Ammons, Daly - 2008 - Distribution, habitat use and ecology of deepwater Anemones (Actiniaria) in the Gulf of Mexico

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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) in
the Gulf of Mexico
Archie W. Ammons a,�, Marymegan Daly b
a Department of Biology, Texas A&M University, MS 3258, College Station, TX 77843, USA
b 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 2008
The 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 a
significant and often dominant fraction throughout the world’s
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 attach-
ment. 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
Gulf’s terrigenous inputs come from the Mississippi River, which
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. Ammons).
deposits the bulk of its sediments over the Mississippi Fan
(Pequegnat, 1983). This feature covers over 10% of the seafloor and
plays a significant 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 confined and isolated biogeo-
graphic 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, flattened 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
2000–2002. 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
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mailto:archman@mail.bio.tamu.edu
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95°°W 90°W 85°W 80°W
30°N
N
25°N
30°N
Texas
30
0m
1,0
00
m
2,0
00
m
3,0
00m
Florida
25°N
95°W 90°W 85°W 80°W
Fig. 1. Locations of DGoMB survey trawls. Water depths in m.
Table 1
DGoMB 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 immediately
sorted to morphotype in the field, enumerated, weighed, and then
fixed 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 identified 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 (1983–1985) of the Northern
Gulf of Mexico Continental Slope Study (NGoMCSS). In situ
observations were provided by close-up anemone and seafloor
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 identified from the deep
Gulf 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-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 sampledfrom 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 (50–220 mm
length; Fig. 2A). Unless wrapped around a sponge or a pennatu-
lacean 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 220–580 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 flocculent sediments. A repeat trawl in June 2001
confirmed 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 Pacific, at depths from 600 to
3570 m (Verrill, 1883; Carlgren, 1942; Wolff, 1961; summarized in
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Table 2
Deepwater 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.
A.W. Ammons, M. Daly / Deep-Sea Research II 55 (2008) 2657–2666 2659
Fautin, 2006). We recovered specimens of C. coronata from three
sites in the Gulf of Mexico, from depths of 420–2790 m. Near the
base of the Mississippi Submarine Canyon (2025–2410 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 pennatula-
ceans. 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 difficult 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 distribu-
tion of ‘‘white sock’’ anemones is shown in Fig. 3.
Specimens of an unidentified species of Paraphelliactis were
collected on the upper continental slope (645–695 m), at the top
of the DeSoto Submarine Canyon. This is the first 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 identification.
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 (40–600 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 flattened 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 Pacific. With the exception of three specimens collected
200–250 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.
A.W. Ammons, M. Daly / Deep-Sea Research II 55 (2008) 2657–26662660
(2286–5320 m). In the Gulf of Mexico, we found specimens at
depths 2100–3665 m (Fig. 3). A single specimen resembling
M. vestita was collected at 340 m, but its identity was not
confirmed. 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 Pacific, M. vestita has
similar settlement habits, but its membersalso 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 superficial
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
name ‘‘Venus Flytrap Anemones’’ (e.g., Riemann-Zürneck, 1978;
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
700–2200 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 1983–1985 NGoMCSS expeditions. H. pilatus was only
encountered at a single 342 m site in the north-central GoM.
A. perdix was recovered from five 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 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 from
the 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 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 (1963–1972);
however records of Actiniaria were omitted in the final report
(Pequegnat, 1983). This was not the case for the 1983–1985
surveys under the NGoMCSS, which included the actiniarians
from both trawls and boxcores (Gallaway et al., 1988). Unfortu-
nately, 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 expedi-
tions 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
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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A.W. Ammons, M. Daly / Deep-Sea Research II 55 (2008) 2657–26662662
Actiniaria from the Gulf of Mexico. From these, we have created
the first 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. long-
icornis, 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 nemato-
cysts examinations required are laborious. Given the large
numbers of individual specimens, the quality of their preserva-
tion, and the similarity of the ‘‘white sock’’ Hormathiid species, we
were unable to identify all specimens to species, and this
imprecision in identification precludes finer-scale analysis at this
time.
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 trawl
samples comprised small numbers of exceptionally large ane-
mones. Four of these low density, but high biomass sites were
located along the lower slope of the west Florida Escarpment,
while the fifth 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 (420–501 m) and
near the bottom (2025–2410) 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 flocculent organic particles, main-
taining 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 thesame 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 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 peak
densities 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 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 exemplified 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 reflecting 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 five 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 (0.35–5.50 per m2) of A. aurelia were extremely high
surface 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 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 fine 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 (2950–3050 m), are
adjacent at the base of the Florida Escarpment; the third (NB3,
1850–1910 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 identified using internal anatomy and the sizes of cnidae
from various parts of the body. The largest two animals, which we
identified 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
enote 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).
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 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 floaters, opportunistic settlers, or
burrowers. Riemann-Zürneck (1979) briefly discussed floating
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 float 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 significant local-scale ecological
effects, altering recruitment and population structure for deep-sea
invertebrates.
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 mush-
room-shaped physa rather than a flattened 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 reflects sampling
method 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 interface
when disturbed (i.e. when a trawl approaches) and specimens are
typically smaller in diameter and length than the trawl meshsize
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-
Zürneck, 1986; see Fig. 9C) and was described in detail by George
(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 (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 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 unidentified ‘‘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 (310–320 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
floor (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 flows
(of either water or sediments) might be favored as dispersal mode
by specific 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 Pacific. Alternatively, Aldred et al. (1979) postulated that
frequent sediment movements in the east Atlantic facilitated the
colonization efforts of Actinoscyphia. Epibenthic floating actiniar-
ians (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 insufficient 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 efficient 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 individual’s morphol-
ogy. 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).
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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 ¼ 46) that were
roughly 10 mm longer than the previous year’s catch. We infer
that the anemones collected during both trawls were of the same
cohort, and that the 10 mm increase represents a year’s 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 George’s (1981) observation of captive A. rugosa
showing a preference for burrowing in sediments rich in organic
matter.
Van-Präet (1985) showed that anemones can uptake dissolved
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
significant 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 benefit 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
Mexico. Van-Präet (1985) identified Phelliactis robusta and
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, fish 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.
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
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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	Distribution, habitat use and ecology of deepwater Anemones (Actiniaria) in the Gulf of Mexico
	Introduction
	Methods
	Results
	Actiniaria of the Gulf of Mexico
	Hormathiidae
	Actinoscyphiid ’’Flytrap Anemones’’
	Other anemone species
	Discussion
	Biogeography of Actiniaria in the Deep Gulf of Mexico
	Abundance of Actiniaria in the Deep Gulf of Mexico
	High density/biomass areas
	High density/biomass areas outside the Gulf of Mexico
	’’Giant anemones’’
	Substrate and mode of attachment
	Deep-sea trash
	Actiniaria living on soft sediments
	Morphological variation associated with attachment mode
	Feeding strategies and growth
	Acknowledgements
	References