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Karas P, Gorny M, & Alarco´n-Mun˜ oz R 2007. Experi- mental studies on the feeding ... American Fisheries Society, Beth- esda, MD, USA. Reiswig HM 1974.

Invertebrate Biology 129(2): 105–120. r 2010, The Authors Journal compilation r 2010, The American Microscopical Society, Inc. DOI: 10.1111/j.1744-7410.2010.00184.x

Characterization of macrofaunal assemblages associated with sponges and tunicates collected off the southeastern United States Cara L. Fiore1,a,b and Pamela Cox Jutte2 1

Grice Marine Laboratory, College of Charleston, Charleston, South Carolina 29412, USA Marine Resources Research Institute, South Carolina Department of Natural Resources, Charleston, South Carolina 29412, USA

2

Abstract. Sponges can serve as hosts to invertebrate assemblages that live and reproduce within them. Sponges also constitute a major part of the benthic epifaunal community on the continental shelf of the southeastern United States; however, little is known about these sponges and the assemblages they harbor. In this study, the associated fauna from a variety of sponges and one species of tunicate collected by submersible from the continental shelf and slope of the southeastern United States at depths in the range 18–875 m were examined. Seventeen sponges, comprising eight species (Ircinia campana, Topsentia sp., Geodia sp., Characella sp., Erylus sp., Apylsina archeri, Cliona sp., and Pheronema carpenteri), and three tunicate colonies (Didemnidae) were fully dissected and all associated organisms were identified and counted. Additionally, the sponges Pheronema annae (951 m) and P. carpenteri (770 m) represent new records for the region. The diversity (H0 ) and density of associates varied considerably among hosts; the densities of associates ranged 0.4–11,684 per 1 L of host volume. Polychaete worms were the most common organisms found, with one species, Haplosyllis spongicola, being especially abundant in I. campana, Topsentia sp., and Cliona sp. The amphipods Ericthonius punctatus and Leucothoe cf. spinicarpa, as well as decapods such as snapping shrimp (Synalpheus sp.) and crabs (e.g., Pilumnus floridana, Micropanope urinator), were also common. The number of symbiont taxa did not significantly increase as the sponge size increased. However, weak positive trends were found between the diversity of associates and increasing canal diameter. Sponges and tunicates were judged to represent legitimate ecological communities harboring a complete food web as well as gravid and juvenile individuals. Additional key words: shelf, slope, symbiont, morphology, Tunicata

Sessile organisms such as sponges, tunicates, and corals often provide microhabitats for various invertebrate species as well as some fishes (Pearse 1932; Tyler & Bo¨hlke 1972; Westinga & Hoejtes 1981; Wendt et al. 1985; Dalby 1996). Sponges, in particular, have been noted for their role as hosts for fauna such as crustaceans, polychaete worms, scyphozoans, fishes, molluscs (e.g., scallops, mussels), echinoderms, and pycnogonids (Pearse 1932; Dauer 1973; Bloom 1975; Ru¨tzler 1976; Biernbaum 1981; Peattie & Hoare 1981; Westinga & Hoejtes 1981; Meroz &

a

Author for correspondence. E-mail: clfi[email protected]

b

Current address: University of New Hampshire, 46 College Rd, Durham, NH, USA.

Ilan 1995; Duarte & Nalesso 1996; Rios & Duffy 1999; Crowe & Thomas 2001). Tunicates have also been noted for such associations with nemerteans, copepods, polychaetes, and amphipods (Dalby 1996; Theil 2000; Yakovis et al. 2005); however, far fewer studies have been conducted on tunicates relative to sponges. The specific relationship that each associate has with its host varies, and is well known for only a few sponge associates. The present study examined sponges and their associates collected by submersible from warm temperate deep water (18–875 m) reefs off the southeastern United States. These findings represent the first detailed examination in the Atlantic of sponge macrofaunal communities at depths greater than can be reached by SCUBA. There has been recent interest in mapping and characterizing hard-bottom habitats 4200 m off the

106

Fiore & Jutte

southeastern United States due to their importance as recruitment sites for many commercially important fishes (SAFMC 2004). Sponges may be important to these habitats because they are known to provide refuge for many invertebrates and fishes and provide a trophic link to secondary consumers (Tyler & Bo¨hlke 1972; Wulff 1994). The region’s distinctive topography (Barans & Henry 1984; Popenoe & Manheim 2001), including the many scarps and caves and extensive hard bottom, and unique oceanography, such as the influx of warm waters of the Gulf Stream and upwelling at the Charleston Bump, may allow for a diverse assemblage of bottom-dwelling organisms such as sponges, corals, and tunicates and their associated invertebrates. The current study examined a greater number of host species than previous efforts (e.g., Frith 1976; Westinga & Hoejtes 1981; Villamizar & Laughlin 1991; Ribeiro et al. 2003), and covered a larger depth profile, ranging 18–875 m. The use of a submersible for sample collection provided the advantage of obtaining relatively intact specimens that were isolated after collection to maintain sample integrity, and also allowed the collection of video of the specimen in situ. In addition, the present study examined sponge symbionts and characteristics such as the size, shape, and structure of the host sponge to determine the factors that may influence the spatial distribution and overall abundance of symbionts within individual sponges. We hypothesized that (1) a diverse community of sponges inhabits the shelf and slope of the region including sponges and tunicates that have not been previously examined for their macrofaunal associates and (2) measures of size of the host, including volume, canal diameter, and wall thickness are correlated with a greater abundance and diversity of associates.

Methods Field collection Sponge and tunicate specimens (n 5 19) were collected during dives (Fig. 1) using the submersible Johnson Sea Link II aboard the R/V Seward Johnson. Dives were conducted at ten shelf-edge and upper-slope locations off northern Florida to South Carolina, in depths ranging 50–951 m, during the summers of 2002, 2003, and 2004 (for detailed methods, see Fiore 2005). For comparative purposes, two sponges were collected from 16 km offshore of Charleston, SC, at 18 m depth by SCUBA divers. Specimens collected during all three sampling periods were fixed in a 10% formalin–seawater solution for 24 h (sponges collected in 2002 were kept in for-

Invertebrate Biology vol. 129, no. 2, spring 2010

Fig. 1. Dive locations of the submersible Johnson Sea Link II in the South Atlantic Bight for the 3 years in which sponges and tunicates were collected. Dive numbers correspond to the following sites: 3468 and 3472, St. Augustine Scarp; 3469 5 Jacksonville Scarp, 3413 5 Razorback, 3410 5 Tattler Town, 3298 & 3297 5 Charleston Lumps South, 3299 5 Charleston Lumps North, 3300 5 Georgetown Hole, 3464 & 3465 5 Popenoes Coral Mounds 1 and 2, 3467 5 Deep Flats, 3470 5 Cutthroat Cliff. Charleston, South Carolina is also marked on the map with a white star.

malin for about 4 months) and then preserved in 70% ethanol. In 2004, however, a new technique used before fixation was conducted in order to obtain as many associates as possible before the dissection of the sponge or tunicate. This approach resulted in more intact fauna due to less damage during the dissection process. The specimens collected in 2004 were placed into plastic bags containing seawater before preservation. After conditions in the bag became anoxic, the sponge or tunicate and faunal associates that evacuated the sponge or tunicate were placed in collection bottles, identical to the procedures followed in previous years.

Laboratory analysis Sponges were rinsed over a 0.5-mm sieve to collect any fauna present on the specimen’s exterior. Three

Sponge- and tunicate-associated macrofauna

107

volume measurements (‘‘wet,’’ ‘‘wrapped,’’ and ‘‘dry’’ volume) were made using volume displacement following the methods modified from Villamizar & Laughlin (1991), in which the sponges were wrapped in a self-sealing polyethylene wrap. The ‘‘wet volume’’ was determined after gently squeezing excess fluid out of the sponge; the ‘‘wrapped volume’’ was measured after wrapping the sponge in the polyethylene wrap. To measure dry volume displacement and dry weight, following dissection, sponges were dried in a Barnstead Thermolyne 30,400 furnace for 42 h at 701C. The three volume measurements were used to calculate the volume of channels and meanders and the total volume of the sponges (Villamizar & Laughlin 1991) as shown below. The atrial volume was calculated only to obtain the total volume. Volume of channels and meanders ¼ wet volume  dry volume Volume of atrium ¼ wrapped volume  wet volume Total volume ¼ atrial volume þ volume of channels and meanders All sponges and tunicates were dissected with the exception of the sponge Pheronema annae LEIDY 1868 (Hexactinellida, Pheronematidae), which could not be processed due to time constraints. Following dissection, symbionts were sorted into major taxonomic groups, identified to the lowest possible taxonomic level, and counted. Taxonomists at the South Carolina Department of Natural Resources were consulted regularly during the symbiont identification process and performed quality assurance and quality control checks. During the dissection process, a caliper was used to take ten arbitrary measurements of host wall thickness and 15 arbitrary measurements of canal diameter, which were then averaged to find the mean thickness and canal diameter for each specimen. The thickness and canal diameter measurements were used as additional parameters to provide a measure of the habitable space within the host for associated fauna. Wall thickness was defined in sponges as the width from the outer surface to the center atrium for sponges, and in tunicates as the interior width of the folds (Fig. 2). Canal diameter in sponges was defined as the network of channels and meanders found in each specimen. In tunicates, canals were defined as the network of open spaces in between the folds, which is where many of the macrofauna were found. Sponges were identified by photographs and spicule preparations using a taxonomic key to Porifera

Fig. 2. Example of a wall thickness measurement (black line) and a canal diameter measurement (white line/arrow) for a sponge (Geodia sp.) (A) and a tunicate (Didemnidae) (B) specimen. Scale bars 5 10 cm.

(Hooper & Van Soest 2002) and through discussions with experts (G. Muricy, C. Diaz, H. Reiswig, pers. comm.). Spicule preparations were performed using a bleach digestion technique, and histological sections were prepared to determine the structure of the mineral skeleton (Hooper 2000). During the 2002 sampling, benthic infaunal samples were collected by the NOAA-NOS Center for Coastal Environmental Health and Biomolecular Research (CCEHBR) Laboratory from several sites sampled in the current study (St. Augustine Scarp, Jacksonville Scarp, Julians Ridge, Georgetown Hole, and Charleston Lumps) (Sedberry et al. 2004), and were made available for comparison with the faunal assemblages of the host specimens in the current study (http://www.nbi.noaa.gov/mapOE.aspx). A

Invertebrate Biology vol. 129, no. 2, spring 2010

108 Young grab (0.03 m2) was used by the submersible to collect the samples at each site that were analyzed at the CCEHBR in Charleston, South Carolina.

Statistical analyses Symbiotic faunal diversity was calculated using the Shannon–Wiener index (H0 ), evenness was calculated as Peilou’s eveness (J0 ) (Brower et al. 1997), and species richness (D) was found using the formula devised by Margalef (1958). The influence of host morphology and habitat characteristics on the diversity and density of symbionts was examined using multiple regressions including all sponge and tunicate specimens. Because of the high numbers of individuals of Haplosyllis spongicola GRUBE 1855, their presence (density) was correlated with community parameters including evenness, diversity, species richness, and physical parameters including depth, volume, canal diameter, and thickness using multiple regression. Backwards stepwise regressions were conducted using JMP statistical software (SAS Institute, Cary, NC, USA). To meet the assumption of normality, some variables were log-transformed (canal diameter and diversity) or rank-transformed (associate density). Linear regressions were used to examine the intraspecific relationships between host characteristics such as volume, thickness, and canal diameter and symbiont density and diversity, but were restricted to Ircinia campana LAMARCK 1814 due to limited replicates of host species for other sponges. Host wall thickness could not be transformed to pass normality tests; therefore, a non-parametric regression (Kendall’s robust regression) was used to test host wall thickness for a relationship with diversity and with density across host taxa (Sokal & Rohlf 1995). In order to quantify differences in community parameters between tunicates and sponges, analysis of variance (ANOVA) was conducted for diversity, evenness, and species richness. A comparison of the density and diversity of faunal assemblages between hosts collected from hard- and soft-bottom sites was conducted in order to examine any influence of substrate on the associate community. A Wilcoxon two-sample test was used due to lack of homoskedacity (Sokal & Rohlf 1995). Additionally, diversity (H0 ), evenness (J0 ), and species richness (D) were compared between the benthic infaunal samples and the faunal assemblages from hosts collected from St. Augustine Scarp using a Wilcoxon test due to lack of homoskedacity. St. Augustine Scarp was the only site with enough host samples to conduct a statistical comparison between the benthic and the host samples.

Invertebrate Biology vol. 129, no. 2, spring 2010

Fiore & Jutte The parametric cluster analysis was based on the density of shared symbiont species per 500 mL of host, and examined the similarity of symbiont assemblages in hosts. Analyses used the hierarchical unweighted pair-group method using arithmetic averages (UPGMA) with the Bray–Curtis similarity coefficient (Chao et al. 2005) in the program R (R Project, Vienna, Austria, http://www.r-project. org). Analysis of similarity (ANOSIM) was conducted (in R) on the cluster analysis to determine significance (Clarke 1993); an overall analysis was first conducted on all groups, followed by pairwise tests of the cluster groups. A Bonferroni correction (Sokal & Rohlf 1995) was incorporated for multiple tests (n 5 6, a0 5 0.008).

Results A total of 18 sponges and three tunicates (Didemnidae) were collected. Two of these sponges, Pheronema carpenteri THOMSON 1869 (Hexactinellida, Pheronematidae) (311400 1200 N, 801160 1200 W) and Pheronema annae (Hexactinellida, Pheronematidae) (301160 4800 N, 791200 2400 W), are new records for the region (Fig. 1, Table 1). With the exception of the sponge P. annae, all specimens were thoroughly dissected to analyze their faunal associate communities. The tunicates’ faunal assemblages, although not the main subject of this study, were used in the analyses for comparative purposes. Eight species of sponges were collected and examined for associates: five Ircinia campana (Demospongia, Dictyoceratidae) (the stinking vase sponge), three Topsentia sp. (Demospongia, Halichondriidae), three Geodia sp. (Demospongia, Geodiidae), and two Cliona sp. (Demospongia, Clionidae). In addition, one specimen of each of the following taxa was collected: Erylus sp. (Demospongia, Geodiidae), Characella sp. (Demospongia, Pachastrellidae), Aplysina archeri HIGGIN 1875 (Demospongia, Aplysinidae) (the stove-pipe sponge), and P. carpeneri. A total of 26,710 symbionts comprising 236 species were collected from all host specimens; the top 50 dominant associate species are given (Table 2). Collection sites ranged from shallow hard- and soft-bottom reefs to deeper mostly soft-bottom or rubble habitats (Table 1).

Composition of associate communities The total percentage of each taxon found was calculated for sponges and tunicates (Table 3). Within sponges, polychaetes were the overwhelmingly dom-

Sponge- and tunicate-associated macrofauna

109

Table 1. Habitat and host characteristics: collection depth (m), temperature (1C), salinity (practical salinity scale), dissolved oxygen (DO, mg L1), volume of the channels and meanders (CM Vol, mL), total volume (T-Vol, mL), average canal diameter (C-diam, mm), average thickness (thick, mm), and dry weight (Dry Wt, g) for each host species. Diversity (H0 ), evenness (J0 ), species richness (D), and density (per liter of host volume) are also given or each host specimen. Dissection data for Pheronema annae are not available (see text for details). Host species Ircinia campana A I. campana B I. campana C I. campana D I. campana E Geodia sp. A Geodia sp. B Geodia sp. C Characella sp. Pheronema carpenteri Topsentia sp. A Topsentia sp. B Topsentia sp. C Cliona sp. A Cliona sp. B Erylus sp. Aplysina archeri Tunicate A Tunicate B Tunicate C Pheronema annae

Depth

Temp.

Salinity

DO

CM Vol

T-Vol

C-diam

Thick

Dry Wt

H0

J0

SR

Density

18 18 52 55 59 875 194 778 778 770 51 55 77 57 57 194 50 46 61 55 951

20.9 20.9 18.4 18.4 19.9 7.7 13.3 9.8 9.8 9.8 20.3 18.4 13.7 18.9 18.3 20.9 20.9 15.9 19.3 18.4 7.8

35.0 35.2 36.4 36.4 37.0 35.0 36.0 35.3 35.2 35.3 36.6 36.4 35.8 36.4 36.4 37.0 37.0 35.8 37.0 36.4 35.0

NA NA 4.8 4.4 NA 4.3 NA 4.4 4.4 4.4 NA 4.4 5.8 NA NA NA NA 5.72 NA 4.4 4.3

273 10 774 546 229 1183 1484 4213 750 735 988 636 350 348 453 458 191 340 90 210 NA

358 280 1347 1123 307 2736 2309 9411 1845 3479 1388 1058 1385 593 711 867 701 893 55 437 NA

1.4 2.0 1.2 1.1 1.4 1.5 1.4 1.6 0.0 1.8 1.0 1.2 1.3 1.3 1.7 1.4 1.4 2.8 1.4 2.2 NA

50.2 20.0 16.2 27.0 50.2 34.1 50.2 47.9 22.8 50.2 170.0 98.1 127.9 77.3 84.6 50.2 50.2 6.9 50.2 4.6 NA

48.1 41.3 73.3 76.7 16.8 372.7 388.3 1280.0 157.5 103.6 254.0 247.2 368.3 285.1 290.1 78.9 24.7 75.1 74.5 90.9 NA

2.53 0.46 0.43 0.04 4.24 0.81 2.99 0.92 2.64 2.24 0.05 0.75 0.11 0.69 0.85 1.48 3.05 4.72 2.22 3.94 NA

0.57 0.09 0.10 0.01 0.92 0.81 0.94 0.92 0.83 0.53 0.02 0.18 0.04 0.25 0.27 0.27 0.75 0.85 0.83 0.78 NA

4.29 3.71 2.65 1.37 5.62 0.72 3.03 0.91 2.62 3.70 1.21 3.05 1.02 1.09 1.59 1.43 3.89 8.74 5.62 6.21 NA

6106 11,294 2680 7464 234 1.5 6.0 0.3 12 36 2720 918 672 422 220 602 200 184 1346 396 NA

Table 2. Results of analysis of similarity (ANOSIM) showing the ANOSIM R-statistic and p-value for the overall test (significance of po0.05) and pairwise tests of cluster Groups I–IV (significance of po0.008). Bold represents significant values. Cluster group

R-statistic

p-value

Overall I versus II I versus III I versus IV II versus III II versus IV III versus IV

0.81 1.00 0.95 0.81 1.00 1.00 0.50

0.0001 0.092 0.019 0.010 0.036 0.037 0.002

inant associates (93%), while the tunicates did not exhibit dominance by any particular taxon (Fig. 3). While the Polychaeta were the most common overall associate taxon (Table 3), their abundance varied considerably among and within host sponge species (Fig. 3). The majority of these polychaetes were Haplosyllis spongicola, which were particularly abundant in I. campana and Topsentia sp. specimens (except for I. campana E, for which H. spongicola comprised

only 35% of the polychaete community). The polychaete family Syllidae was the most commonly observed across all host taxa and depths, with the genus Syllis being particularly abundant, after H. spongicola. Other commonly encountered polychaete families were Nereidae (e.g., Neanthes succinea FREY and LEUKART 1847), Polynoidae (e.g., Harmothoe spp.), Terebellidae (e.g., Loimia medusa SAVIGNY in LARMARK 1818), and Eunicidae (e.g., Eunice filamentosa GRUBE 1856). Polychaetes were found in all hosts, except for two Geodia sp. (A and C) specimens, which contained few overall associates. The rest of the associates included a variety of taxa (Fig. 3), of which the most commonly observed included Leucothoe cf. spinicarpa ABILDGAARD 1789 and Ericthonius punctatus BATE 1857 (Amphipoda,); Hansenium bowmani KENSLEY 1984A (Isopoda); Synalpheus spp. (Decapoda); Ophiothrix angulata SAY 1825 (Ophuiroidea); Pilumnus floridana STIMPSON 1871 (Decapoda); and Parviturboides interruptus ADAMS 1850 (Gastropoda). The amphipod species of L. spinicarpa has undergone recent revision (Thomas & Klebba 2006, 2007) and individuals observed in the current study are likely part of a ‘‘Leucothoe complex.’’ Gravid individuals were also found in

Invertebrate Biology vol. 129, no. 2, spring 2010

110 Table 3.

Fiore & Jutte Collection site, year of collection, and habitat description for each host specimen.

Host species

Site

Year

Description Sediment-covered hard bottom with scattered sessile invertebrates Sediment-covered hard bottom with scattered sessile invertebrates Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Mostly soft bottom, scattered rocky rubble with few sessile invertebrates Scattered large rocks on a sediment bottom, some small sessile invertebrates Largely flat, some gentle slopes, coral rubble and sediment Largely flat, some gentle slopes, coral rubble and sediment Largely flat, some gentle slopes, coral rubble and sediment Mostly soft bottom, scattered rocky rubble with few sessile invertebrates Mostly soft bottom, scattered rocky rubble with few sessile invertebrates Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Well-defined reef with large boulders, many sessile invertebrates, also thick sediment areas Well-defined reef with large boulders, many sessile invertebrates, also thick sediment areas Soft and hard bottom with scattered boulders and sessile invertebrates Soft and hard bottom with scattered boulders and sessile invertebrates Mostly flat pavement and rocky rubble, few sessile invertebrates Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment Large boulders, ledges and overhangs, many sessile invertebrates, generally little sediment

Ircinia campana A

Near Charleston, SC, USA

2004

I. campana B

Near Charleston, SC, USA

2004

I. campana C

2004

Geodia sp. A

St. Augustine Scarp North, FL, USA St. Augustine Scarp South, FL, USA St. Augustine Scarp, FL, USA Mystery Site 1, SC, USA

Geodia sp. B

Charleston Lumps, SC, USA

2002

Geodia sp. C

Popenoes Coral Mounds 1

2004

Characella sp.

Popenoes Coral Mounds 1

2004

Pheronema carpenteri

Popenoes Coral Mounds 2

2004

Pheronema annae

Cutthhroat Cliff

2004

Topsentia sp. A

2002

Topsentia sp. C

St. Augustine Scarp, FL, USA St. Augustine Scarp South, FL, USA Tattlertown, SC, USA

Cliona sp. A

Jacksonville Scarp, FL, USA

2002

Cliona sp. B

Jacksonville Scarp, FL, USA

2002

Erylus sp.

Julians Ridge, SC, USA

2002

Aplysina archeri

Georgetown Hole, SC, USA

2002

Didemnidae sp. A

Razorback, SC, USA

2003

Didemnidae sp. B

St. Augustine Scarp, FL, USA St. Augustine Scarp South, FL, USA

2002

I. campana D I. campana E

Topsentia sp. B

Didemnidae sp. C

many sponge and tunicate hosts, including amphipods, isopods, and polychaetes.

Associate abundance, density, and diversity Diversity values of faunal communities associated with sponges and tunicates varied considerably within and between host species (Table 4). As a general trend, the hosts with the highest total number of

Invertebrate Biology vol. 129, no. 2, spring 2010

2004 2002 2004

2004 2003

2004

associates also had some of the lowest diversity and evenness values. The tunicates had significantly higher diversity (F1,18 5 7.6, p 5 0.01) and species richness (F1,18 5 22.9, p 5 0.0001) than sponges. Evenness was generally higher in the tunicates than in the sponges but not significantly (po0.05). Additionally, tunicates tended not to be dominated by a single symbiont taxa or species. Among the rest of the outer

Sponge- and tunicate-associated macrofauna

111

Fig. 3. Average calculated density of major associate taxa for each host species on log scale. Standard error bars are shown.

shelf hosts, diversity was often strongly affected by the presence of the polychaete H. spongicola, particularly for the sponges I. campana (n 5 17,860, mean density 5 5229 L1) and Topsentia sp. (n 5 5760, mean density 5 1504 L1). The diversity of I. campana associates varied considerably within this species, with a particularly high diversity for specimen E relative to the other I. campana specimens. The density of polychaetes was much greater for I. campana and Topsentia sp. than the densities of the other taxa collected from the hosts (Fig. 3). Haplosyllis spongicola accounted for  90% (r99%) of the total symbionts in all Topsentia sp. specimens and the four I. campana (A–D) specimens, resulting in a large difference in abundance between H. spongicola and the rest of the symbiont species. Cliona sp. and Erylus sp., also outer shelf sponges, contained a high density of polychaetes, similar to I. campana and Topsentia sp. but to a lesser extent; H. spongicola was the most common polychaete in Cliona sp. and Erylus sp. (Cliona sp. n 5 5360, mean density 5 5276 L1; Erylus sp. n 5 5512, density 5 5590 L1), while the densities of the other taxa were relatively low in these two sponges (Fig. 3). Diversity was relatively low for both of these sponge species, and there was a large difference between the number of the most abundant symbiont (H. spongicola) and the number of the second most abundant symbiont for each host, resulting in low community evenness. Aplysina archeri, the last outer shelf sponge, had a relatively high diversity, but few total symbionts and fewer H. spongicola (n 5 22, density 5 31 L1) relative to the previously mentioned sponges. In addition, the densities of the major taxa found in A. archeri were relatively low compared with the other host specimens. There was also a relatively small gap

in number between the most abundant (n 5 22) and the second most abundant (n 5 12) symbionts for A. archeri, resulting in a relatively higher evenness. Aplysina archeri was also one of two sponges (see the details on P. carpenteri below) to contain a fish, the tusked goby, Risor ruber ROSE´N 1911 (Gobiidae). The diversity and abundance of symbionts associated with the slope sponges (Geodia sp., Characella sp., and P. carpenteri) also varied considerably. Specimens of Geodia sp. had a relatively high evenness, and the shallower specimen (B) had a relatively high diversity; however, few total symbionts were found in each specimen of Geodia (n 5 4, 14, and 3, respectively, mean density 5 4 L1). The sponge Characella sp., which had no visible canals, also had relatively high diversity and low densities of associated taxa (Table 4, Fig. 3). Few overall symbionts (n 5 22, density 5 12 L1) were found, and there was a small difference between the abundance of the most abundant symbiont species and the abundance of the other symbiont species, yielding high evenness. The glass sponge P. carpenteri, despite the relatively high density of ophiuroids (density 5 23 L1) (Fig. 3), also had a relatively high diversity and included a juvenile eel (Dysommina rugosa GINSBURG 1951). In contrast to the sponges collected from the shelf, P. carpenteri and Characella sp. contained no H. spongicola and only one specimen of Geodia sp. (B) contained one H. spongicola (n 5 1). Of the benthic infaunal samples, 34% of the ten most abundant infaunal species were also observed at least once in one or more hosts (e.g., H. spongicola, Ampelisca sp. [Amphipoda]), while 66% were never observed in the hosts (e.g., Glycera sp. [Polychaeta], Rildardanus laminose PEARSE 1912 [Amphipoda]). Additionally, only two of the ten most abundant host-associated species (H. spongicola and E. pun-

Invertebrate Biology vol. 129, no. 2, spring 2010

Invertebrate Biology vol. 129, no. 2, spring 2010

Eunice sp.

S

S

F

Og

F/Hf

17

20

Luconacia

Apseuda cf

sp.

Gammaropsis

F/Hf

F

Hh

28

Cymadus

30

S

Oc

25

Caprella sp.

compta

F

G

F/Hf

24

Chevalia sp.

bermudeus

incerta

F

Hf

He

15

O

S

G

14

F/Hf

He

F/Hd

S

Gammaridae

9

5

4

Oc

F

G

Ca

Ca

F

Elasmopus levis

halichondriae

Colomastix

appendiculata

Dulichiella

spinicarpa

Leucothoe

punctatus

Ericthonius

2

49

50

Arabella mutans

verilli

Steblosoma

Da

F

Fa

43

Potamilla

44

G

reniformis

G

Da

C/Sa

40

G

39

Ca

Anaitides sp.

32

Streblosoma sp.

Harmothoe sp.

moniloceras

Nicon

succinea

F

27

Neanthes

Oa

S

26

Syllis gracilis

29

G

Ca

Oa

23

caulleryi

F

G

Ca

F/Da

19

G

Syllis sp. 12

G

Ca

S

level

Taxonomic

D/Sa

Ca,b

level

Trophic

Polydora

Amphipoda

C

B

8

18

Exogone dispar

1

rank

Overall

Harmothoe sp.

spongicola

Haplosyllis

Polychaeta

species

Faunal associate

0

0

0

0

6

0

0

0

8

96

72

253

0

1

2

0

0

0

0

1

0

7

0

0

0

28

3032

campana A

Ircinia

0

13

0

0

8

0

0

0

0

0

9

92

0

0

0

0

0

0

0

2

0

2

0

0

0

24

3025

B

0

0

13

15

0

0

9

0

6

2

2

5

4

0

3

0

1

0

0

0

1

1

0

15

4

1

3444

C

0

0

1

0

0

0

0

0

0

0

1

0

0

0

0

1

0

0

0

0

1

0

0

0

0

0

8352

D

0

0

0

0

1

2

0

0

0

0

4

2

0

3

0

0

0

0

0

4

0

0

0

0

1

0

7

E

1

0

0

0

0

0

0

0

0

0

5

0

0

0

0

0

0

0

0

0

3

0

0

0

0

0

3960

A

6

0

0

0

0

0

15

31

0

1

14

15

0

0

1

0

0

0

0

0

2

1

0

4

0

0

880

B

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

920

C

2

0

0

0

0

0

0

0

1

0

20

0

0

0

0

0

4

0

0

0

0

0

0

0

0

0

222

1

0

0

0

0

0

0

0

2

0

4

0

0

0

0

0

2

0

0

0

0

0

0

0

1

0

136

0

0

0

0

0

0

0

0

13

0

0

0

0

0

0

0

0

0

0

0

1

0

0

1

0

0

512

I. campana I. campana I. campana I. campana Topsentia sp. Topsentia sp. Topsentia sp. Cliona sp. A Cliona sp. B Erylus sp.

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

1

0

0

12

0

0

0

22

archeri

Aplysina

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

A

0

0

0

0

0

3

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

1

B

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

C

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

Geodia sp. Geodia sp. Geodia sp. Characella sp.

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

7

0

0

0

0

0

0

15

0

0

carpenteri

Pheronema

0

0

0

0

0

0

0

0

0

1

16

17

0

0

0

3

0

0

5

2

0

2

0

0

0

0

0

idae A

Didemn-

2

0

0

0

0

16

0

0

13

0

15

5

0

0

0

0

0

0

0

2

0

0

1

0

0

0

0

idae B

Didemn-

0

0

0

0

3

0

0

0

1

1

39

28

0

0

0

2

0

0

6

1

5

0

2

0

0

2

4

idae C

Didemn-

12

13

14

15

18

21

24

31

44

101

201

417

4

4

6

6

7

7

11

13

13

13

15

20

21

55

24,517

Total

Table 4. The 50 most abundant associate species for all host specimens. Columns: OR, overall rank; the corresponding major taxon is given for each associate species: A, Amphipoda; B, Bivalve; D, Decapoda; G, Gastropoda; I, Isopoda; O, Ophiuroidea; P, Polychaeta; S, Sipuncula. The column ‘‘Taxonomic level’’ indicates the taxonomic level for the givien trophic level information: C, class; F, family; G, genus; O, order; P, phylum; S, species.

112 Fiore & Jutte

21

34

Dk

Fk

Ok

P

C

C

C

D/Oy

6

C

D/Oy

7

2

0

75

12

0

0

19

4

323

0

0

0

0

0

0

21

0

0

0

0

3

0

0

0

4

18

6

0

0

14

0

16

0

0

0

0

0

0

11

0

0

6

0

0

0

0

0

4

0

0

0

0

0

6

7

0

0

0

0

0

0

0

0

0

0

0

0

0

0

b

0

2

0

1

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3

0

0

0

0

0

0

0

0

0

1

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

0

0

0

0

1

1

0

0

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

3

0

0

0

2

0

0

0

0

0

0

0

2

6

6

0

0

0

0

0

c

0

0

0

0

0

0

0

0

0

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

7

0

0

0

0

0

0

1

0

5

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

1

0

0

0

0

0

0

0

0

0

0

0

0

3

0

0

0

0

0

0

6

0

0

0

0

0

0

3

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

d

0

0

0

0

0

0

2

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

e

9

0

0

0

4

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

3

0

0

0

80

0

0

8

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

0

14

5

7

0

0

7

19

0

5

0

0

0

0

7

0

f

0

0

0

0

0

0

0

1

3

0

0

7

8

0

11

0

0

0

0

0

0

0

0

2

0

0

14

0

0

0

0

4

0

0

0

0

6

0

0

0

0

0

0

0

0

11

17

10

93

38

87

5

36

22

368

5

7

7

8

16

32

35

11

6

6

7

9

10

11

g

Fauchald & Jumars 1979 (and references therein). Neves & Omena 2003. Duffy 1990 (and references therein). Theil 1999. Duffy & Hay 2000. Thomas 1993. Butler et al. 1983. hZimmerman et al. 1979. iChristian & Luczkovich 1999. jDuffy et al. 2001. kBarnes 1987. lNicotri 1980. mCartes et al. 2007. nNielson 2001. o Kvitek et al. 2008. pDuffy 2002. qCarlier et al. 2007. rGrall et al. 2006. sKaras et al. 2007. tLe Loc’h & Hily 2005. uFrick et al. 2003. vKennedy et al. 2001. wGore & Abele. xSchram 1986. yHendler et al. 1995.

a

Sipuncula

Sipuncula

Bivalve 1

Bivalvia

interruptus

Parviturboides

Gastropoda

angulata

Ophiothrix

Ophioprium sp.

Ophiuroidea

10

O

O/Ck

dubia

O

O/Ck

48

F

F

11

Ox

Ox

Leptochelia sp.

16

3

G

Leptochelia

Tanaidacea

coralicola

Jaeropsis

bowmani

Hansenium

Isopoda

rusimanus

Pachycheles

Ow

G

Ov

38

Pontonia

47

S

Ou

margarita

G

Os/Ct

37

G

G

36

Oq/Cr

Cp

Planes minutus

22

13

Munida irrasa

floridana

Pilumnus

townsendi

Synalpheus

carolinensis

Pagurus

G

46

Hn/So

S

Hm

H/Cm

45

Lembos sp.

Lembos smithi

12

G

Hl

Decapoda

F

G

Dk

42

S

G

F

41

Hj

Hi

F/Hf

Ampithoe valida

35

33

31

Corophioidae

mucronatus

Gammarus

websteri

Lembos

plumulosus

Leptocheirus

Sponge- and tunicate-associated macrofauna 113

Invertebrate Biology vol. 129, no. 2, spring 2010

114

Fiore & Jutte

Table 5. Total percentage of each major associate taxon for all sponges and all tunicates. Taxa Amphipoda Isopoda Echinodermata Mollusca Polychaeta Decapoda Other

Sponges

Tunicates

4 1.5 0.5 0.4 93 0.3 0.3

32 9.3 1.3 0.7 28 28 0.7

ctatus), and one percent of the total species, were also observed in the infauna samples. While the calculated parameters were generally higher for the benthic infauna than for the hosts (Table 5), there was no significant difference in the diversity or the evenness values (p40.05) between the benthic fauna and the host-associated fauna from St. Augustine Scarp. Species richness, however, was significantly higher in the benthic infaunal samples compared with the hosts (W 5 77, p 5 0.0005).

Fig. 4. Parametric cluster analysis of symbiont communities using hierarchical clustering and Bray– Curtis similarity based on the density of symbiont species. I, II, III, and IV are the major groups recognized.

Invertebrate Biology vol. 129, no. 2, spring 2010

Community similarity analysis Parametric cluster analysis of hosts according to their symbiont community composition and density yielded a dendrogram with four possible groups (Fig. 4). All three tunicate specimens clustered into Group I. Group II consisted of the deep-water sponges Characella sp. and P. carpenteri, but did not include Geodia sp., which is found at similar depths. Group III consisted mainly of I. campana (with the exception of one I. campana found in Group IV), and one Topsentia sp. Group IV was mixed, including primarily those sponges having a relatively low dominance by H. spongicola (with the exception of Topsentia sp. B and C). The ANOSIM of the whole cluster analysis yielded a significant difference among groups (R 5 0.81, p 5 0.001). The only pairwise comparison that was significant was that between Groups III and IV (R 5 0.05, p 5 0.002) (Table 6).

Effects of host characteristics The relationships between the physical characteristics of the hosts and the habitat (Table 4) with asso-

(2.18) (1.21–3.05) (5.62–6.21) (2.11) (1.09–1.59) (2.32) (1.03) (2.05) (0.52) 10.95 10.24 8.41 6.85 (0.01) (0.04) (0.03) (0.03) 3.66 3.47 3.28 3.07 Jacksonville Scarp (n 5 3) Julians Ridge (n 5 6) Geortown Hole (n 5 4) Charleston Lumps (n 5 3)

(0.19) (0.18) (0.27) (0.1)

0.94 0.90 0.90 0.94

0.92 (0.03) 3.46 (0.22) St. Augustine Scarp (n 5 1)

9.84 (1.55)

Ircinia campana (n 5 3) Topsentia sp. (n 5 2) Tunicate (n 5 2) Mean Cliona sp. (n 5 2) Erylus sp. (n 5 1) Aplysina archeri (n 5 1) Geodia sp. (n 5 1)

1.57 0.40 3.08 1.73 0.77 1.48 3.05 2.99

(2.32) (0.5–0.75) (2.22–3.94) (1.75) (0.69–0.85)

0.34 0.10 0.81 0.43 0.26 0.27 0.75 0.94

(0.5) (0.2–0.18) (0.78–0.83) (0.39) (0.25–0.27)

3.21 2.13 5.92 3.68 1.34 1.43 3.89 3.03

D J0 H0 Host D J0 H0 Benthic infaunal sample

Table 6. Comparison of diversity (H0 ), evenness (J0 ), and species richness (D) between the benthic infaunal samples and the corresponding host samples. Values are given as means with standard deviation when sample size greater than two, or range when sample size is two. A mean value is also presented for all hosts collected from St. Augustine Scarp.

Sponge- and tunicate-associated macrofauna

115 ciate community metrics for I. campana yielded only one significant relationship. While no significant relationships were observed between symbiont abundance and host size, a significant positive relationship was observed between the volume of channels and meanders, a measure of habitable space, and the total volume of the host (F1,3 5 26.5, p 5 0.014). As sponge morphology is often irregular, the relationship between the volume of channels and meanders and the total volume may be shaped by multiple factors that influence the shape and the size of the sponge. Multiple regression analyses using sponge and tunicate specimens found significant relationships between the diversity and the density of associates with respect to host morphology. When log-transformed, symbiont diversity was used as the dependent variable; only canal diameter was found to be significantly and positively correlated with diversity (F1,16 5 0.4, p 5 0.03). Canal diameter was also found to be significantly and negatively correlated with symbiont densities (rank-transformed) (F1,18 5 4.4, p 5 0.049). In both cases, the regressions yielded low regression coefficients. Non-parametric regressions, which were completed to test host wall thickness for a relationship with diversity and with density, yielded no significant relationships between host thickness and symbiont density or diversity. No significant relationship was found between the physical characteristics of the habitat from which the sponges were collected and symbiont density or diversity. There was no significant difference in the diversity or the density of associated fauna of hosts from hard and soft substrates (p40.05). Backward stepwise regression of the density of H. spongicola with community and physical parameters yielded a significant model (at the a 5 0.10 level), where depth, host wall thickness, and diversity were inversely related to density (R2 5 0.277, F1,15 5 4.4, p 5 0.052; F1,15 5 4.2, p 5 0.059; F1,15 5 6.72, p 5 0.02, respectively). The regression was not significant, however, at a 5 0.05.

Discussion Sponge habitat and distribution Sessile organisms, sponges in particular, have been noted for their abundance on hard-bottom habitats (Struhsaker 1969; Wenner et al. 1983; Barans & Henry 1984; Van Dolah et al. 1987; Griffin 2005). In the present study, 18 sponges and three tunicates, comprising nine total species, were identified from the shelf and slope off Florida, Georgia, and South Carolina, including four sponge genera not reported by previous studies: Erylus, Topsentia, Characella,

Invertebrate Biology vol. 129, no. 2, spring 2010

116 Pheronema annae, and Pheronema carpenteri. Although some of these sponges may have not been reported by previous studies due to the greater depths sampled in the current study, the need for more detailed assessments of the epifauna of this region is apparent. Interestingly, the two glass sponges reported here, P. annae and P. carpenteri, both represent new records for the region. Pheronema annae has been documented previously in the Caribbean and northwestern and mid-Atlantic, while P. carpenteri has been documented in the northeastern Atlantic, but not off of North America (Reiswig & Champagne 1995; Reiswig, pers. comm.). Previous documentation of sponges of the class Demospongiae (Van Soest 1994) indicates that some sponges collected in the present study from cool-temperate waters at the northern shelf sites may be at, or near, the limit of their range. These include Erylus sp., Topsentia sp., Aplysina archeri, and Ircinia campana. In fact, during the current study, I. campana was collected up to a depth of 58 m, which is deeper than any previous reports (Pearse & Williams 1951; Wenner et al. 1983; Fernando & Sven 2003). Because of the flow of warm water from the Gulf Stream and areas of cold upwelling water at the Charleston Bump, the region investigated in the current study may represent a convergence zone for many sponge genera with tropical and sub-tropical ranges, such as Apylsina and Erylus, and those inhabiting colder waters (e.g., Cliona sp., Geodia sp., Pheronema spp.), allowing for a diverse assemblage of sponges and tunicates. Additionally, the presence of such a variety of sponges, tunicates, and the assemblages they harbor lends support to the recent interest in characterizing the bottom habitat of the region due to its importance as a habitat for commercial fish species. The opportunity to use a submersible to collect the sponge and tunicate specimens yielded a valuable insight into the surrounding habitat of the collected specimens, as well as allowing for exploration into less studied regions where sponges and tunicates provide microhabitats. At the same time, however, sponge and tunicate collections were limited by this collection technique and the current study is meant to provide a baseline for more detailed future studies of the sponge and tunicate communities inhabiting the continental shelf and slope of the southeastern United States.

Characterization of associates While there have been a plethora of studies examining sessile hosts and their symbionts in shallow wa-

Invertebrate Biology vol. 129, no. 2, spring 2010

Fiore & Jutte ters (Ru¨tzler 1976; Hendler 1984; Magnino & Gaino 1998; Rios & Duffy 1999; Crowe & Thomas 2001), sponge symbiont composition, as well as factors affecting symbiont communities (e.g., seasonality, currents, habitat type), are likely to differ between shallow water (o100 m) and deep-water sponge communities. The current study presents the first in-depth look at sponges and their associated fauna inhabiting the continental shelf and slope off the southeastern United States. The current study is also one of a few studies that have examined fauna associated with tunicates (e.g., Svavarsson 1990; Dalby 1996; Theil 2000) and hexactinellid glass sponges (e.g., Kunzmann 1996; Beaulieu 2001a,b). While the diversity and species richness of associates were significantly higher in tunicates, this should be interpreted cautiously due to the limited sample size. The most notable difference between the tunicate and the sponge hosts was the lack of Haplosyllis spongicola in the tunicates. Whether this difference is due to food preference, habitat preference, attraction, or repulsion by other organisms, and other factors remains unknown and is a subject of future studies. It is clear from the present study that this polychaete varies in density even among sponges. Diversity values of the sponge faunal communities examined in the current study were generally lower than the values reported by previous studies of sponge symbionts (Duarte & Nalesso 1996; Ribeiro et al. 2003) although one I. campana specimen (E) and the tunicates had H0 values similar to other assessments (Wendt et al. 1985). However, diversity values of the symbiotic communities from four of the five I. campana specimens from the current study were similar to those documented by Wendt et al. (1985) (H0 5 0.71). In both studies, the diversity was low mainly due to the overwhelming abundance of the syllid polychaete H. spongicola. Dominance by H. spongicola has been noted by previous studies in this region (Wendt et al. 1985; for the sponges I. campana and Haliclona oculata) and in the Caribbean and Indian Ocean (Reiswig 1974; for the sponges Mycale sp., Tethya crypta, and Verongia gigantea; Magnino & Gaino 1998; for the sponge Mycale microsigmatosa, respectively). While this polychaete has been documented outside of sponges in sediments and on hard substrates (Wenner et al. 1983; Uebelacker & Johnson 1984), the overwhelming abundance in some host species and not others in the present study and the fact that it has been documented to use its sponge host for food (Magnino & Gaino 1998) indicate that there is some host preference and/or deterrence by the hosts. Haplosyllis spongicola are also thought to play a major role in

Sponge- and tunicate-associated macrofauna structuring polychaete communities (Neves & Omena 2003), and possibly the whole symbiont community within sponges. For example, the shear number alone of H. spongicola found within a host will greatly reduce the number of other potential host inhabitants and may even limit the size of potential inhabitants as a result of these polychaetes filling most of the available space. The density of H. spongicola in the present study was negatively correlated at the a 5 0.1 level with diversity, host wall thickness, and depth, suggesting that high densities of the polychaete affect community structure. The diversity of faunal associates in the current study was generally lower in the hosts with higher densities of H. spongicola. The results of the regression also indicate that physical parameters may influence the density of H. spongicola. Consequently, when H. spongicola colonizes a sponge or a tunicate, their density could then influence the associate community structure. However, the regression had low test statistics and would benefit from the analysis of a larger sample size in the future. There may also be interspecific competition for food if H. spongicola is sharing a host with another associate that preys on the host for food (e.g., Synalpheus spp.). Future studies examining interactions among common sponge or tunicate-associated fauna would shed light on community structure within these hosts. The cluster analysis reflected the dominance of H. spongicola among Group III (I. campana and Topsentia sp.), and to a lesser extent, Group IV. The fact that there was a significant difference between Groups III and IV supports the previous statement. While the other groups were not statistically different, thereby limiting interpretation, there appears to be a distinction among groups based solely on the results of the cluster analysis. Groups I and II appeared to be shaped by a similarity in the abundances of multiple symbionts (Group I) or the presence of a few shared species (Group II, i.e., the ophiuroid, Ophioprium sp., sipunculids, and syllid polychaetes). The grouping of the tunicates indicated that while there was not a large overlap in symbiont species within the tunicates, they were still more similar to each other with respect to symbiont communities than to the sponges. The tunicates did share similar numbers of a few symbionts, such as the amphipods, E. punctatus, L. cf. spinicarpa, and syllid polychaetes. Interestingly, the results suggest that depth is not a large factor in shaping these faunal associate communities. The close associations between mobile invertebrates and sponges have led several researchers to maintain that a sponge can be characterized as an

117 ecological community (e.g., Tyler & Bo¨hlke 1972; Peattie & Hoare 1981; Westinga & Hoejtes 1981; Ilan et al. 1994). Analyses in the current study indicated that canal diameter appeared to influence symbiont density (negatively) and diversity (positively); however, additional samples would likely yield a clearer relationship. Interestingly, Ru¨tzler (1976) observed a significant negative relationship between sponge canal size and associate total number and a significant positive relationship between sponge canal size and associate weight. This was attributed to fewer niches offered by larger canal sizes that are occupied by fewer and larger organisms, while small canal sizes may contain more niches, which can support larger numbers of small-sized associates. In addition, while earlier studies and the results of the present study suggest that a relationship between sponge volume and species number does exist (Uebelacker 1977; Westinga & Hoejtes 1981; Villamizar & Laughlin 1991; Duarte & Nalesso 1996; Ribeiro et al. 2003), there may be no clear trend across species. In addition, due to the lack of many unique species found in the sponges relative to the surrounding environment (Dauer 1973; Wenner et al. 1983; the current study), these hosts may be more appropriately thought of as ‘‘city-like’’ communities as opposed to isolated islands. In an effort to better understand the role of sponges and tunicates as host organisms, faunal associate communities were compared with benthic infaunal samples collected concurrently by CCEHBR from collection sites in the current study. While there was no significant difference in the diversity between the two samples, suggesting that the benthos may serve as a source for many of the associated fauna, the densities of certain fauna differed between the benthos and the hosts, possibly due to the ability of certain species (e.g., H. spongicola) to flourish in the host. Interestingly, the fact that the benthic infaunal samples were generally more diverse suggests that only some species of infauna have a preference or ability to inhabit the sponge or tunicate hosts. This conclusion is also supported by differences in species composition; there was some overlap in species found in benthic samples and in the animal hosts, but only about a third of the most abundant benthic species were found in animal hosts.

Conclusions The current study, while limited in sample size, provides an important basis for future studies through an examination of sessile invertebrates and their complex faunal associate communities. The

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Fiore & Jutte

sponges and tunicates in this region play an important role in habitat structure; although several of the observed host taxa were reported by previous assessments in this region, four unique genera were collected by this study. A diverse and abundant assemblage of sponge and tunicate hosts contributes to the biodiversity of this area and provides a reproductive habitat for many species that are important trophic links to larger consumers. Acknowledgments. We would like to thank the rest of the thesis committee, G. Sedberry, C. Biernbaum, and M. Hughes, for support during the research period. Assistance throughout this project from scientists at the SCDNR was also greatly appreciated, in particular, S. Crowe, M. Levisen, G. Riekerk, R. Van Dolah, D. Knott, R. King, P. Weinbach, S. Burns, and M. Arendt. Thanks are due to J. Hyland, C. Cooksey, and the biologists at NOAA-NOS CCEHBR, Charleston, SC, for the benthic infaunal data. Sponge taxonomy would not have been possible without the help of G. Muricy, C. Diaz, and H. Reiswig. In addition, thanks are due to M. Zokan and D. Wyanski for fish identification. We are grateful to two anonymous reviewers for their critique of the manuscript. This project was funded by NOAA Ocean Exploration grants, NA16RP2697, NA03OAR4600097, NA04OAR46 00055. This is contribution 652 from SCDNR-MRD and 338 from GMBL.

References Barans JM Jr & Henry VJ Jr 1984. A description of shelf edge groundfish habitat along the southeastern United States. Northeast Gulf Sci. 7: 77–96. Barnes RD 1987. Invertebrate Zoology, 5th ed. pp. 263– 665. Saunders College Publishing, New York, NY, USA. Beaulieu S 2001a. Colonization of habitat islands in the deep sea: recruitment to glass sponge stalks. Deep-Sea Res. Part I Oceanogr. Res. Pap. 48: 1121–1137. FFF 2001b. Life on glass houses: sponge stalk communities in the deep sea. Mar. Biol. 138: 803–817. Biernbaum CK 1981. Seasonal changes in the amphipod fauna of Microciona prolifera (Ellis and Solander) (Porifera: Demospongia) and associated sponges in a shallow salt-marsh creek. Estuaries 4: 85–96. Bloom SA 1975. The motile escape response of a sessile prey; a sponge–scallop mutualism. J. Exp. Mar. Biol. Ecol. 17: 311–321. Brower JE, Zar JH, & von Ende CN 1997. Field and Laboratory Methods for General Ecology, 4th ed. pp. 177– 187. McGraw-Hill, Boston, MA, USA. Butler JN, Morris BF, Cadwallader J, & Stoner AW 1983. Studies of Sargassum and the Sargassum community. Bermuda Biol. Stn. Spec. Publ. 22: 1–307. Carlier A, Riera P, Amouroux JM, Bodiou JY, & Gre’mare A 2007. Benthic trophic network in the Bay of

Invertebrate Biology vol. 129, no. 2, spring 2010

Banyuls-sur-Mer (northwest Mediterranean, France): an assessment based on stable carbon and nitrogen isotopes analysis. Est. Coast Shelf Sci. 72: 1–15. Cartes JE, Huguet C, Parra S, & Sanchez F 2007. Trophic relationships in deep-water decapods of Le Danois bank (Cantabrian sea, NE Atlantic): trends related with depth and seasonal changes in food quality and availability. Deep-Sea Res. I 54: 1091–1110. Chao A, Chazdon RL, Colwell RK, & Shen TJ 2005. A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol. Lett. 8: 148–159. Christian RR & Luczkovich JJ 1999. Organizing and understanding a winter’s seagrass foodweb network through effective trophic levels. Ecol. Mod. 117: 99–124. Clarke KR 1993. Non-parametric multivariate analysis of changes in community structure. Aust. J. Ecol. 18: 117–143. Crowe SE & Thomas JD 2001. Abundance and distribution of commensal amphipods from common marine sponges of southeast Florida. In: Modern Approaches to The Study of Crustacea. Escobar-Briones E & Alvarez F, eds., pp. 105–110. Kluwer Academic/Plenum Publishers, New York, NY, USA. Dalby JE Jr 1996. Nemertean, copepod, and amphipod symbionts of the dimorphic ascidian Pyura stolonifera near Melbourne, Australia: specificities to host morphs and factors affecting prevelences. Mar. Biol. 126: 231– 243. Dauer DM 1973. Polychaete fauna associated with Gulf of Mexico sponges. Fla. Sci. 36: 192–196. Duarte LFL & Nalesso RC 1996. The sponge Zygomycale parishii (Bowerbank) and its endobiotic fauna. Estuar. Coast Shelf Sci. 42: 139–151. Duffy EJ 1990. Amphipods on seaweeds: partners or pests? Oecologia 83: 267–276. FFF 2002. The ecology and evolution of eusociality in sponge-dwelling shrimp. In: Genes, Behavior, and Evolution in Social Insects. pp. 217–254. Higashi S, ed., University of Hokkaido Press, Sapporo, Japan. Duffy JE & Hay ME 2000. Strong impacts of grazing amphipods on the organization of a benthic community. Ecol. Monogr. 70: 237–263. Duffy JE, Macdonald KS, Rhode JM, & Parker JD 2001. Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82: 2417–2434. Fauchald K & Jumars PA 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr. Mar. Biol. Annu. Rev. 17: 193–284. Fernando P & Sven Z 2003. Distribution and abundance of sponges of the genus Ircinia (Poriferea: Demospongiae) in the Santa Marta area, Colombian Caribbean. Bol. Investig. Mar. Costeras. 32: 75–91. Fiore CL 2005. Characterization of macrofaunal assemblages associated with sponges and tunicates off the southeastern United States. Master’s thesis, College of Charleston, Charleston, South Carolina. 122 pp.

Sponge- and tunicate-associated macrofauna Frick MG, Williams KL, Bolten AB, Bjorndal KA, & Martins HR 2003. Diet and fecundity of Columbus carbs, Planes minutus, associated with oceanic-stage loggerhead sea turtles, Caretta caretta, and inanimate flotsam. J. Crust. Biol. 24: 350–355. Frith DW 1976. Animals associated with sponges at North Hayling, Hampshire. Zool. J. Linn. Soc. 58: 353–362. Gore RH & Abele LG 1976. Shallow water porcelain crabs from the Pacific coast of Panama and adjacent Caribbean waters (Crustacea: Anomura: Porcellanidae). Smithson. Contrib. Zool. 237: 1–30. Grall J, Le Loc’h F, Guyonnet B, & Riera P 2006. Community structure and food web based on stable isotopes (d15N and d13C) analysis of a North Eastern Atlantic Maerl bed. J. Exp. Mar. Biol. Ecol. 338: 1–15. Griffin SB 2005. Reef morphology and invertebrate distribution at continental shelf edge reefs in the South Atlantic Bight. Master’s thesis, College of Charleston, Charleston, South Carolina. 94 pp. Hendler G 1984. The association of Ophiothrix lineata and Callyspongia vaginalis: a brittlestar-sponge cleaning symbiosis? Mar. Ecol. 5: 9–27. Hendler G, Miller JE, Pawson DL, & Kier PM 1995. Sea Stars, Sea Urchins, and Allies. pp. 90–195. Smithsonian Institution Press, Washington, DC, USA. Hooper JNA 2000. Guide to sponge collection and identification. Available at http://www.qm.qld.gov.au/organisation/ sections/SessileMarineInvertebrates/index.asp Hooper JNA & Van Soest RWM 2002. Systema Porifera, A Guide to the Classification of Sponges. Kluwer Academic/Plenum Publishers, New York. NY, USA. 1810 pp. Ilan M, Ben-Eliahu MN, & Galil BS 1994. Three deep water sponges from the eastern Mediterranean and their associated fauna. Ophelia 39: 45–54. Karas P, Gorny M, & Alarco´n-Mun˜oz R 2007. Experimental studies on the feeding ecology of Munida subrugosa (White, 1847) (Decapoda: Anomura: Galatheidae) from the Magellan region, southern Chile. Sci. Mar. 71: 187–190. Kennedy H, Richardson CA, Duarte CM, & Kenedy DP 2001. Diet and association of Pontonia pinnphylax occuring in Pinna nobilis: insights from stable isotope analysis. J. Mar. Biol. Assoc. UK 81: 177–178. Kunzmann K 1996. Associated fauna of selected sponges (Hexactinellida and Demospongiae) from the Weddell Sea, Antarctica. Ber. Palarforsch. 210: 1–93. Kvitek RG, Goldberg JD, Smith GJ, Doucette GJ, & Silver MW 2008. Domoic acid contamination within eight representative species from the benthic food web of Monteray Bay, California, USA. Mar. Ecol. Prog. Ser. 367: 35–47. Le Loc’h F & Hily C 2005. Stable carbon and nitrogen isotope analysis of Nephrops norvegicus/Meruccius merluccius fishing grounds in the Bay of Biscay (Northeast Atlantic). Can. J. Fish. Aquat. Sci. 62: 123–132. Magnino G & Gaino E 1998. Haplosyllis spongicola (Grube) (Polychaeta, Syllidae) associated with two spe-

119 cies of sponges from East Africa (Tanzania, Indian Ocean). Mar. Ecol. 19: 77–87. Margalef DR 1958. Information theory in ecology. Gen. Syst. 3: 36–71. Meroz E & Ilan M 1995. Cohabitation of a coral reef sponge and a colonials cyphozoan. Mar. Biol. 124: 453–459. Neves G & Omena E 2003. Influence of sponge morphology on the composition of the polychaete associated fauna from Rocas Atoll, northeast Brazil. Coral Reefs 22: 123–129. Nicotri ME 1980. Factors involved in herbivore food preference. J. Exp. Mar. Biol. Ecol. 42: 13–26. Nielson KJ 2001. Bottom-up and top-down forces in tide pools: test of a food chain model in an intertidal community. Ecol. Monogr. 71: 187–217. Pearse AS 1932. Inhabitants of certain sponges at Dry Tortugas. Carnegie Inst. 28: 117–124. Pearse AS & Williams LG 1951. The biota of the reefs of the Carolinas. J. Elisha Mitchell Sci. Soc. 67: 133– 161. Peattie ME & Hoare R 1981. The sublittoral ecology of the Menai Strait II. The sponge Halichondria panacea (Pallas) and its associated fauna. Estuar. Coast. Shelf Sci. 13: 621–635. Popenoe P & Manheim FT 2001. Origin and history of the Charleston Bump—geological formations, currents, bottom conditions, and their relationships to wreckfish habitats on the Blake Plateau. In: Island in the Stream: Oceanography and Fisheries of the Charleston Bump, American Fisheries Society, Symposium 25. Sedberry GR, ed., pp. 43–93. American Fisheries Society, Bethesda, MD, USA. Reiswig HM 1974. Water transport, respiration and energetics of three tropical marine sponges. J. Exp. Mar. Biol. Ecol. 14: 231–249. Reiswig HM & Champagne P 1995. The NE Atlantic glass sponges Pheronema carpenteri (Thomson) and P. grayi Kent (Porifera: Hexactinellida) are synonyms. Zool. J. Linn. Soc. 115: 373–384. Ribeiro SM, Omena EP, & Muricy G 2003. Macrofauna associated with Mycale microsigmatosa (Porifera, Demospongiae) in Rio de Janeiro State, SE Brazil. Estuar. Coast. Shelf Sci. 57: 951–959. Rios R & Duffy JE 1999. Description of Synalpheus williamsi, a new species of sponge-dwelling shrimp (Crustacea: Decapoda: Alpheidae), with remarks on its first larval stage. Proc. Biol. Soc. Wash. 112: 541–552. Ru¨tzler K 1976. Ecology of Tunisian commercial sponges. Tethys 7: 249–264. Sedberry GR, Cooksey CL, Crowe SE, Hyland J, Jutte PC, Ralph CM, & Sautter LR 2004. Characterization of deep reef habitat off the southeastern US, with particular emphasis on discovery, exploration and description of reef fish spawning sites. Final report, project number NA16RP2697. South Carolina Department of Natural Resources Marine Resources Research Institute, Charleston, SC, USA. 61 pp.

Invertebrate Biology vol. 129, no. 2, spring 2010

120 Schram FR 1986. Crustacea. pp. 3–334. Oxford University Press, New York, NY, USA. Sokal RR & Rohlf FJ 1995. Biometry, 3rd ed. pp. 423–541. W. H. Freeman and Company, New York, NY, USA. South Atlantic Fishery Management Council (SAFMC) 2004. Informational public hearing document on marine protected areas to be included in amendment 14 to the fishery management plan for the snapper grouper fishery of the South Atlantic region. Available at http:// www.safmc.net. Struhsaker P 1969. Demersal fish resources: composition, distribution, and commercial potential of the continental shelf stocks off southeastern United States. Fish. Indust. Res. 4: 261–300. Svavarsson J 1990. Life cycle and population dynamics of the symbiotic copepod Lichomolgus canui Sars associated with the ascidian Halocynthia pyriformis (Rathke). J. Exp. Mar. Biol. Ecol. 142: 1–12. Theil M 1999. Host-use and population demographics of the ascidian-dwelling amphipod Leucothoe spinicarpa — indication for extended parental care and advanced social behaviour. J. Nat. Hist. 33: 193–206. FFF 2000. Population and reproductive biology of two sibling amphipod species from ascidians and sponges. Mar. Biol. 137: 661–674. Thomas JD 1993. Identification Manual for the Marine Amphipoda: (Gammaridea) I. Common Coral Reef and Rocky Bottom Amphipods of South Florida. pp. 1–83. Florida Department of Environmental Protection, Tallahassee, FL. Thomas JD & Klebba KN 2006. Studies of commensal Leucothoid amphipods: two new sponge-inhabitaing species from south Florida and the western Caribbean. J. Crust. Biol. 26: 13–22. FFF 2007. New species and host associations of commensal leucothoid amphipods from coral reefs in Florida and Belize (Crustacea: Amphipoda). Zootaxa 1494: 1–44. Tyler JC & Bo¨hlke JE 1972. Records of the sponge-dwelling fishes, primarily of the Caribbean. Bull. Mar. Sci. 22: 601–642. Uebelacker JM 1977. Cryptofaunal species/area relationship in the coral reef sponge, Gelloides digitalis. Proc. Third Internat. Coral Reef Symp. 69–73.

Invertebrate Biology vol. 129, no. 2, spring 2010

Fiore & Jutte Uebelacker JM & Johnson PG 1984. Taxonomic Guide to the Polychaetes of Northern Gulf of Mexico. Vols. I– VII. Prepared for Minerals Management Service US Department of Interior. Barry A. Vittor & Assoc., Mobile, AL, USA. Van Dolah RF, Wendt PH, & Nicholson N 1987. Effects of a research trawl on a hard-bottom assemblage of sponges and corals. Fish. Res. 5: 39–54. Van Soest RWM 1994. Demosponge distribution patterns. In: Sponges in Time and Space: Biology, Chemistry, Paleontology. Van Soest RWM, Van Kempen, Theo MG, & Braekman J, eds., pp. 213–223. A. A. Balkema, Rotterdam, the Netherlands. Villamizar E & Laughlin RA 1991. Fauna associated with the sponges Aplysina archeri and Aplysina lacunosa in a coral reef of the Archipelago de Los Roques, National Park, Venezuela. In: Fossil and Recent Sponges. Reitner J & Keupp H, eds., pp. 522–542. Springer, Berlin, Germany. Wendt PH, Van Dolah RF, & O’Rourke C 1985. A comparative study of the invertebrate macrofauna associated with seven sponge and coral species collected from the South Atlantic Bight. J. Elisha Mitchell Sci. Soc. 101: 187–203. Wenner EL, Knott DM, Van Dolah RF, & Burrell VG 1983. Invertebrate communities associated with hard bottom habitats in the South Atlantic Bight. Estuar. Coast. Shelf Sci. 17: 143–158. Westinga E & Hoejtes PC 1981. The intrasponge fauna of Spheciospongia vesparia (Porifera, Demospongiae) at Curacao and Bonaire. Mar. Biol. 62: 139–150. Wulff JL 1994. Sponge feeding by Caribbean angelfishes, trunkfishes, and filefishes. In: Sponges in Time and Space. Van Soest RWM, Van Kempen TMG, & Braekman JC, eds., pp. 265–271. Balkema, Rotterdam, the Netherlands. Yakovis EL, Artemieva AV, Fokin MV, Grishankov AV, & Shunatova NN 2005. Patches of barnacles and ascidians in soft bottoms: associated motile fauna in relation to the surrounding assemblage. J. Exp. Mar. Biol. Ecol. 327: 210–224. Zimmerman R, Gibson R, & Harrington J 1979. Herbivory and detritivory among gammaridean amphipods from a Florida seagrass community. Mar. Biol. 54: 41–47.

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