demosponges (Pile et al., 1996, 1997) and corals (Ayukai, 1995) in shallow water have been shown to remove as much as 90% of the ultraplankton from the water that passes over them. The daily fluxes of ultraplankton to these communities range from 9 to 1970 mg C d1 m2. We estimate conservatively that the bed of S. hawaiicus off Kona, Hawaii, is responsible for the flux of 55 mg C d1 m2, which places it in the range of shallow-water tropical systems (Reiswig, 1974; Ayukai, 1995). Fluxes in temperate and boreal systems are even higher (Pile et al., 1996, 1997), most likely because of higher productivity of the pelagic ecosystems in these regions. Unfortunately, flow cytometry is not a reliable tool for quantification of rare plankton such as larger phytoplankton cells, and we were unable to determine their role in hexactinellid nutrition. However, larger cells are unlikely to be consumed by sponges. The only documented case of sponges phagocytizing cells larger than 5 mm occurred in the shallow Antarctic and was the result of a settling bloom of diatoms (Gaino et al., 1994). Clearly, shallow-water sponge communities are significant sinks for particulate organic material (POM) and have recently been shown to be net sinks for dissolved organic carbon (DOC) as well (Yahel et al., 2003). Hexactinellids may also be able to remove DOC from the water column, and further investigation into the roles
POM and DOC in meeting the sponges’ nutritional needs are merited. There are two potential sources of food for suspension-feeding organisms in the deep sea. The focus in the past has been on the role of vertical particle flux in the form of detritus from the euphotic zone as the primary source of food for deep-sea organisms (see review by Graf, 1992). However, much of the particulate carbon is in the ultraplankton fraction (Sherr and Sherr, 1991). It is difficult to find these cells in sediment traps unless they are incorporated into large detritus particles such as fecal pellets (Lochte and Turley, 1988; Pfannkuche and Lochte, 1993). In addition, it is now generally accepted that ultraplankton can support dense communities of suspension-feeding macroinvertebrates in shallow water (see review by Gili and Coma, 1998). Ultraplankton can be found in the deep sea either as resident plankton communities (Wishner, 1980; Karl and Knauer, 1984; Graf, 1989; Pile and Young, 1999) or as cells displaced from the surface by oceanographic processes (Witman et al., 1993). Our data clearly show that dense beds of hexactinellids are capable of moving large amounts of ultraplankton from the pelagic community to the benthos and that these sponges are most likely dependent nutritionally on ultraplankton. Downwelling waters are probably responsible for maintaining this community off Kona. However, in other parts of the deep sea, where downwelling may not be present, the role of resident ultraplankton in maintaining deep-sea suspension-feeding communities, such as demosponges and corals, remains to be examined.
Acknowledgments We are grateful to the captain and crew of the R./ V. Ka’imikai-o-Kanaloa, and the pilots and crew of the Pisces V submersible for their assistance in collecting the in situ data. S. Arellano, S. Brooke, C. Mah, M. Maldanado, T. Prowse, H. Reiswig, J. Watanabe, and M. Wood participated in the fieldwork. Research was supported by funds from the Hawaii Undersea Research Laboratory (National Undersea Research Program of NOAA) to CMY and AJP, as well as the Australian Research Council and University of Sydney Research funds to AJP.
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in Sponge Biology. Smithsonian Institution Press, Washington, DC, pp. 504–510. Ribes, M., Coma, R., Gili, J.M., 1999. Natural diet and grazing rate of the temperate sponge Dysidea avara (Demospongiae, Dendrocertida) throughout an annual cycle. Marine Ecology Progress Series 176, 179–190. Rice, A.L., Thurston, M.H., New, A.L., 1990. Dense aggregations of hexactinellid sponge, Pheronema carpenteri, in the Porcupine Seabight (northeast Atlantic Ocean) and possible causes. Progress in Oceanography 24, 179–196. Savarese, M., Patterson, M.R., Chernykh, V.I., Fialkov, V.A., 1997. Trophic effects of sponge feeding within Lake Baikal’s littoral zone. 1. In situ pumping rates. Limnology and Oceanography 42, 171–178. Sherr, E.B., Sherr, B.F., 1991. Planktonic microbes, Tiny cells at the base of the ocean’s food webs. Trends in Ecology and Evolution 6, 50–54. Sorokin, Y.I., 1973. Trophical role of bacteria in the ecosystem of the coral reef. Science 242, 415–417. Tabachnick, K.R., 1994. Distribution of recent Hexactinellida. In: van Soest, R., van Kempen, B., Braekman, G. (Eds.), Sponges in Time and Space. Balkema, Rotterdam, pp. 225–232. Tabachnick, K.R., Levi, C., 2000. Porifera Hexactinellida, Amphidoscophora, off New Caledonia. Re´sultats des Campagnes MUSORSTOM, vol. 21(184). Me´moires du Muse´um national d’Histoire naturelle (France), Paris, pp. 53–140.
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Deep-Sea Research I 53 (2006) 1148–1156 www.elsevier.com/locate/dsr
The natural diet of a hexactinellid sponge: Benthic–pelagic coupling in a deep-sea microbial food web Adele J. Pilea,, Craig M. Youngb,c a
School of Biological Sciences (A08), University of Sydney, Sydney, NSW 2006, Australia b Harbor Branch Oceanographic Institution, Fort Pierce, FL 23062, USA c Oregon Institute of Marine Biology, 63466 Boat Basin Drive Charleston, OR 97420, USA
Received 21 July 2005; received in revised form 23 March 2006; accepted 26 March 2006 Available online 13 June 2006
Abstract Dense communities of shallow-water suspension feeders are known to sidestep the microbial loop by grazing on ultraplankton at its base. We quantified the diet, rates of water processing, and abundance of the deep-sea hexactinellid sponge Sericolophus hawaiicus, and found that, like their demosponge relatives in shallow water, hexactinellids are a significant sink for ultraplankton. S. hawaiicus forms a dense bed of sponges on the Big Island of Hawaii between 360 and 460 m depth, with a mean density of 4.7 sponges m2. Grazing of S. hawaiicus on ultraplankton was quantified from in situ samples using flow cytometry, and was found to be unselective. Rates of water processing were determined with dye visualization and ranged from 1.62 to 3.57 cm s1, resulting in a processing rate of 7.972.4 ml sponge1 s1. The large amount of water processed by these benthic suspension feeders results in the transfer of approximately 55 mg carbon and 7.3 mg N d1 m2 from the water column to the benthos. The magnitude of this flux places S. hawaiicus squarely within the functional group of organisms that link the pelagic microbial food web to the benthos. r 2006 Elsevier Ltd. All rights reserved. Keywords: Hexactinellid; Ultraplankton; Suspension feeding
1. Introduction Benthic suspension feeders in shallow marine ecosystems are capable of transferring large quantities of material from the overlying water column to the sea floor. For example, dense communities dominated by bivalves and corals can remove a large proportion of the particles larger than 5 mm from the water column (Glynn, 1973; Sorokin, 1973; Peterson and Black, 1987). The microbial commuCorresponding author.
E-mail address: [email protected] (A.J. Pile). 0967-0637/$ - see front matter r 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.dsr.2006.03.008
nity, which is now known to play a key role in planktonic food webs, is also an important source of food to benthic communities (Azam et al., 1983; Ayukai, 1995; reviewed by Gili and Coma, 1998). Hexactinellid or glass sponges are among the most common megafaunal organisms at bathyal and abyssal depths throughout the world’s oceans (Tabachnick, 1994). Dense bands of hexactinellids are dominant features of the continental slopes off Europe (Rice et al., 1990), Morocco (Barthel et al., 1996), and the Antarctic (Barthel et al., 1991). Aspects of physiology (Mackei et al., 1983; Leys, 1995; Leys and Mackie, 1997; Leys and Lauzon,
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1998) and reproduction (Boury-Ensault et al., 1999) have been studied in a few hexactinellids that extend up to SCUBA depths; but overall, we know very little about the physiology, reproduction, or ecological relationships of the common hexactinellids at bathyal depths. Like their demosponge relatives (Reiswig, 1971; Pile et al., 1996, 1997; Ribes et al., 1999), hexactinellids may use ultraplankton as their primary food source (Reiswig, 1990; Wyeth et al., 1996). Because modern hexactinellids live mostly below the euphotic zone, in a region where bacterioplankton and protozoans are the most common midwater organisms, bacterivory would be an appropriate strategy. We have recently discovered a dense and discrete band of hexactinellid sponges between 360 and 460 m depths off Kona, Hawaii. A recently described species, Sericolophus hawaiicus (Tabachnick and Levi, 2000), dominated this assemblage. S. hawaiicus has the general shape of an arum lily, with the proximal end of the organism anchored in the sediment by a thick rope of very long (up to 50 cm) glass spicules (Fig. 1A). The distal portion is
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bilaterally symmetrical with the body folded outward, the exhalent surface forming a shallow, expanded concavity (rather than the lining of an internal chamber, which is typical for most sponges), and the inhalent side forming an umbrella-like feeding surface. In the population we studied, virtually all individuals were oriented into the prevailing current. Details of orientation and spatial distribution will be described in a separate paper. The discrete vertical distribution of this species is dramatic, and we undertook the present study on feeding mechanisms as a step toward determining the potential cause of this distribution. Specifically, we investigated whether ultraplankton are an important food source for these sponges.
2. Materials and methods Sponge-mediated carbon and nitrogen fluxes were estimated conservatively by a modified version of the general model for organism-mediated flux (Pile
Figure 1. Drawings of Sericolophus hawaiicus, the sucker, and its use. (A) Drawing depicting the exhalent surface of S. hawaiicus with an expanded oscular area where water exits the sponge. There is a fine net over the oscular area, presumably to prevent debris from entering the aquiferous system. (B) Photograph of the sucker in position after having taken simultaneous water sample from the exhalent pocket of the sponge and near by ambient water. (C) Diagram of the sucker.
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et al., 1996): organismmediated flux Dwatercolumn property ¼ vol: processed ðvol: processed=pumping unitÞ time number of pumping units , m2
ð1Þ
where the water-column property is the cell count of ultraplankton, volume processed is in l, and pumping unit is one full-sized S. hawaiicus. This model requires the collection of three kinds of information at similar temporal and spatial scales; (1) sponge retention of ultraplankton (measured by comparing upstream and downstream ultraplankton abundance by flow cytometry), (2) instantaneous sponge pumping rate (measured by dye transit through the sponge), and (3) sponge abundance (determined by quantitative analysis of video transects). The in situ work was accomplished with Pisces V submersible on the leeward slope of the Mauna Loa volcano, off Kona, Hawaii (190 32.6421 N 150 0.2151W), between 30 November and 8 December 2001. 2.1. Retention of ultraplankton by sponges Paired water samples (n ¼ 20) were collected simultaneously from the exhalent current and the ambient water upstream with a portable device, which we referred to as ‘‘the sucker’’ (Figs. 1B and C). The sucker is a two-pronged fork made of welded aluminum pipe that holds a spring-loaded 5ml syringe at the end of each prong. One manipulator arm was used to carefully position one of the syringes within the exhalent pocket of the sponge, with the other syringe immediately upcurrent on the opposite side of the sponge. A pin pulled by the second manipulator arm released the springs, causing water to be drawn quickly and simultaneously into both syringes. Syringes were rinsed with 10% p-formaldehyde prior to the dive and 0.01 ml remained in the very tip of each syringe to preserve the samples in situ after collection. Upon returning to the surface, samples were preserved for flow cytometry according to standard protocols (Pile et al., 1996). Four paired samples, the maximum that could be carried on the submersible, were collected on 1, 2, 3, 7, and 8 December 2001.
Ultraplankton populations were quantified with a Becton Dickson FACSCalibur flow cytometer at The Centaury Institute, Sydney, Australia, following the techniques of Marie et al. (1997). Yellowgreen fluorescent microspheres (0.95 mm diameter beads, Molecular Probes) were added to each sample at a final concentration of 239 beads 50 ml1 as both an indicator of volume processed and as an internal reference. Samples were run such that the event rate was below 1000 cells s1 to avoid coincidence, and the duration of the run was determined by gating on the beads. Runs ceased when bead count was 239. Orange fluorescence (from phycoerythrin), red fluorescence (from chlorophyll), and green fluorescence (from DNA stained with SYBR Green) were collected through band-pass interference filters at 650, 585, and 530 nm, respectively. The five measured parameters (forward- and rightangle light scatter (FALS and RALS), orange, red, and green fluorescence) were recorded on fourdecade logarithmic scales, sorted in list mode, and analyzed with CYTOWIN, a custom-designed software (Vaulot, 1989). After processing, nine paired samples were found to contain sponge cells or sediment, possibly indicating improper placement of the syringes by the manipulator arm. In order to assure conservative estimates of food consumption, we removed these potentially artefactual samples from the data set. Ultraplankton populations were identified to four general cell types: bacteria, Prochlorococcus sp., Synechococcus-type cyanobacteria, and phototrophic eukaryotes 43 mm. Cell types were visually confirmed, and mean cell diameters were measured (n ¼ 50) by epifluorescence microscopy after staining with Hoechsts 33342 (final concentration 0.45 mg ml1). Differences between cell counts from upstream and exhalent current water (n ¼ 11) of each type of ultraplankton were analyzed by paired t-tests with a Bonferroni-transformed experimentwise a of 0.01 to determine the effect of S. hawaiicus on ultraplankton (Zar, 1984). The mean feeding efficiency for each sponge was calculated as ((mean cell count ambientmean cell count exhalent)/mean cell count ambient) 100 for each type of ultraplankton (Pile et al., 1996). Differences in retention efficiencies between types of ultraplankton were tested with analysis of variance models after homogeneity of variance was checked by Levine’s test (Zar, 1984). A conservative estimate of ultraplankton food consumed was obtained by converting the mean number of ultraplankton cells removed to an
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equivalent mass of C and N. For heterotrophic bacteria, we used a cell-to-carbon conversion factor of 20 fg C cell1 with a C/N ratio of 3.5 (Wheeler and Kirchman, 1986). For the photosynthetic prokaryotes, Prochlorococcus sp. and Synechococcus-type cyanobacteria, we used a cell conversion factor for carbon of 46 and 470 fg cell1 (Campbell et al., 1994; Bertilsson et al., 2003) and for nitrogen of 9.4 and 35 fg cell1 (Bertilsson et al., 2003). Carbon and nitrogen conversions for photosynthetic eukaryotes o3 mm were calculated based on the mean biovolume (5.13 mm3), where pg C cell1 is equal to 0.109 V0.991 and pg N cell1 is equal to 0.0172 V1.023 (Montagnes et al., 1994). These conversion factors have been used for cells with mean diameters that are equal to or greater than those found during this study (Ducklow et al., 1993). We are aware of the limitations of such calculations and have presented the consumption and flux data in such a way that the values can be recalculated, should better conversion values for these cell types become available. We would like to know if S. hawaiicus grazes selectively on any components of the plankton community. Selectivity indices require an estimate of the probability that a particle in a given size category will be retained by the filtering apparatus and ingested (Vanderploeg and Scavia, 1979). This is generally calculated empirically from microscopic measurements of the filtering apparatus, but such measurements are unavailable for S. hawaiicus. Therefore, to determine if S. hawaiicus grazes selectively on any portion of the plankton community, the percentage of carbon in the diet of the sponges was compared to the percentage of carbon in the plankton using a Kolmogorov–Smirnov twosample test (Pile et al., 1996). 2.2. Instantaneous sponge pumping rate Excurrent flow velocity was measured with dyerelease experiments conducted on five S. hawaiicus. Fluorescein dye was released from a 50-ml syringe on the upstream side of the sponge. Dye plumes issuing from the oral surface of the sponge were videotaped with a Sony digital video camera mounted on the submersible in a plane perpendicular to the orientation of the sponge. Two parallel lasers were mounted on the camera, 15.25 cm apart for scale. Velocity of the current was determined using frame-by-frame video analysis following the techniques of Savarese et al. (1997).
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Volume flux was empirically calculated as Q ¼ uA, where Q is the volume flow (ml s1), u is velocity (cm s1), and A is the oscular area (cm2). The multiple oscula are positioned mostly in the center indentation of the sponge (Fig. 1). The area of this indentation was measured from the videotape. Examination of preserved specimens indicates that nearly 50% of the area consists of oscular openings, but we made our estimates more conservative by assuming that only one-third of the indentation area would serve as oscular area. Our estimate of volume processed is based on a plugflow model, in which the velocity profile of the exhalent current is rectangular rather than a laminar pipe flow with a parabolic velocity profile. This model is appropriate for the shape of the exhalent current in ascidians (Fiala-Medioni, 1973, 1978), and most likely for sponges as well (Savarese et al., 1997). As we had no data on the temporal patterns of feeding in this species, we assumed conservatively that the sponges process water at the measured instantaneous rates for only 12 h d1 (Pile et al., 1996). Tropical, boreal, and temperate demosponges can have variable water-processing rates over a diel cycle (Reiswig, 1974; Pile et al., 1996, 2003; Savarese et al., 1997). Comparisons of instantaneous rate measurements with longer records indicate that the volume processed calculated from a 12-h instantaneous rate is comparable to the volume processed computed from a 24-h pumping record (Pile, unpublished data). 2.3. Sponge abundance Density of S. hawaiicus within its discrete zone of high density was determined from 12 horizontal video transects by the Pisces V submersible and RCV 150 ROV. All animals in every contiguous video field (n450 in each transect) were counted, and field sizes were calibrated by parallel laser dots. 3. Results 3.1. Sponge retention of ultraplankton Sponges significantly reduced the abundance of all types of ultraplankton (Fig. 2). Concentrations of bacteria (Student’s paired t-test t10 ¼ 9:75), Prochlorococcus sp. (Student’s paired t-test t10 ¼ 5:68), Synechococcus-type cyanobacteria (Student’s paired t-test t10 ¼ 8:44), and photosynthetic eukaryotes o3 mm (Student’s paired t-test
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streams from the oscula within the exhalent pocket of the sponge. The velocity of the exhalent current from exhalent pocket ranged from 1.62 to 3.57 cm s1 with an average velocity of 2.23(70.77 s.d.) cm s1. The average volume processed by large S. hawaiicus was 7.94(72.44) ml sponge1 s1.
7 ambient exhalent
6
Mean 105 cells ml-1
5 4
3.3. Sponge abundance 3 2 1 0
(A)
Bacteria
Prochlorococcus Synechococcus
Picoeucaryotes
Mean retention efficiency (%)
100
80
60
40
3.4. Sponge-mediated fluxes
20
This dense bed of S. hawaiicus is responsible for a flux of at least 55 mg C d1 m2 and 7.3 mg N d1 m2 from the water column (Table 1). Most of the carbon (64%) and much of the nitrogen (36%) is supplied by Synechococcus-type cyanobacteria, even though these make up only about 10% of the ultraplankton population by number. Bacteria, which are the numerical dominants of the ultraplankton, are nitrogen rich and constitute the other major contributor to the nitrogen flux. Prochlorococcus sp. makes lesser contributions to the carbon and nitrogen flux than the other two prokaryotes. Compared to the contribution of prokaryotes, carbon and nitrogen fluxes of photosynthetic eukaryotes o3 mm are minor, contributing only 8% of the total carbon and 9% of the total nitrogen flux. These fluxes are not statistically different from the ratio of carbon and nitrogen available within the water-column community (Kolmogorov–Smirnov two-sample test, D4;4 ¼ 32, po0:01), indicating that S. hawaiicus does not graze selectively.
0 Bacteria
(B)
The sponges were found primarily in areas of sediment between fingers of basaltic rock that ran down the slope perpendicular to the island. Sponge densities were calculated only for the sedimented areas; the rocky fingers, where sponges were rare, were not included since they did not represent part of the sponge habitat. Large S. hawaiicus occurred at a mean density of 4.7(70.36 s.d.) sponges m2. Although there were also small sponges in some quadrats, these were not included in the estimate, because we had no empirical data on pumping rates or removal of ultraplankton by animals of this size.
Prochlorococcus Synechococcus
Picoeucaryotes
Type of ultraplankton
Figure 2. Effect of Sericolophus hawaiicus on ultraplankton: (A) concentration of each type of ultraplankton in the ambient water and water from the exhalent surface of the hexactinellid sponge S. hawaiicus, and (B) feeding efficiencies. (a) Mean cell concentrations of ambient water and water from the exhalent surface. All sponges significantly reduced concentrations of all types of ultraplankton. White bars denote ambient water (n ¼ 11) and black bars denote water from the exhalent surface (n ¼ 11), while the error bars are one s.d. (b) Polled feeding efficiencies of all the sponges (n ¼ 11) on ultraplankton. There were no statistical differences between the efficiencies and error bars are one s.d.
t10 ¼ 16:21) in water collected from the exhalent pocket were significantly lower than ambient concentrations. There were no differences among the retention efficiencies of the various kinds of ultraplankton (ANOVA, F 3;43 ¼ 0:191, p ¼ 0:906), which ranged from 47% for bacteria to 54% for autotrophic eukaryotes o3 mm. 3.2. Instantaneous pumping rates of sponges Even when large clouds of dye were released over a sponge, dye was only seen exiting in well-defined
4. Discussion As is typical for shallow-water demosponges, the bathyal hexactinellid S. hawaiicus feeds on ultraplankton. This is not unexpected, as laboratory studies (Wyeth et al., 1996) and field sampling
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Table 1 Mean flux of the various types of ultraplankton by Sericolophus hawaiicus Cell type
Prokaryotes Bacteria Prochlorococcus sp. Synechococcus sp. Eukaryotes Autotrophic eukaryotes o3 mm Total
Mean 103 cells available (ml1)
Mean 103 cells retained (ml1)
Carbon flux (mg C day1 m2)
Nitrogen flux (mg N day1 m2)
464 (72) 111 (17) 62 (10)
309 (71) 76 (17) 47 (11)
10.0 (18) 6.0 (10) 35.0 (64)
2.8 (39) 1.2 (16) 2.6 (36)
8 (1)
5 (1)
4.0 (8) 55
0.7 (9) 7.3
Standard cell-to-carbon conversion factors were used to empirically calculate carbon and nitrogen values. Values in parentheses represent the percentage of the total available.
(Reiswig, 1990) of much shallower hexactinellid sponges in the sounds and fjords of British Columbia, Canada, suggested that bacteria are a likely food item for this group. However, the present study is the first investigation of the natural diet of a hexactinellid sponge. Like shallow-water demosponges, S. hawaiicus appear to graze unselectively on ultraplankton (Reiswig, 1971; Pile et al., 1996, 1997). Retention efficiencies of these hexactinellids are lower than those of demosponges that have been investigated. Demosponges typically have retention efficiencies between 95% and 99% on all types of ultraplankton (Reiswig, 1971; Pile et al., 1996, 1997). We measured retention efficiencies between 47% and 54% for S. hawaiicus on the same types of plankton by similar analytical techniques. The three types of phototrophic ultraplankton we found in the diet of S. hawaiicus would not normally be expected at the depth where these sponge populations occur, because of low light levels and slow sinking rates. In some regions, phototrophic ultraplankton are carried to similar depths by the decaying fecal pellets of grazing salps (Lochte and Turley, 1988; Graf, 1989; Pfannkuche and Lochte, 1993). However, we believe that the deep occurrence of phototrophic ultraplankton off Kona can be explained by the interaction of several oceanographic processes. First, phototrophic ultraplankton occur at relatively great depths in Hawaiian waters because of the unusual clarity of the water. The chlorophyll maximum surrounding the Hawaiian Islands is generally below 100 m, and the Synechococcus and Prochlorococcus maxima may be as deep as 150 m, with cells found as deep as 200 m (Campbell and Vaulot, 1993). Second, there is
a consistent downwelling current at the depth of the sponges directly off Kona. We have observed this prevailing downslope current repeatedly during sponge dives, and its prevalence is revealed by the consistent upslope orientation of virtually all planar cnidarians as well as the hexactinellid sponges themselves. It appears likely that the phototrophic ultraplankton are carried downward at surface abundances by the water masses that are deflected downward at this point of the Kona Coast. These omnivorous sponges graze nonselectively on ultraplankton, consuming both heterotrophic and phototrophic organisms. In general, the lower C:N ratio of heterotrophs makes them excellent sources of nitrogen (Geider and LaRoche, 2002; Bertilsson et al., 2003), whereas the larger phototrophs are better sources of carbon. Clearly, the nutritional composition of ultraplankton will change seasonally. In other deep-sea sponges, this variation may drive seasonal reproduction (Witte, 1996). Water-processing rates by S. hawaiicus are within the range measured for shallow-water demosponges. Freshwater sponges in Lake Baikal have instantaneous pumping velocities between 0.2 and 3.3 cm s1 (Savarese et al., 1997). Mycale lingua, a boreal marine demosponge species, has an instantaneous velocity of 14.0 cm s1, whereas the range for three species of tropical marine demosponges is 7.3–14.6 cm s1 (Reiswig, 1974; Pile et al., 1996). In shallow-water systems, sponge communities may be capable of completely filtering the overlying water column on a daily basis (Reiswig, 1974; Pile et al., 1997). As hexactinellid sponge communities are limited to greater depths, it is highly unlikely that they will impact the entire overlying water column,
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but they can have a substantial impact on the concentration of plankton in the benthic boundary layer (Buss and Jackson, 1981; Peterson and Black, 1987; Pile et al., 1997). The large amount of ultraplankton removed by S. hawaiicus makes this species an important component of the functional group that links the pelagic microbial food web to the benthos. The number of macroinvertebrates that have been shown to sidestep the microbial loop and directly utilize the base of the microbial food web as a primary food source is evergrowing, and currently includes demosponges, ascidians, soft corals, and bivalves (see review by Gili and Coma, 1998). We are aware of only one other deep-sea organism that has been shown empirically to retain ultraplankton, the cold seep mussel Bathymodiolus childressi (Pile and Young, 1999). However, suspension feeders are not uncommon at slope and abyssal depths, particularly in areas of accelerated flow such as rocks and seamounts, so it is likely that many deepsea demosponges, bivalves, and ascidians graze on ultraplankton. Dense macroinvertebrate communities dominated by demosponges (Pile et al., 1996, 1997) and corals (Ayukai, 1995) in shallow water have been shown to remove as much as 90% of the ultraplankton from the water that passes over them. The daily fluxes of ultraplankton to these communities range from 9 to 1970 mg C d1 m2. We estimate conservatively that the bed of S. hawaiicus off Kona, Hawaii, is responsible for the flux of 55 mg C d1 m2, which places it in the range of shallow-water tropical systems (Reiswig, 1974; Ayukai, 1995). Fluxes in temperate and boreal systems are even higher (Pile et al., 1996, 1997), most likely because of higher productivity of the pelagic ecosystems in these regions. Unfortunately, flow cytometry is not a reliable tool for quantification of rare plankton such as larger phytoplankton cells, and we were unable to determine their role in hexactinellid nutrition. However, larger cells are unlikely to be consumed by sponges. The only documented case of sponges phagocytizing cells larger than 5 mm occurred in the shallow Antarctic and was the result of a settling bloom of diatoms (Gaino et al., 1994). Clearly, shallow-water sponge communities are significant sinks for particulate organic material (POM) and have recently been shown to be net sinks for dissolved organic carbon (DOC) as well (Yahel et al., 2003). Hexactinellids may also be able to remove DOC from the water column, and further investigation into the roles
POM and DOC in meeting the sponges’ nutritional needs are merited. There are two potential sources of food for suspension-feeding organisms in the deep sea. The focus in the past has been on the role of vertical particle flux in the form of detritus from the euphotic zone as the primary source of food for deep-sea organisms (see review by Graf, 1992). However, much of the particulate carbon is in the ultraplankton fraction (Sherr and Sherr, 1991). It is difficult to find these cells in sediment traps unless they are incorporated into large detritus particles such as fecal pellets (Lochte and Turley, 1988; Pfannkuche and Lochte, 1993). In addition, it is now generally accepted that ultraplankton can support dense communities of suspension-feeding macroinvertebrates in shallow water (see review by Gili and Coma, 1998). Ultraplankton can be found in the deep sea either as resident plankton communities (Wishner, 1980; Karl and Knauer, 1984; Graf, 1989; Pile and Young, 1999) or as cells displaced from the surface by oceanographic processes (Witman et al., 1993). Our data clearly show that dense beds of hexactinellids are capable of moving large amounts of ultraplankton from the pelagic community to the benthos and that these sponges are most likely dependent nutritionally on ultraplankton. Downwelling waters are probably responsible for maintaining this community off Kona. However, in other parts of the deep sea, where downwelling may not be present, the role of resident ultraplankton in maintaining deep-sea suspension-feeding communities, such as demosponges and corals, remains to be examined.
Acknowledgments We are grateful to the captain and crew of the R./ V. Ka’imikai-o-Kanaloa, and the pilots and crew of the Pisces V submersible for their assistance in collecting the in situ data. S. Arellano, S. Brooke, C. Mah, M. Maldanado, T. Prowse, H. Reiswig, J. Watanabe, and M. Wood participated in the fieldwork. Research was supported by funds from the Hawaii Undersea Research Laboratory (National Undersea Research Program of NOAA) to CMY and AJP, as well as the Australian Research Council and University of Sydney Research funds to AJP.
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