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Deep-Sea Research II 55 (2008) 2657–2666

Contents lists available at ScienceDirect

Deep-Sea Research II

0967-06

doi:10.1

� Corr

E-m

journal homepage: www.elsevier.com/locate/dsr2

Distribution, habitat use and ecology of deepwater Anemones (Actiniaria) inthe Gulf of Mexico

Archie W. Ammons a,�, Marymegan Daly b

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

a r t i c l e i n f o

Article history:

Accepted 12 July 2008The distribution of deepwater Actiniaria is poorly known. Rarely are these organisms identified to

family, as this requires both well-preserved specimens and taxonomic expertise. Ecological information

Available online 6 September 2008

Keywords:

Benthic environment

Deep water

Ecological associations

Epipsammon

Megafauna

45/$ - see front matter & 2008 Published by

016/j.dsr2.2008.07.015

esponding author. Fax: +1979 845 2891.

ail address: archman@mail.bio.tamu.edu (A.W

a b s t r a c t

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 asignificant and often dominant fraction throughout the world’soceans, with representatives known from depths greater than6000 m (e.g., Carlgren, 1956; Menzies et al., 1973). Members of theOrders Pennatulacea (sea pens) and Ceriantharia (tube anemones)often dominate numerically, being specially adapted for living in softsediments. True sea anemones (Order Actiniaria) are patchier indistribution, as many members require hard substrata for attach-ment. As much of the deep sea lacks such substrate, actiniarianspecies that must attach to substrata settle opportunistically, if at all.

Although deepwater trawls may yield biased results regardingcommunity structure (M. Wicksten, personal communication),they remain among the few tools available to deep-sea biologistsfor carrying out zoogeographic surveys (Gage and Tyler, 1991). TheDeepwater Program: Gulf of Mexico Continental Slope Habitatsand Benthic Ecology Project (DGoMB) conducted such a samplingprogram and its many trawls, covering a wide diversity ofhabitats, provide a rare opportunity to examine communitystructure 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 mostof the geomorphic features found in larger basins. The continentalmargins are structurally complex, containing numerous canyons,hills, knolls, enclosed basins, and escarpments. Two-thirds of theGulf’s terrigenous inputs come from the Mississippi River, which

Elsevier Ltd.

. Ammons).

deposits the bulk of its sediments over the Mississippi Fan(Pequegnat, 1983). This feature covers over 10% of the seafloor andplays a significant role in benthic faunal structure throughoutmost of the northcentral and northwestern Gulf. This and themyriad topographic features of the Gulf create a high diversity ofbenthic habitats within a relatively confined and isolated biogeo-graphic area. Such an area is ideal for studying large-scaleecological processes.

Actiniaria comprises over 1100 species worldwide (Fautin,2006). Most species are sessile, attached to hard substrates. Aswith many marine invertebrates, shallow-water Actinaria aremuch better known than their deep-sea counterparts, which havebeen the focus of relatively few biogeographic or ecologicalstudies. Many deepwater actiniarians have burrowing lifestyles.True burrowing actiniarians (i.e. Edwardsia) use a bulb-like physato dig and anchor into sediments, in lieu of a broad, flattened pedaldisc. In the deep Gulf of Mexico (and other basins), some epilithicspecies live in sediments by grasping a ball of mud with the pedaldisc. We consider this epipelic lifestyle ecologically similar to thatof true burrowing species. Additional attachment substrates in theGulf of Mexico include other animals and trash; we discuss thebiogeographical, morphological, and ecological implications ofthese strategies.

2. Methods

Deepwater trawls were carried out as part of the DGoMB2000–2002. A 12.2 m otter trawl with 3.8-cm mesh was deployedfrom R.V. Gyre at 39 stations (Fig. 1) along the northern

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95°°W 90°W 85°W 80°W

30°NN

25°N

30°NTexas

300m

1,000m

2,000m

3,000m

Florida

25°N

95°W 90°W 85°W 80°W

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

Table 1DGoMB station data for voucher specimens of Actiniaria

Species Station Lat. 1N Long. 1W Depth (m) Date

Actinauge longicornis NB5 26.250693 91.240297 2100–2110 9-May-00

B3 26.168170 91.748757 2300–2620 10-May-00

S41 28.072240 86.677498 2955–3030 9-June-00

MT1 28.529045 89.816425 420–501 17-June-00

2MT1 28.552447 89.838332 461 3-June-01

Chondrophellia coronata MT5 27.263362 88.564210 2025–2410 4-June-00

MT6 27.037953 87.861228 2680–2790 5-June-00

MT1 28.529045 89.816425 420–501 17-June-00

Paraphelliactis sp. S35 29.316083 87.045490 645–695 12-June-00

Stephanauge nexilis B3 26.168170 91.748757 2300–2620 10-May-00

MT5 27.263362 88.564210 2025–2410 4-June-00

MT6 27.037953 87.861228 2680–2790 5-June-00

Monactis vestita B3 26.168170 91.748757 2300–2620 10-May-00

Actinoscyphia sp. B2b 26.613773 92.326848 2140–2330 19-June-00

A.W. Ammons, M. Daly / Deep-Sea Research II 55 (2008) 2657–26662658

continental slope (37 trawls) and abyssal plain (5 trawls),recovering 321actiniarian specimens. These were immediatelysorted to morphotype in the field, enumerated, weighed, and thenfixed in 4% buffered formalin for storage at Texas A&M University.When possible, anemone mass was determined using volumedisplacement. This technique is commonly used for zooplanktonhauls, provides more consistent measurements than wet weights,and can be performed quickly with many samples. Voucherspecimens (Table 1) were identified by taxonomic specialists;then returned to Texas A&M University and used to identify theremaining specimens.

Additional records for anemones in the Gulf of Mexico weregathered from expedition reports (1983–1985) of the NorthernGulf of Mexico Continental Slope Study (NGoMCSS). In situ

observations were provided by close-up anemone and seafloorphotographs taken in November 2000 from DSV Alvin duringAtlantis voyage 3, leg 58 (‘‘Edge of the Gulf Cruise’’, chief scientist I.MacDonald). This cruise was partially funded by the DGoMBproject, and visited sites in the Gulf of Mexico adjacent to many ofthe trawling areas.

3. Results

3.1. Actiniaria of the Gulf of Mexico

Nine species of Actiniaria have been identified from the deepGulf of Mexico (Table 2). Six of these, comprising the majority of

the individuals encountered, belong to family Hormathiidae.Three other families (Actinoscyphiidae, Actinostolidae, Halcurii-dae) also are reported from the region. Of these, only Actinoscy-phiidae was encountered in the DGoMB trawls. Of the 86 deep-seatrawls, ranging in depth from 175 to 3720 m, 44 (51%) sampledactiniarians.

3.2. Hormathiidae

In terms of diversity and biomass, the majority of deepwaterActiniaria we sampled from the Gulf of Mexico belong toHormathiidae. Members of this family share many features,including a thick-walled column, a strong mesogleal marginalsphincter, and relatively short tentacles, and thus must bedifferentiated based on histological and anatomical details(Carlgren, 1949).

Specimens belonging to Actinauge longicornis collected fromDGoMB are white and moderate to large sized (50–220 mmlength; Fig. 2A). Unless wrapped around a sponge or a pennatu-lacean stalk, the diameters of the pedal disc and column areroughly equal. In its contracted state, a member of A. longicornis isovoid or a squat cylinder. The oral disc is broad, with short, stout,pale violet marginal tentacles. The column bears small tuberclesand a deciduous cuticle, giving it a rough texture. In manyspecimens of A. longicornis, the tubercles are fused distally; this ismost pronounced in the largest specimens.

A. longicornis is known from several sites in the west Atlanticand Caribbean, at depths 220–580 m (summarized in Fautin,2006). We found members of A. longicornis in three sites, at depthsfrom 420 to 2620 m. This species was unusually abundant at thehead of the Mississippi Submarine Canyon (station MT1), a sitewith highly flocculent sediments. A repeat trawl in June 2001confirmed the abundance of A. longicornis at MT1. Virtually allA. longicornis specimens (117 out of 120) from this site wereepipelic rather than epilithic/epizooic. In terms of megafaunalbiomass at the head of the Mississippi Submarine Canyon,A. longicornis comprised more than twice that of all other trawlorganisms combined.

Chondrophellia coronata is another moderate-sized anemone,with specimens ranging from 20 to 50 mm in diameter. LikeA. longicornis, specimens of C. coronata collected in the DGoMB arewhite and bear tubercles that are fused distally (Fig. 2B). The twoare distinguished by the presence of gametogenic tissue on theolder mesenteries in members of Chondrophellia. The tentacles offreshly caught specimens of C. coronata were orange; this differsfrom the pale purple tentacles of A. longicornis.

C. coronata is widespread. It is reported from the eastern andwestern North Atlantic and eastern Pacific, at depths from 600 to3570 m (Verrill, 1883; Carlgren, 1942; Wolff, 1961; summarized in

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Table 2Deepwater Actiniaria identified from the Gulf of Mexico

Depth range (m)

Family Hormathiidae

Actinauge longicornis (Verrill, 1882) 420–3030

Chondrophellia coronata (Verrill, 1883) 420–2790

Paraphelliactis sp. 645–695

Stephanauge nexilis (Verrill, 1883) 2100–3150

Monactis vestita (Gravier, 1918) 2100–3645a

Adamsia obvolva (Daly et al., 2004) 375–576

Family Actinoscyphiidae

Actinoscyphia (Stephenson, 1920) 751–2330

Family Actinostolidae

Antholoba perdix (Verrill, 1882) 329–475

Family Halcuriidae

Halcurias pilatus (McMurrich, 1893) 342

Records combined from DGoMB and NGoMCSS expedition logs.

Fig. 2. Members of Hormathiidae identified from trawls during DGoMB expedi-

tions 2000–2002. (A) Actinauge longicornis. (B) Chondrophellia coronata. (C)

Paraphelliactis sp. (D) Stephanauge nexilis. (E) Monactis vestita. (F) Adamsia obvolva.

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Fautin, 2006). We recovered specimens of C. coronata from threesites in the Gulf of Mexico, from depths of 420–2790 m. Near thebase of the Mississippi Submarine Canyon (2025–2410 m),members of C. coronata were very common, constituting overone-third of the trawl biomass and being nearly as abundant aselasipodid holothurians. Unlike similarly abundant A. longicornis

specimens at the top of the Mississippi Canyon, nearly all (66 of69) C. coronata at the base of the canyon were attached to rocksubstrata. Other substrata to which we found this speciesattached include hexactinellid sponges and stalks of pennatula-ceans. Only a single epipelic specimen was collected, at thedetritus-rich head of the Mississippi Canyon.

Paraphelliactis (Fig. 2C) is an exclusively deepwater genuswhose members are similar to C. coronata and A. longicornis in sizeand general appearance. Paraphelliactis differs from Actinauge andChondrophellia in having more mesenteries at the base than at themargin. Preserved specimens of C. coronata, A. longicornis, andParaphelliactis sp. are extremely difficult to distinguish reliablybased on general external appearance, and were generally lumpedtogether as ‘‘white sock’’ anemones. This colloquial descriptiveterm refers to the color and sock-like appearance of contractedspecimens has been used by local biologists since the late 1980s(M. Wicksten, personal communication). Zoogeographic distribu-tion of ‘‘white sock’’ anemones is shown in Fig. 3.

Specimens of an unidentified species of Paraphelliactis werecollected on the upper continental slope (645–695 m), at the topof the DeSoto Submarine Canyon. This is the first reportedoccurrence of this genus from the Gulf of Mexico, and theshallowest occurrence for the genus. Dunn (1982) listed threespecies of Paraphelliactis, P. pabista, P. michaelsarsi, and P. spinosa,

from British Columbia (2430 m), the Canary Islands (2603 m), andthe Denmark Straits (1416 m), respectively. Four of the sixspecimens of Paraphelliactis recovered from the DeSoto Canyonwere attached to rocks; the attachment mode of the remainingtwo could not be determined. These specimens could be assignedto Paraphelliactis because they all lacked cinclides and had morethan 96 tentacles, but the internal morphology was poorlypreserved, precluding more precise identification.

Members of Stephanauge nexilis (Fig. 2D) are smaller than thoseof A. longicornis, C. coronata, or Paraphelliactis sp., with nospecimens from the Gulf of Mexico exceeding 25 mm in diameter.The pedal disc and column of a member of this species are roughlyequal in diameter, and the column is smooth. Color ranges fromwhite or cream to dull orange.

Specimens of S. nexilis have been reported from the NWAtlantic (40–600 m; Fautin, 2005). Specimens often collectedattached to octocorals (Carlgren, 1942; Widersten, 1976). In theGulf of Mexico, we found S. nexilis restricted to the lowercontinental slope (42000 m), with greatest abundance at thebase of the Mississippi Submarine Canyon (Fig. 3). It was notencountered at any of the abyssal plain stations. Collectedspecimens were all attached to (or recently detached from) rocks,dead shells, sponges, or pennatulaceans.

Monactis vestita is unlike the other species of Hormathiidaecollected in the Gulf of Mexico in appearance, in that its membersform a low spreading mound in contraction (Fig. 2E). Specimens ofM. vestita are small (o8 mm pedal disc diameter), with a broadpedal disc and a low, almost flattened column. In contrast to theother hormathiids found in the Gulf of Mexico, the column wall ofM. vestita is very thin, becoming transparent proximally. Theoverall color of the animal is pale white to pink.

White et al. (1999) indicated that M. vestita occurs throughoutthe Atlantic basin and reported its occurrence within the abyssalNE Pacific. With the exception of three specimens collected200–250 m off of northern Argentina, all other specimens hadbeen 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.

A.W. Ammons, M. Daly / Deep-Sea Research II 55 (2008) 2657–26662660

(2286–5320 m). In the Gulf of Mexico, we found specimens atdepths 2100–3665 m (Fig. 3). A single specimen resemblingM. vestita was collected at 340 m, but its identity was notconfirmed. This species lives attached to hard substrate; in theGulf of Mexico and Atlantic, these include rocks, wood, deadshells, and, in one case, a nutshell. In the NE Pacific, M. vestita hassimilar settlement habits, but its members also attach to livemollusc shells, possibly in a form of symbiosis (White et al., 1999).

Adamsia obvolva is typically a symbiont of the hermit crabSympagurus pictus (see Daly et al., 2004), and the only actiniarianspecies 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 inhabitedby the hermit crab (Fig. 2F). Tentacles are deep maroon. Because itis an obligate symbiont, the distribution of A. obvolva is largelyshaped by the distribution of its host, rather than substrate typeas in other actiniarians in the Gulf of Mexico.

We found A. obvolva in association with two hosts notpreviously reported; the hermit crab Parapagurus pilosimanus

and the buccinid gastropod Oocorys. We encountered A. obvolva attwo locations within the upper Mississippi Canyon: at stationMT2, 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 onS. pictus by earlier expeditions along the upper continental slopesoff Louisiana, Mississippi, and south Texas (Daly et al., 2004). Itsbathymetric range is from 375 to 737 m, and may be restricted toupper 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 inthe Gulf of Mexico, being both common and possessing a largeaperture. The carcinoecium of A. obvolva bears superficialresemblance to shells of Oocorys.

3.3. Actinoscyphiid ‘‘Flytrap Anemones’’

The family Actinoscyphiidae is represented in the Gulf ofMexico by the genus Actinoscyphia. In members of this family, thediameter of the oral disc greatly exceeds that of the pedal disc. Inlife, the oral disc is typically held parallel to the substrate andperpendicular to the column (Fig. 4A) leading to the commonname ‘‘Venus Flytrap Anemones’’ (e.g., Riemann-Zurneck, 1978;Dunn, 1983).

Two species of Actinoscyphia, A. saginata, and A. aurelia, werereported by Aldred et al. (1979) in the North Atlantic. Of these,

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A. saginata is far more common, occurring at depths of700–2200 m throughout the Atlantic, while A. aurelia is onlyknown from the East Atlantic, primarily off of NW Africa. In theGulf of Mexico, Actinoscyphia was encountered at four widelydispersed sites (Fig. 5). The single retained specimen was attachedto the anchor spicules of a large hexactinellid sponge, and toodamaged to identify to species. Actinoscyphia was reported byAldred et al. (1979) and shown in photographs from variousexpeditions to lie upright and unattached on sediments (e.g.,Fig. 4A). However, Dunn (1983) reported that the pedal discs ofspecimens of A. plebia appear to have been wrapped around thincylindrical objects, and both Stephenson (1920) and Carlgren(1949) included attachment to worm-tubes or hexactinellidspicules as part of the diagnosis for the genus.

3.4. Other anemone species

Small numbers of Antholoba perdix and Halcurias pilatus werereported by Gallaway et al. (1988) in the northern Gulf of Mexicoduring the 1983–1985 NGoMCSS expeditions. H. pilatus was onlyencountered at a single 342 m site in the north-central GoM.A. perdix was recovered from five shallow sites in the northcentraland northeastern GoM, between 325 and 475 m. Neither of theserecords is associated with specimens or a narrative report of theliving appearance, anatomy, or identification authority. H. pilatus

has previously been reported from Chile (820 m), dredged by the

Fig. 4. Upstream vs. downstream particle feeding in anemones. (A) Upstream feeding b

which typically has a concave surface in life. The oral disc can be oriented into the curr

sediments. (B) Downstream feeding demonstrated by unidentified actiniarian possessin

and are well suited for epibenthic detritophagy. Photographs taken during Alvin dives

Fig. 5. Reported localities for Actino

Albatross Expedition (McMurrich, 1893). A. perdix is known fromthe Northwest Atlantic (110–210 m: Verrill, 1882; Widersten,1976).

4. Discussion

4.1. Biogeography of Actiniaria in the Deep Gulf of Mexico

Despite considerable deepwater sampling over the last40 years, very little is known about populations of deepwaterActiniaria in the Gulf of Mexico. The most extensive megafaunalsurveys were carried out by the R.V. Alaminos (1963–1972);however records of Actiniaria were omitted in the final report(Pequegnat, 1983). This was not the case for the 1983–1985surveys under the NGoMCSS, which included the actiniariansfrom both trawls and boxcores (Gallaway et al., 1988). Unfortu-nately, few voucher specimens were used to classify the NGoMCSStrawl samples. We believe this led to a misreporting of all ‘‘whitesock’’ hormathiids as A. longicornis, limiting the utility of theserecords for our population analysis. Virtually, all preservedanemone specimens from both Alaminos and NGoMCSS expedi-tions were lost or destroyed over the years (M. Wicksten, personalcommunication).

The collections made as part of the DGoMB expeditions thusrepresent the only remaining specimen collections of deepwater

y Actinoscyphia, which has short tentacles relative to the large size of the oral disc,

ent and is thus efficient for upstream particle collection; it may also brush against

g long tentacles and smaller oral surface. The elongate tentacles trail downstream

3633 and 3634, respectively, in the northern Gulf of Mexico.

scyphia in the Gulf of Mexico.

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Actiniaria from the Gulf of Mexico. From these, we have createdthe first distribution maps of deepwater Actiniaria for this basin(Figs. 3 and 5). These maps show basin-wide distributions alongthe lower continental slope and abyssal plain for the smallerhormathiid species S. nexilis and M. vestita. The much larger‘‘white sock’’ anemones also appear to be basin-wide, with adepth preference for the upper-mid continental slope. A. long-

icornis, C. coronata and the undescribed species of Paraphelliactis

are very similar in appearance, and most animals could not bedifferentiated to species. The internal anatomy of many specimenswas not adequately preserved, and the histological and nemato-cysts examinations required are laborious. Given the largenumbers of individual specimens, the quality of their preserva-tion, and the similarity of the ‘‘white sock’’ Hormathiid species, wewere unable to identify all specimens to species, and thisimprecision in identification precludes finer-scale analysis at thistime.

4.2. Abundance of Actiniaria in the Deep Gulf of Mexico

4.2.1. High density/biomass areas

At five of the seven sites with high anemone biomass, the trawlsamples comprised small numbers of exceptionally large ane-mones. Four of these low density, but high biomass sites werelocated along the lower slope of the west Florida Escarpment,while the fifth was sited within the upper DeSoto SubmarineCanyon (Fig. 6). All of these were within the eastern Gulf, in areaswith little hard substrate other than an infrequent pebble ormelon-sized rock.

The remaining two high biomass sites also had high anemoneabundance. Both of these high density and high biomass siteswere within the Mississippi Canyon, at the top (420–501 m) andnear the bottom (2025–2410) of this prominent sub-sea feature.These two habitats differ tremendously in terms of sedimentcomposition. The upper canyon sediments are 495% silts andclays with high amounts of flocculent organic particles, main-taining a benthic environment prone to frequent burial. The lowercanyon has far less silt or clay (o60%), and has rocks. The uppercanyon 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 ofthe upper slope canyon, whereas C. coronata is more common inthe deep canyon. Like many deepwater cnidarians (e.g., Actinoscyphia,Umbellula, Funiculina), both species have broad bathymetricranges, and little is known regarding specific 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 peakdensities and biomass in areas of the deep sea where organic

Fig. 6. Trawl biomass plots for deepwater Actiniaria. Sites marked with the letter ‘‘N’’ d

matter accumulates, such as canyons and trench floors. Gage andTyler (1991) noted that actiniarians were common in moreproductive and energetic marginal areas, where they attached tostones, shells, and boulders and attained large sizes. In the NEAtlantic, these patterns are clearly exemplified by the work ofThurston 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 thebiomass; only holothurians were more abundant or had greaterbiomass. In the nearby Madeira Abyssal Plain, the abundance andbiomass of Actiniaria were far lower (0.8% abundance and 0.1%biomass), perhaps reflecting reduced phytodetrital inputs and thedestructive effects of a large and recent turbidite (Thurston et al.,1994). Aldred et al. (1979) found high abundances Actinoscyphia

aurelia at five sites in the center of the West African upwellingregion, one of which (Meteor station 100) has the highest knowndensity of megafauna in the deep sea. This species is encounteredonly rarely elsewhere. Among the explanations for such highdensities (0.35–5.50 per m2) of A. aurelia were extremely highsurface productivity (200 g/carbon/m2/yr�1) fueling particle feed-ing, 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 areamong the most productive in the deep Gulf of Mexico, withspringtime surface chlorophyll values at least twice that of any ofour other deep Gulf survey sites (SeaWIFS year 2000 records). Thisproductivity is fueled by nutrient exports from the MississippiRiver, which also delivers massive amounts of fine sediment. Thus,conditions in the upper canyon are similar to those in the WestAfrican upwelling region (high surface productivity, frequentbenthic disturbance), which may account for the abundance ofA. longicornis.

4.3. ‘‘Giant anemones’’

Four large ‘‘white sock’’ hormathiids were recovered at threetrawl stations along the lower continental slope between 1850and 3050 m. Two of these sites, S40 and S41 (2950–3050 m), areadjacent at the base of the Florida Escarpment; the third (NB3,1850–1910 m) is just outside of Atakapa Basin in the north-centralGulf. In terms of both physical size and volume displacement,these four animals are more than twice as large as all otheranemones encountered in the DGoMB samples. These animalswere all identified using internal anatomy and the sizes of cnidaefrom various parts of the body. The largest two animals, which weidentified as A. longicornis, were collected at S41, have a contractedlength of 210 and 220 mm, and each displaced more than 2000 ml.The smaller of these specimens (Fig. 7) had an epilithic habit; thepedal disc of the larger animal was packed with spicules,indicating that it had been attached to a large hexactinellid

enote both high abundance and high biomass. Station MT1 indicated with arrow.

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sponge. The epilithic specimen sampled nearby at S40 wasphysically smaller, yet still displaced approximately 900 ml. Thelarge epilithic anemone found 700 km to the west at station NB3was roughly equal in size to the one at S40, but its length anddisplacement were not directly measured.

Deep-sea organisms are expected to have relatively lowmetabolic 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 ofhabitat (Shick, 1991). Rocky areas are rarely sampled with trawlsor sleds, as the gear is easily tangled, damaged, or lost. We inferthat the unusually large actiniarians are old, having takenadvantage of hard substrata sheltered from burial or collectionevents. More of these ‘‘giant anemones’’ may be found in the Gulfof Mexico where large swathes of undisturbed hard substrate arepresent (i.e. escarpments, cold seeps, canyon walls).

Fig. 7. ‘‘Giant’’ A. longicornis from the base of the West Florida Escarpment

(2955–3030 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.

Fig. 8. Actiniarians attached to man-made trash. (A) Unidentified anemones (indicated

of the North Florida Escarpment. Photograph taken during Alvin dive 3644. (B) Actina

Canyon. Dark material coating body column is detritus from surface sediments.

4.4. Substrate and mode of attachment

4.4.1. Deep-sea trash

Most species of Actiniaria are presently known from shallowwater and are epilithic, attaching to rock, shell, and coral. Becausesuch substrata are limited in the deep-sea, deepwater actiniarianseither must be epibenthic floaters, opportunistic settlers, orburrowers. Riemann-Zurneck (1979) briefly discussed floatingforms, which include members of a handful of genera (Actinostola,Bolocera, Liponema, Segonzactis) possessing unusually broad pedaldiscs. These animals neither burrow nor grasp substrate with thepedal disc; rather they float within/atop the ooze-like nepheloidlayer. Opportunistic substrates for settlement include otherinvertebrates such as scaphopods, hermit crabs, and sponges;manganese nodules (e.g., Bathyphellia australis Dunn, 1983); whaleskeletons (Foell and Pawson, 1986; Daly and Gusmao, 2007) andtrash.

Large quantities of human-generated trash were encounteredduring the DGoMB cruises. Although the long-term ecologicaleffects of deep-sea trash are presently unknown, much of thistrash serves as attachment for epilithic faunas such as serpulidworms, barnacles, zoanthids, and actiniarians (Fig. 8A). On oneoccasion, we found more than 50 juvenile anemones attached to agarbage sack; at the top of the Mississippi Submarine Canyon, weobserved a few adult A. longicornis attached to fragments ofcrockery (Fig. 8B), alongside identically sized specimens on rocks.Because availability of hard substrate regulates distributions ofmany sessile invertebrates (Lauerman et al., 1996), man-madetrash in the deep sea could have significant local-scale ecologicaleffects, altering recruitment and population structure for deep-seainvertebrates.

4.4.2. Actiniaria living on soft sediments

Actiniarians use two primary modes of anchoring in softsediments. True burrowing anemones have a bulbous or mush-room-shaped physa rather than a flattened pedal disk. The physais used to excavate/anchor in soft sediment (Williams, 1981;Ansell and Peck, 2000). We found no true burrowing anemones inthese trawls. We suspect that their absence reflects samplingmethod rather than actual distributions of burrowing anemones;

by arrows) attached to discarded metal drum (overlaid by plastic mesh) at the base

uge longicornis attached to fragment of crockery from the top of the Mississippi

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burrowing forms typically retract below the sediment interfacewhen disturbed (i.e. when a trawl approaches) and specimens aretypically smaller in diameter and length than the trawl mesh sizeof 3.8 cm.

Alternatively, some epipelic actiniarians use the pedal disk tograsp a ball of sediment. This mode of attachment has beendocumented for several species of Hormathiidae (e.g., Verrill,1883; McMurrich, 1893; Carlgren, 1934; Dunn, 1982; Riemann-Zurneck, 1986; see Fig. 9C) and was described in detail by George(1981) for Actinauge rugosa collected from the Northern BlakePlateau 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) hypothesizedthat in grasping a mud ball, Sicyonis tuberculata countered thedislodgement forces of near-bottom currents.

Actiniaria anchoring themselves by grasping sediment wererecovered from 3 of the 39 stations surveyed in the DGoMB trawls.All of these sites had the soft sediment bottoms typical of mostdeep-sea environments. Station MT1 at the top of the MississippiSubmarine Canyon (420–500 m) had extremely flocculent sedi-

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.

ment that was highly enriched with detritus. In addition toA. longicornis, we collected high numbers of the thin-shelledmytilid Amygdalum politum encapsulated in dense mud cocoons.The macrofauna was dominated by scavenging amphipods. Levinet al. (2000) found a similar community in the oxygen minimumzones (OMZs) of the deep NW Arabian Sea. The site at the top ofthe Mississippi Canyon had the highest biomass and the secondhighest 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 amud ball was survey station C1, 95 km southwest of the upperMississippi Canyon station. At this site, four unidentified ‘‘whitesock’’ hormathiids were recovered, two of which clearly had apedal disc grasping a ball of sediment. Station C1 and MT1 areboth relatively shallow (310–320 m), and both are within closerange of the Mississippi Canyon. Despite these general similarities,MT1 is the most ecologically distinct non-chemoautotrophicdeepwater habitat in the Gulf of Mexico, and is not faunisticallysimilar to any other sample area.

Because soft sediments characterize of much of the deep-seafloor (Heezen and Hollister, 1971; Menzies et al., 1973; Marshall,1979; Gage and Tyler, 1991), burrowing and mud graspingActiniaria have an advantage over epilithic forms as colonizersof deep-sea sediments. Furthermore, species that have a pedaldisc capable of both attaching to hard substrates and graspingmud have a broader array of habitats open to them than dospecies that can only attach to hard substrates or burrow in softsediments. The ability to grasp sediment may also provide ameans of recovering from dislodgement from hard substrata asrocks, sponges, or shells may allow an animal greater motility, ormay enable the animal to avoid burial. Both Aldred et al. (1979)and Foell and Pawson (1986) argued that horizontal surface flows(of either water or sediments) might be favored as dispersal modeby specific anemones. Foell and Pawson (1986) hypothesized thatfood gathering was enhanced by the motility of the large solitaryanemone they observed ‘‘rolling’’ along the bottom in the abyssalNE Pacific. Alternatively, Aldred et al. (1979) postulated thatfrequent sediment movements in the east Atlantic facilitated thecolonization efforts of Actinoscyphia. Epibenthic floating actiniar-ians (i.e. Segonzactis) may have enhanced dispersal potentialbecause of increased motility. We concur that mud ball graspinghas probably facilitated the colonization of the deep Gulf ofMexico by A. longicornis (and possibly by C. coronata andParaphelliactis), although the amount of sediment enclosed bythe pedal disc is small and likely insufficient to maintainanchorage in any but the lightest currents. However, the weightof the sediment bolus would keep the animal properly orientedupon resettlement, at which point it could dig into the sedimentto form a new mud ball or replenish its existing one. This is ahighly efficient dispersion method with little energetic loss to theanemone.

4.4.3. Morphological variation associated with attachment mode

The mode of attachment may shape an individual’s morphol-ogy. This is most evident in animals that attach to pennatulaceanstalks or the anchor spicules of hexactinellid sponges (Fig. 9A andB); an attached animal typically has a pedal disc that is generallywider than does an animal grasping a mud ball or attached torocks (Fig. 9D). Additionally, in comparison to a mud ball graspingspecimen, the body column of an epizooic specimen is typicallyshorter, and the fused tubercles may be more prominent.A specimen grasping a mud ball often has the pedal disc retractedinside the column (Fig. 9C); the aperture at the aboral end iscaused by a constriction of the proximal column around the ball ofmud grasped by the pedal disc. This aperture was erroneouslyreferred to as an anus (George, 1981).

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4.5. Feeding strategies and growth

The 74 specimens of A. longicornis collected at the top of theMississippi Canyon (MT1) were remarkably similar in size(�70 mm long) and shape. A repeat trawl at this site 1 year latercollected many specimens of A. longicornis (n ¼ 46) that wereroughly 10 mm longer than the previous year’s catch. We inferthat the anemones collected during both trawls were of the samecohort, and that the 10 mm increase represents a year’s growth.Such rapid growth may be attributed to the massive organicmatter inputs from the Mississippi River. Shick (1991) postulatedthat burrowing anemones might be able to take advantage ofenhanced dissolved organic matter in sediments, a hypothesissupported by George’s (1981) observation of captive A. rugosa

showing a preference for burrowing in sediments rich in organicmatter.

Van-Praet (1985) showed that anemones can uptake dissolvednutrients (amino acids, glucose) across the ectoderm. In theshallow-water anemone Anemonia sulcata, up to 50% of energyneeds were met through this mode. Such ‘‘epidermal feeding’’ canbe enhanced via extensions of the body column, expansion of theoral disc, and projections of tentacles. In the highly oligotrophicwaters of the deep sea, direct nutrient uptake is probably not asignificant energy source, except possibly in detritus-rich canyonsand other depocenters. Burrowing species may be able to exploitthe dissolved organic content within the sediment, which mayexceed that of overlying waters by an order of magnitude (Gageand Tyler, 1991). Such a nutritional benefit may explain the highabundance and biomass values for mud ball grasping Actiniaria atthe top of the Mississippi Submarine Canyon, where sedimentsare unusually rich in detritus.

Although feeding behavior of deepwater Actiniaria has notbeen directly observed in the Gulf of Mexico, studies withecologically and taxonomically similar species provide someinsight into nutrition in deepwater anemones in the Gulf ofMexico. Van-Praet (1985) identified Phelliactis robusta andActinoscyphia as well as adapted for particle feeding, possessinga ciliated epidermis ideal for retaining micro zooplankton,phytoplankton, and detritus; these same attributes characterizeActinauge, Chondrophellia, and Paraphelliactis. Feeding strategieshave been well documented for S. tuberculata, a deep-sea speciesthat has an oral disc morphology similar to that of Actinoscyphia.Lampitt and Patterson (1987) observed S. tuberculata in theabyssal NE Atlantic and noted that the oral disc was activelyoriented into the current. We observed similar orientation inActinoscyphia in the Gulf of Mexico (Fig. 4A). This contrasts withthe downstream particle feeding seen in some other actiniarians(Fig. 4B), in which tentacles are carried by the current. Based onthe prey items found in gut content analysis (including planktonicforaminifera, fish scales, and a Plesiopenaeus shrimp nearly aslarge as the anemone that ingested it), Lampitt and Patterson(1987) hypothesized that S. tuberculata captured planktonic andepibenthic prey and also caught material when the tentaclesbrushed against the sediment.

Acknowledgements

This project was supported by the Minerals ManagementService, as part of the Deepwater Program: Gulf of MexicoContinental Slope Habitats and Benthic Ecology Study (#30991).Adorian Ardelean, Ha-Rim Cha, and Daphne Fautin of theUniversity of Kansas contributed valuable taxonomic expertise.Mary Wicksten (TAMU) and Daphne Fautin (University of Kansas)provided valuable comments as reviewers. We would also like tothank Erin Brewer, Sophie DeBeukelaer, Thomas Decker, Fain

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.

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