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Deep-Sea Research II 55 (2008) 26572666

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Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2

Distribution, habitat use and ecology of deepwater Anemones (Actiniaria) in the Gulf of Mexico
Archie W. Ammons a,, Marymegan Daly b
a b

Department of Biology, Texas A&M University, MS 3258, College Station, TX 77843, USA Department of Evolution, Ecology, and Organismal Biology, Ohio State University, Columbus, OH 43210, USA

a r t i c l e in fo
Article history: Accepted 12 July 2008 Available online 6 September 2008 Keywords: Benthic environment Deep water Ecological associations Epipsammon Megafauna

abstract
The distribution of deepwater Actiniaria is poorly known. Rarely are these organisms identied to family, as this requires both well-preserved specimens and taxonomic expertise. Ecological information is similarly lacking. From the results of a comprehensive surveying program in the deep Gulf of Mexico, we report the occurrence of nine species of Actiniaria. For the most abundant four of these, we plot distributions and discuss habitat use, morphological variation, and feeding strategies. Actiniaria in the Gulf appear to have broad, basin-wide distributions with little depth preference. Faunal biomass is highest in the NE Gulf within submarine canyons or at the base of slope escarpments. Attachment mode is mostly opportunistic on various types of hard substrata, including trash. Sediment-dwelling forms are very abundant at an organically rich site within a large submarine canyon. & 2008 Published by Elsevier Ltd.

1. Introduction Among deep-sea benthic organisms, anthozoans comprise a signicant and often dominant fraction throughout the worlds oceans, with representatives known from depths greater than 6000 m (e.g., Carlgren, 1956; Menzies et al., 1973). Members of the Orders Pennatulacea (sea pens) and Ceriantharia (tube anemones) often dominate numerically, being specially adapted for living in soft sediments. True sea anemones (Order Actiniaria) are patchier in distribution, as many members require hard substrata for attachment. As much of the deep sea lacks such substrate, actiniarian species that must attach to substrata settle opportunistically, if at all. Although deepwater trawls may yield biased results regarding community structure (M. Wicksten, personal communication), they remain among the few tools available to deep-sea biologists for carrying out zoogeographic surveys (Gage and Tyler, 1991). The Deepwater Program: Gulf of Mexico Continental Slope Habitats and Benthic Ecology Project (DGoMB) conducted such a sampling program and its many trawls, covering a wide diversity of habitats, provide a rare opportunity to examine community structure at a basin-wide scale. A small oceanic basin bordered on three sides by continents, the Gulf of Mexico covers only 1.5 million km2, but possesses most of the geomorphic features found in larger basins. The continental margins are structurally complex, containing numerous canyons, hills, knolls, enclosed basins, and escarpments. Two-thirds of the Gulfs terrigenous inputs come from the Mississippi River, which
Corresponding author. Fax: +1 979 845 2891.

deposits the bulk of its sediments over the Mississippi Fan (Pequegnat, 1983). This feature covers over 10% of the seaoor and plays a signicant role in benthic faunal structure throughout most of the northcentral and northwestern Gulf. This and the myriad topographic features of the Gulf create a high diversity of benthic habitats within a relatively conned and isolated biogeographic area. Such an area is ideal for studying large-scale ecological processes. Actiniaria comprises over 1100 species worldwide (Fautin, 2006). Most species are sessile, attached to hard substrates. As with many marine invertebrates, shallow-water Actinaria are much better known than their deep-sea counterparts, which have been the focus of relatively few biogeographic or ecological studies. Many deepwater actiniarians have burrowing lifestyles. True burrowing actiniarians (i.e. Edwardsia) use a bulb-like physa to dig and anchor into sediments, in lieu of a broad, attened pedal disc. In the deep Gulf of Mexico (and other basins), some epilithic species live in sediments by grasping a ball of mud with the pedal disc. We consider this epipelic lifestyle ecologically similar to that of true burrowing species. Additional attachment substrates in the Gulf of Mexico include other animals and trash; we discuss the biogeographical, morphological, and ecological implications of these strategies.

2. Methods Deepwater trawls were carried out as part of the DGoMB 20002002. A 12.2 m otter trawl with 3.8-cm mesh was deployed from R.V. Gyre at 39 stations (Fig. 1) along the northern

E-mail address: archman@mail.bio.tamu.edu (A.W. Ammons). 0967-0645/$ - see front matter & 2008 Published by Elsevier Ltd. doi:10.1016/j.dsr2.2008.07.015

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95W 30N Texas

90W

85W

80W 30N N

0m 30 00m 0 1,
2, 00

Florida
0m

25N

3,0

00

25N 90W 85W 80W

95W

Fig. 1. Locations of DGoMB survey trawls. Water depths in m.

Table 1 DGoMB station data for voucher specimens of Actiniaria Species Actinauge longicornis Station Lat. 1N NB5 B3 S41 MT1 2MT1 26.250693 26.168170 28.072240 28.529045 28.552447 Long. 1W 91.240297 91.748757 86.677498 89.816425 89.838332 Depth (m) 21002110 23002620 29553030 420501 461 Date 9-May-00 10-May-00 9-June-00 17-June-00 3-June-01

the individuals encountered, belong to family Hormathiidae. Three other families (Actinoscyphiidae, Actinostolidae, Halcuriidae) also are reported from the region. Of these, only Actinoscyphiidae was encountered in the DGoMB trawls. Of the 86 deep-sea trawls, ranging in depth from 175 to 3720 m, 44 (51%) sampled actiniarians.

3.2. Hormathiidae In terms of diversity and biomass, the majority of deepwater Actiniaria we sampled from the Gulf of Mexico belong to Hormathiidae. Members of this family share many features, including a thick-walled column, a strong mesogleal marginal sphincter, and relatively short tentacles, and thus must be differentiated based on histological and anatomical details (Carlgren, 1949). Specimens belonging to Actinauge longicornis collected from DGoMB are white and moderate to large sized (50220 mm length; Fig. 2A). Unless wrapped around a sponge or a pennatulacean stalk, the diameters of the pedal disc and column are roughly equal. In its contracted state, a member of A. longicornis is ovoid or a squat cylinder. The oral disc is broad, with short, stout, pale violet marginal tentacles. The column bears small tubercles and a deciduous cuticle, giving it a rough texture. In many specimens of A. longicornis, the tubercles are fused distally; this is most pronounced in the largest specimens. A. longicornis is known from several sites in the west Atlantic and Caribbean, at depths 220580 m (summarized in Fautin, 2006). We found members of A. longicornis in three sites, at depths from 420 to 2620 m. This species was unusually abundant at the head of the Mississippi Submarine Canyon (station MT1), a site with highly occulent sediments. A repeat trawl in June 2001 conrmed the abundance of A. longicornis at MT1. Virtually all A. longicornis specimens (117 out of 120) from this site were epipelic rather than epilithic/epizooic. In terms of megafaunal biomass at the head of the Mississippi Submarine Canyon, A. longicornis comprised more than twice that of all other trawl organisms combined. Chondrophellia coronata is another moderate-sized anemone, with specimens ranging from 20 to 50 mm in diameter. Like A. longicornis, specimens of C. coronata collected in the DGoMB are white and bear tubercles that are fused distally (Fig. 2B). The two are distinguished by the presence of gametogenic tissue on the older mesenteries in members of Chondrophellia. The tentacles of freshly caught specimens of C. coronata were orange; this differs from the pale purple tentacles of A. longicornis. C. coronata is widespread. It is reported from the eastern and western North Atlantic and eastern Pacic, at depths from 600 to 3570 m (Verrill, 1883; Carlgren, 1942; Wolff, 1961; summarized in

Chondrophellia coronata MT5 MT6 MT1 Paraphelliactis sp. Stephanauge nexilis S35 B3 MT5 MT6 B3 B2b

27.263362 88.564210 20252410 4-June-00 27.037953 87.861228 26802790 5-June-00 28.529045 89.816425 420501 17-June-00 29.316083 87.045490 645695 12-June-00

26.168170 91.748757 23002620 10-May-00 27.263362 88.564210 20252410 4-June-00 27.037953 87.861228 26802790 5-June-00 26.168170 91.748757 23002620 10-May-00 26.613773 92.326848 21402330 19-June-00

Monactis vestita Actinoscyphia sp.

continental slope (37 trawls) and abyssal plain (5 trawls), recovering 321actiniarian specimens. These were immediately sorted to morphotype in the eld, enumerated, weighed, and then xed in 4% buffered formalin for storage at Texas A&M University. When possible, anemone mass was determined using volume displacement. This technique is commonly used for zooplankton hauls, provides more consistent measurements than wet weights, and can be performed quickly with many samples. Voucher specimens (Table 1) were identied by taxonomic specialists; then returned to Texas A&M University and used to identify the remaining specimens. Additional records for anemones in the Gulf of Mexico were gathered from expedition reports (19831985) of the Northern Gulf of Mexico Continental Slope Study (NGoMCSS). In situ observations were provided by close-up anemone and seaoor photographs taken in November 2000 from DSV Alvin during Atlantis voyage 3, leg 58 (Edge of the Gulf Cruise, chief scientist I. MacDonald). This cruise was partially funded by the DGoMB project, and visited sites in the Gulf of Mexico adjacent to many of the trawling areas.

3. Results 3.1. Actiniaria of the Gulf of Mexico Nine species of Actiniaria have been identied from the deep Gulf of Mexico (Table 2). Six of these, comprising the majority of

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Table 2 Deepwater Actiniaria identied from the Gulf of Mexico Depth range (m) Family Hormathiidae Actinauge longicornis (Verrill, 1882) Chondrophellia coronata (Verrill, 1883) Paraphelliactis sp. Stephanauge nexilis (Verrill, 1883) Monactis vestita (Gravier, 1918) Adamsia obvolva (Daly et al., 2004) Family Actinoscyphiidae Actinoscyphia (Stephenson, 1920) Family Actinostolidae Antholoba perdix (Verrill, 1882) Family Halcuriidae Halcurias pilatus (McMurrich, 1893) Records combined from DGoMB and NGoMCSS expedition logs.

4203030 4202790 645695 21003150 21003645a 375576

7512330

329475

342

Fig. 2. Members of Hormathiidae identied from trawls during DGoMB expeditions 20002002. (A) Actinauge longicornis. (B) Chondrophellia coronata. (C) Paraphelliactis sp. (D) Stephanauge nexilis. (E) Monactis vestita. (F) Adamsia obvolva.

Fautin, 2006). We recovered specimens of C. coronata from three sites in the Gulf of Mexico, from depths of 4202790 m. Near the base of the Mississippi Submarine Canyon (20252410 m), members of C. coronata were very common, constituting over one-third of the trawl biomass and being nearly as abundant as elasipodid holothurians. Unlike similarly abundant A. longicornis specimens at the top of the Mississippi Canyon, nearly all (66 of 69) C. coronata at the base of the canyon were attached to rock substrata. Other substrata to which we found this species attached include hexactinellid sponges and stalks of pennatulaceans. Only a single epipelic specimen was collected, at the detritus-rich head of the Mississippi Canyon. Paraphelliactis (Fig. 2C) is an exclusively deepwater genus whose members are similar to C. coronata and A. longicornis in size and general appearance. Paraphelliactis differs from Actinauge and Chondrophellia in having more mesenteries at the base than at the margin. Preserved specimens of C. coronata, A. longicornis, and Paraphelliactis sp. are extremely difcult to distinguish reliably based on general external appearance, and were generally lumped together as white sock anemones. This colloquial descriptive term refers to the color and sock-like appearance of contracted specimens has been used by local biologists since the late 1980s (M. Wicksten, personal communication). Zoogeographic distribution of white sock anemones is shown in Fig. 3. Specimens of an unidentied species of Paraphelliactis were collected on the upper continental slope (645695 m), at the top of the DeSoto Submarine Canyon. This is the rst reported occurrence of this genus from the Gulf of Mexico, and the shallowest occurrence for the genus. Dunn (1982) listed three species of Paraphelliactis, P. pabista, P. michaelsarsi, and P. spinosa, from British Columbia (2430 m), the Canary Islands (2603 m), and the Denmark Straits (1416 m), respectively. Four of the six specimens of Paraphelliactis recovered from the DeSoto Canyon were attached to rocks; the attachment mode of the remaining two could not be determined. These specimens could be assigned to Paraphelliactis because they all lacked cinclides and had more than 96 tentacles, but the internal morphology was poorly preserved, precluding more precise identication. Members of Stephanauge nexilis (Fig. 2D) are smaller than those of A. longicornis, C. coronata, or Paraphelliactis sp., with no specimens from the Gulf of Mexico exceeding 25 mm in diameter. The pedal disc and column of a member of this species are roughly equal in diameter, and the column is smooth. Color ranges from white or cream to dull orange. Specimens of S. nexilis have been reported from the NW Atlantic (40600 m; Fautin, 2005). Specimens often collected attached to octocorals (Carlgren, 1942; Widersten, 1976). In the Gulf of Mexico, we found S. nexilis restricted to the lower continental slope (42000 m), with greatest abundance at the base of the Mississippi Submarine Canyon (Fig. 3). It was not encountered at any of the abyssal plain stations. Collected specimens were all attached to (or recently detached from) rocks, dead shells, sponges, or pennatulaceans. Monactis vestita is unlike the other species of Hormathiidae collected in the Gulf of Mexico in appearance, in that its members form a low spreading mound in contraction (Fig. 2E). Specimens of M. vestita are small (o8 mm pedal disc diameter), with a broad pedal disc and a low, almost attened column. In contrast to the other hormathiids found in the Gulf of Mexico, the column wall of M. vestita is very thin, becoming transparent proximally. The overall color of the animal is pale white to pink. White et al. (1999) indicated that M. vestita occurs throughout the Atlantic basin and reported its occurrence within the abyssal NE Pacic. With the exception of three specimens collected 200250 m off of northern Argentina, all other specimens had been encountered on the lower continental slope or abyssal plain

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Fig. 3. Deepwater Actiniaria distributions in the northern Gulf of Mexico. Scaled circles indicate numerical counts from trawls. (A) White sock hormathiids, (B) Stephanauge nexilis and (C) Monactis vestita.

(22865320 m). In the Gulf of Mexico, we found specimens at depths 21003665 m (Fig. 3). A single specimen resembling M. vestita was collected at 340 m, but its identity was not conrmed. This species lives attached to hard substrate; in the Gulf of Mexico and Atlantic, these include rocks, wood, dead shells, and, in one case, a nutshell. In the NE Pacic, M. vestita has similar settlement habits, but its members also attach to live mollusc shells, possibly in a form of symbiosis (White et al., 1999). Adamsia obvolva is typically a symbiont of the hermit crab Sympagurus pictus (see Daly et al., 2004), and the only actiniarian species we found not reported outside the Gulf of Mexico. A. obvolva has a stout, orange-colored column with a wide, asymmetric pedal disc that enwraps the gastropod shell inhabited by the hermit crab (Fig. 2F). Tentacles are deep maroon. Because it is an obligate symbiont, the distribution of A. obvolva is largely shaped by the distribution of its host, rather than substrate type as in other actiniarians in the Gulf of Mexico. We found A. obvolva in association with two hosts not previously reported; the hermit crab Parapagurus pilosimanus and the buccinid gastropod Oocorys. We encountered A. obvolva at two locations within the upper Mississippi Canyon: at station MT2, we found two specimens in association with P. pilosimanus (Fig. 2F), and at MT1 three specimens were found on Oocorys. In

addition to the upper Mississippi Canyon, A. obvolva was found on S. pictus by earlier expeditions along the upper continental slopes off Louisiana, Mississippi, and south Texas (Daly et al., 2004). Its bathymetric range is from 375 to 737 m, and may be restricted to upper slope depths. The hermit crabs P. pilosimanus and S. pictus both range from outer continental shelf depths to over 2000 m (Lemaitre, 1989). Oocorys is favored by deepwater hermit crabs in the Gulf of Mexico, being both common and possessing a large aperture. The carcinoecium of A. obvolva bears supercial resemblance to shells of Oocorys.

3.3. Actinoscyphiid Flytrap Anemones The family Actinoscyphiidae is represented in the Gulf of Mexico by the genus Actinoscyphia. In members of this family, the diameter of the oral disc greatly exceeds that of the pedal disc. In life, the oral disc is typically held parallel to the substrate and perpendicular to the column (Fig. 4A) leading to the common rneck, 1978; name Venus Flytrap Anemones (e.g., Riemann-Zu Dunn, 1983). Two species of Actinoscyphia, A. saginata, and A. aurelia, were reported by Aldred et al. (1979) in the North Atlantic. Of these,

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A. saginata is far more common, occurring at depths of 7002200 m throughout the Atlantic, while A. aurelia is only known from the East Atlantic, primarily off of NW Africa. In the Gulf of Mexico, Actinoscyphia was encountered at four widely dispersed sites (Fig. 5). The single retained specimen was attached to the anchor spicules of a large hexactinellid sponge, and too damaged to identify to species. Actinoscyphia was reported by Aldred et al. (1979) and shown in photographs from various expeditions to lie upright and unattached on sediments (e.g., Fig. 4A). However, Dunn (1983) reported that the pedal discs of specimens of A. plebia appear to have been wrapped around thin cylindrical objects, and both Stephenson (1920) and Carlgren (1949) included attachment to worm-tubes or hexactinellid spicules as part of the diagnosis for the genus. 3.4. Other anemone species Small numbers of Antholoba perdix and Halcurias pilatus were reported by Gallaway et al. (1988) in the northern Gulf of Mexico during the 19831985 NGoMCSS expeditions. H. pilatus was only encountered at a single 342 m site in the north-central GoM. A. perdix was recovered from ve shallow sites in the northcentral and northeastern GoM, between 325 and 475 m. Neither of these records is associated with specimens or a narrative report of the living appearance, anatomy, or identication authority. H. pilatus has previously been reported from Chile (820 m), dredged by the

Albatross Expedition (McMurrich, 1893). A. perdix is known from the Northwest Atlantic (110210 m: Verrill, 1882; Widersten, 1976).

4. Discussion 4.1. Biogeography of Actiniaria in the Deep Gulf of Mexico Despite considerable deepwater sampling over the last 40 years, very little is known about populations of deepwater Actiniaria in the Gulf of Mexico. The most extensive megafaunal surveys were carried out by the R.V. Alaminos (19631972); however records of Actiniaria were omitted in the nal report (Pequegnat, 1983). This was not the case for the 19831985 surveys under the NGoMCSS, which included the actiniarians from both trawls and boxcores (Gallaway et al., 1988). Unfortunately, few voucher specimens were used to classify the NGoMCSS trawl samples. We believe this led to a misreporting of all white sock hormathiids as A. longicornis, limiting the utility of these records for our population analysis. Virtually, all preserved anemone specimens from both Alaminos and NGoMCSS expeditions were lost or destroyed over the years (M. Wicksten, personal communication). The collections made as part of the DGoMB expeditions thus represent the only remaining specimen collections of deepwater

Fig. 4. Upstream vs. downstream particle feeding in anemones. (A) Upstream feeding by Actinoscyphia, which has short tentacles relative to the large size of the oral disc, which typically has a concave surface in life. The oral disc can be oriented into the current and is thus efcient for upstream particle collection; it may also brush against sediments. (B) Downstream feeding demonstrated by unidentied actiniarian possessing long tentacles and smaller oral surface. The elongate tentacles trail downstream and are well suited for epibenthic detritophagy. Photographs taken during Alvin dives 3633 and 3634, respectively, in the northern Gulf of Mexico.

Fig. 5. Reported localities for Actinoscyphia in the Gulf of Mexico.

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Actiniaria from the Gulf of Mexico. From these, we have created the rst distribution maps of deepwater Actiniaria for this basin (Figs. 3 and 5). These maps show basin-wide distributions along the lower continental slope and abyssal plain for the smaller hormathiid species S. nexilis and M. vestita. The much larger white sock anemones also appear to be basin-wide, with a depth preference for the upper-mid continental slope. A. longicornis, C. coronata and the undescribed species of Paraphelliactis are very similar in appearance, and most animals could not be differentiated to species. The internal anatomy of many specimens was not adequately preserved, and the histological and nematocysts examinations required are laborious. Given the large numbers of individual specimens, the quality of their preservation, and the similarity of the white sock Hormathiid species, we were unable to identify all specimens to species, and this imprecision in identication precludes ner-scale analysis at this time. 4.2. Abundance of Actiniaria in the Deep Gulf of Mexico 4.2.1. High density/biomass areas At ve of the seven sites with high anemone biomass, the trawl samples comprised small numbers of exceptionally large anemones. Four of these low density, but high biomass sites were located along the lower slope of the west Florida Escarpment, while the fth was sited within the upper DeSoto Submarine Canyon (Fig. 6). All of these were within the eastern Gulf, in areas with little hard substrate other than an infrequent pebble or melon-sized rock. The remaining two high biomass sites also had high anemone abundance. Both of these high density and high biomass sites were within the Mississippi Canyon, at the top (420501 m) and near the bottom (20252410) of this prominent sub-sea feature. These two habitats differ tremendously in terms of sediment composition. The upper canyon sediments are 495% silts and clays with high amounts of occulent organic particles, maintaining a benthic environment prone to frequent burial. The lower canyon has far less silt or clay (o60%), and has rocks. The upper canyon site MT1 (Fig. 6) was surveyed again 12 months later, showing similarly high densities of the same dominant species (A. longicornis). A. longicornis is the most common actiniarian of the upper slope canyon, whereas C. coronata is more common in the deep canyon. Like many deepwater cnidarians (e.g., Actinoscyphia, Umbellula, Funiculina), both species have broad bathymetric ranges, and little is known regarding specic depth, settlement, and trophic preferences. Our study indicates that A. longicornis thrives in conditions poorly suited for sessile attachment. 4.2.2. High density/biomass areas outside the Gulf of Mexico George (1981) postulated that sedentary epifauna attain peak densities and biomass in areas of the deep sea where organic

matter accumulates, such as canyons and trench oors. Gage and Tyler (1991) noted that actiniarians were common in more productive and energetic marginal areas, where they attached to stones, shells, and boulders and attained large sizes. In the NE Atlantic, these patterns are clearly exemplied by the work of Thurston et al. (1994) in the Porcupine Abyssal Plain, where lumped Actiniaria (including cerianthids and some zoanthids) made up 22% of sled-collected megafauna, and 3.8% of the biomass; only holothurians were more abundant or had greater biomass. In the nearby Madeira Abyssal Plain, the abundance and biomass of Actiniaria were far lower (0.8% abundance and 0.1% biomass), perhaps reecting reduced phytodetrital inputs and the destructive effects of a large and recent turbidite (Thurston et al., 1994). Aldred et al. (1979) found high abundances Actinoscyphia aurelia at ve sites in the center of the West African upwelling region, one of which (Meteor station 100) has the highest known density of megafauna in the deep sea. This species is encountered only rarely elsewhere. Among the explanations for such high densities (0.355.50 per m2) of A. aurelia were extremely high surface productivity (200 g/carbon/m2/yr1) fueling particle feeding, and frequent environmental disturbances (e.g., slumps, turbidity currents) facilitating rapid dispersal and repopulation (Aldred et al., 1979). The surface waters overlying the upper Mississippi Canyon are among the most productive in the deep Gulf of Mexico, with springtime surface chlorophyll values at least twice that of any of our other deep Gulf survey sites (SeaWIFS year 2000 records). This productivity is fueled by nutrient exports from the Mississippi River, which also delivers massive amounts of ne sediment. Thus, conditions in the upper canyon are similar to those in the West African upwelling region (high surface productivity, frequent benthic disturbance), which may account for the abundance of A. longicornis. 4.3. Giant anemones Four large white sock hormathiids were recovered at three trawl stations along the lower continental slope between 1850 and 3050 m. Two of these sites, S40 and S41 (29503050 m), are adjacent at the base of the Florida Escarpment; the third (NB3, 18501910 m) is just outside of Atakapa Basin in the north-central Gulf. In terms of both physical size and volume displacement, these four animals are more than twice as large as all other anemones encountered in the DGoMB samples. These animals were all identied using internal anatomy and the sizes of cnidae from various parts of the body. The largest two animals, which we identied as A. longicornis, were collected at S41, have a contracted length of 210 and 220 mm, and each displaced more than 2000 ml. The smaller of these specimens (Fig. 7) had an epilithic habit; the pedal disc of the larger animal was packed with spicules, indicating that it had been attached to a large hexactinellid

Fig. 6. Trawl biomass plots for deepwater Actiniaria. Sites marked with the letter N denote both high abundance and high biomass. Station MT1 indicated with arrow.

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sponge. The epilithic specimen sampled nearby at S40 was physically smaller, yet still displaced approximately 900 ml. The large epilithic anemone found 700 km to the west at station NB3 was roughly equal in size to the one at S40, but its length and displacement were not directly measured. Deep-sea organisms are expected to have relatively low metabolic rates, slow growth, and increased longevity (George, 1981; Gage and Tyler, 1991; Thurston et al., 1994; Lauerman et al., 1996); sea anemones may have long life spans regardless of habitat (Shick, 1991). Rocky areas are rarely sampled with trawls or sleds, as the gear is easily tangled, damaged, or lost. We infer that the unusually large actiniarians are old, having taken advantage of hard substrata sheltered from burial or collection events. More of these giant anemones may be found in the Gulf of Mexico where large swathes of undisturbed hard substrate are present (i.e. escarpments, cold seeps, canyon walls).

4.4. Substrate and mode of attachment 4.4.1. Deep-sea trash Most species of Actiniaria are presently known from shallow water and are epilithic, attaching to rock, shell, and coral. Because such substrata are limited in the deep-sea, deepwater actiniarians either must be epibenthic oaters, opportunistic settlers, or rneck (1979) briey discussed oating burrowers. Riemann-Zu forms, which include members of a handful of genera (Actinostola, Bolocera, Liponema, Segonzactis) possessing unusually broad pedal discs. These animals neither burrow nor grasp substrate with the pedal disc; rather they oat within/atop the ooze-like nepheloid layer. Opportunistic substrates for settlement include other invertebrates such as scaphopods, hermit crabs, and sponges; manganese nodules (e.g., Bathyphellia australis Dunn, 1983); whale skeletons (Foell and Pawson, 1986; Daly and Gusmao, 2007) and trash. Large quantities of human-generated trash were encountered during the DGoMB cruises. Although the long-term ecological effects of deep-sea trash are presently unknown, much of this trash serves as attachment for epilithic faunas such as serpulid worms, barnacles, zoanthids, and actiniarians (Fig. 8A). On one occasion, we found more than 50 juvenile anemones attached to a garbage sack; at the top of the Mississippi Submarine Canyon, we observed a few adult A. longicornis attached to fragments of crockery (Fig. 8B), alongside identically sized specimens on rocks. Because availability of hard substrate regulates distributions of many sessile invertebrates (Lauerman et al., 1996), man-made trash in the deep sea could have signicant local-scale ecological effects, altering recruitment and population structure for deep-sea invertebrates.

Fig. 7. Giant A. longicornis from the base of the West Florida Escarpment (29553030 m). This animal has been removed from the rock to which it was attached. Two specimens of this size and morphology were recovered from the trawl site.

4.4.2. Actiniaria living on soft sediments Actiniarians use two primary modes of anchoring in soft sediments. True burrowing anemones have a bulbous or mushroom-shaped physa rather than a attened pedal disk. The physa is used to excavate/anchor in soft sediment (Williams, 1981; Ansell and Peck, 2000). We found no true burrowing anemones in these trawls. We suspect that their absence reects sampling method rather than actual distributions of burrowing anemones;

Fig. 8. Actiniarians attached to man-made trash. (A) Unidentied anemones (indicated by arrows) attached to discarded metal drum (overlaid by plastic mesh) at the base of the North Florida Escarpment. Photograph taken during Alvin dive 3644. (B) Actinauge longicornis attached to fragment of crockery from the top of the Mississippi Canyon. Dark material coating body column is detritus from surface sediments.

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burrowing forms typically retract below the sediment interface when disturbed (i.e. when a trawl approaches) and specimens are typically smaller in diameter and length than the trawl mesh size of 3.8 cm. Alternatively, some epipelic actiniarians use the pedal disk to grasp a ball of sediment. This mode of attachment has been documented for several species of Hormathiidae (e.g., Verrill, 1883; McMurrich, 1893; Carlgren, 1934; Dunn, 1982; Riemann rneck, 1986; see Fig. 9C) and was described in detail by George Zu (1981) for Actinauge rugosa collected from the Northern Blake Plateau off North Carolina. In the laboratory, captive A. rugosa formed mud balls when in contact with organically rich substrate. A nutritional explanation for this was hypothesized by George (1981) but not tested. Lampitt and Patterson (1987) hypothesized that in grasping a mud ball, Sicyonis tuberculata countered the dislodgement forces of near-bottom currents. Actiniaria anchoring themselves by grasping sediment were recovered from 3 of the 39 stations surveyed in the DGoMB trawls. All of these sites had the soft sediment bottoms typical of most deep-sea environments. Station MT1 at the top of the Mississippi Submarine Canyon (420500 m) had extremely occulent sedi-

ment that was highly enriched with detritus. In addition to A. longicornis, we collected high numbers of the thin-shelled mytilid Amygdalum politum encapsulated in dense mud cocoons. The macrofauna was dominated by scavenging amphipods. Levin et al. (2000) found a similar community in the oxygen minimum zones (OMZs) of the deep NW Arabian Sea. The site at the top of the Mississippi Canyon had the highest biomass and the second highest abundance values for anemones in the Gulf of Mexico (Fig. 6); 97% of the anemones at this site were grasping mud balls. The only other site at which we collected anemones grasping a mud ball was survey station C1, 95 km southwest of the upper Mississippi Canyon station. At this site, four unidentied white sock hormathiids were recovered, two of which clearly had a pedal disc grasping a ball of sediment. Station C1 and MT1 are both relatively shallow (310320 m), and both are within close range of the Mississippi Canyon. Despite these general similarities, MT1 is the most ecologically distinct non-chemoautotrophic deepwater habitat in the Gulf of Mexico, and is not faunistically similar to any other sample area. Because soft sediments characterize of much of the deep-sea oor (Heezen and Hollister, 1971; Menzies et al., 1973; Marshall, 1979; Gage and Tyler, 1991), burrowing and mud grasping Actiniaria have an advantage over epilithic forms as colonizers of deep-sea sediments. Furthermore, species that have a pedal disc capable of both attaching to hard substrates and grasping mud have a broader array of habitats open to them than do species that can only attach to hard substrates or burrow in soft sediments. The ability to grasp sediment may also provide a means of recovering from dislodgement from hard substrata as rocks, sponges, or shells may allow an animal greater motility, or may enable the animal to avoid burial. Both Aldred et al. (1979) and Foell and Pawson (1986) argued that horizontal surface ows (of either water or sediments) might be favored as dispersal mode by specic anemones. Foell and Pawson (1986) hypothesized that food gathering was enhanced by the motility of the large solitary anemone they observed rolling along the bottom in the abyssal NE Pacic. Alternatively, Aldred et al. (1979) postulated that frequent sediment movements in the east Atlantic facilitated the colonization efforts of Actinoscyphia. Epibenthic oating actiniarians (i.e. Segonzactis) may have enhanced dispersal potential because of increased motility. We concur that mud ball grasping has probably facilitated the colonization of the deep Gulf of Mexico by A. longicornis (and possibly by C. coronata and Paraphelliactis), although the amount of sediment enclosed by the pedal disc is small and likely insufcient to maintain anchorage in any but the lightest currents. However, the weight of the sediment bolus would keep the animal properly oriented upon resettlement, at which point it could dig into the sediment to form a new mud ball or replenish its existing one. This is a highly efcient dispersion method with little energetic loss to the anemone. 4.4.3. Morphological variation associated with attachment mode The mode of attachment may shape an individuals morphology. This is most evident in animals that attach to pennatulacean stalks or the anchor spicules of hexactinellid sponges (Fig. 9A and B); an attached animal typically has a pedal disc that is generally wider than does an animal grasping a mud ball or attached to rocks (Fig. 9D). Additionally, in comparison to a mud ball grasping specimen, the body column of an epizooic specimen is typically shorter, and the fused tubercles may be more prominent. A specimen grasping a mud ball often has the pedal disc retracted inside the column (Fig. 9C); the aperture at the aboral end is caused by a constriction of the proximal column around the ball of mud grasped by the pedal disc. This aperture was erroneously referred to as an anus (George, 1981).

Fig. 9. Epizoic and epipelic attachment by Hormathiidae. (A) Epizoic white sock hormathiid (arrow) with pedal disc wrapped around hexactinellid anchor spicules. (B) Actinauge longicornis on pennatulacean stalk. (C) Mud-ball grasping specimen of A. longicornis. The pedal disc is withdrawn inside the proximal column, leaving only a small aperture formed by constriction of the column. (D) Living epipelic white sock hormathiid presumably anchored by grasping a ball of mud. Photograph taken east of Mississippi Canyon ($1900 m) during Alvin dive 3633.

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4.5. Feeding strategies and growth The 74 specimens of A. longicornis collected at the top of the Mississippi Canyon (MT1) were remarkably similar in size ($70 mm long) and shape. A repeat trawl at this site 1 year later collected many specimens of A. longicornis (n 46) that were roughly 10 mm longer than the previous years catch. We infer that the anemones collected during both trawls were of the same cohort, and that the 10 mm increase represents a years growth. Such rapid growth may be attributed to the massive organic matter inputs from the Mississippi River. Shick (1991) postulated that burrowing anemones might be able to take advantage of enhanced dissolved organic matter in sediments, a hypothesis supported by Georges (1981) observation of captive A. rugosa showing a preference for burrowing in sediments rich in organic matter. et (1985) showed that anemones can uptake dissolved Van-Pra nutrients (amino acids, glucose) across the ectoderm. In the shallow-water anemone Anemonia sulcata, up to 50% of energy needs were met through this mode. Such epidermal feeding can be enhanced via extensions of the body column, expansion of the oral disc, and projections of tentacles. In the highly oligotrophic waters of the deep sea, direct nutrient uptake is probably not a signicant energy source, except possibly in detritus-rich canyons and other depocenters. Burrowing species may be able to exploit the dissolved organic content within the sediment, which may exceed that of overlying waters by an order of magnitude (Gage and Tyler, 1991). Such a nutritional benet may explain the high abundance and biomass values for mud ball grasping Actiniaria at the top of the Mississippi Submarine Canyon, where sediments are unusually rich in detritus. Although feeding behavior of deepwater Actiniaria has not been directly observed in the Gulf of Mexico, studies with ecologically and taxonomically similar species provide some insight into nutrition in deepwater anemones in the Gulf of et (1985) identied Phelliactis robusta and Mexico. Van-Pra Actinoscyphia as well as adapted for particle feeding, possessing a ciliated epidermis ideal for retaining micro zooplankton, phytoplankton, and detritus; these same attributes characterize Actinauge, Chondrophellia, and Paraphelliactis. Feeding strategies have been well documented for S. tuberculata, a deep-sea species that has an oral disc morphology similar to that of Actinoscyphia. Lampitt and Patterson (1987) observed S. tuberculata in the abyssal NE Atlantic and noted that the oral disc was actively oriented into the current. We observed similar orientation in Actinoscyphia in the Gulf of Mexico (Fig. 4A). This contrasts with the downstream particle feeding seen in some other actiniarians (Fig. 4B), in which tentacles are carried by the current. Based on the prey items found in gut content analysis (including planktonic foraminifera, sh scales, and a Plesiopenaeus shrimp nearly as large as the anemone that ingested it), Lampitt and Patterson (1987) hypothesized that S. tuberculata captured planktonic and epibenthic prey and also caught material when the tentacles brushed against the sediment.

Hubbard, Lindsey Loughry, Erin Moyer, Clifton Nunnally, photographers aboard DSV Alvin, and the crew of R.V. Gyre. M.D. acknowledges support from NSF Grants DEB 9978106 (to D. G. Fautin in the PEET program) and DEB 0415277. References
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Acknowledgements This project was supported by the Minerals Management Service, as part of the Deepwater Program: Gulf of Mexico Continental Slope Habitats and Benthic Ecology Study (#30991). Adorian Ardelean, Ha-Rim Cha, and Daphne Fautin of the University of Kansas contributed valuable taxonomic expertise. Mary Wicksten (TAMU) and Daphne Fautin (University of Kansas) provided valuable comments as reviewers. We would also like to thank Erin Brewer, Sophie DeBeukelaer, Thomas Decker, Fain

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