Table Of ContentMALACOLOGIA, 1998, 40(1-2): 63-112
A NEW GENUS AND FIVE NEW SPECIES OF MUSSELS (BIVALVIA, MYTILIDAE)
FROM DEEP-SEA SULFIDE/HYDROCARBON SEEPS IN THE GULF OF MEXICO
Richard G. Gustafson^*, Ruth D. Turner^, RichardA. Lutz\ & Robert C. Vrijenhoek^
ABSTRACT
Five new species of modioliform mussels in the family Mytilidae are described from material
collected at sulfide/hydrocarbon seeps in the Gulf of Mexico. New definitive taxa, placed in the
subfamily Bathymodiolinae, include the genus Tamu and the species Tamu fisheri from hydro-
carbonseepsonthe LouisianaContinental Slope, Bathymodiolus heckeraefrom brine seeps at
the base of the West Florida Escarpment in the eastern Gulf of Mexico, and Bathymodiolus
brooksifromtheWestFloridaEscarpmentsiteandfrom hydrocarbonseepsatAlaminosCanyon
inthewesternGulfofMexico.Anadditionaltwonewmusselspecies,whichexhibitcombinations
of morphological characters unlike any existing mytilid genus but for which molecular data are
equivocal, are provisionally placed in the genera Bathymodiolus and Idas, respectively. These
are: "Bathymodiolus"childressi from hydrocarbon seepsatAlaminosCanyon andthe Louisiana
Continental Slope, and"Idas"macdonaldi (inthesubfamilyModiolinae)from hydrocarbonseeps
onthe Louisiana Continental Slope.
Keywords: Mytilidae, deep-sea, sulfide seeps, hydrocarbon seeps, Bathymodiolinae.
INTRODUCTION drothermal vents on the Juan de Fuca Ridge
in the north-eastern Pacific (Juniper et al.,
Modioliform mussels in the family Mytilidae 1992) and Amygdalum politum (Verrill &
are conspicuous members of many deep-sea Smith, in Verrill, 1880), a small thin-shelled
hydrothermal vent and cold-water methane/ mytilid, occurs near cold water hydrocarbon
sulfideseepenvironments.Acommonfeature seeps on the Louisiana Continental Slope
of these mussels is their dependence on sul- (Turner, 1985).
fide-oxidizing or methanotrophic symbionts As yet undescribed modioliform mussels
(Fisher, 1990; Cavanaugh, 1992). The first were reported from hydrothermal vents or
vent mussel described was Bathymodiolus cold-seeps in the Pacific Ocean at Guaymas
thermophilus Kenk & Wilson, 1985, which oc- Basin (Turner, 1985), MiddleValley(Juniperet
curs at hydrothermal vents on the Galápagos al., 1992), the Mariana Back-Arc Basin
Riftandthe East Pacific Rise (EPR). Recently (Hessler & Lonsdale, 1991), and the Mid-Oki-
described species are: B. platifrons Hashi- nawa Trough (Hashimoto et al., 1995); and in
moto & Okutani, 1994; B. japonicus Ha- theAtlantic Ocean atthe South Barbados ac-
shimoto & Okutani, 1994; B. adulcidos Hashi- cretionary prism (Jollivet et al., 1990) and on
moto & Okutani, 1994; and B. septemdierum the Mid-Atlantic Ridge at 37°50'N ("Menez
Hashimoto & Okutani, 1994, from vent and Gwen" site), 37°17'N ("Lucky Strike" site),
cold seep sites around Japan; B. brevier 29°N ("BrokenSpur"site),and 14°45'N (Cosel
Cosel, Métivier & Hashimoto, 1994, and B. etal., 1997).
elongatusCosel, Métivier& Hashimoto, 1994, An allozyme survey by Craddock et al.
from vent sites in the south Pacific; and B. (1995) identified several additional modio-
puteoserpentis Cosel, Métivier & Hashimoto, liform taxa from sulfide/hydrocarbon seeps in
1994, from the Snake Pit site on the Mid-At- the Gulf of Mexico. A subsequent analysis of
lanticRidge. Inaddition,thesmall mussel Idas these specimens for DNA sequences from a
washingtonia (Bernard, 1978) occurs at hy- region ofthe mitochondrial Cytochrome Ox-
^^IMnustsiteuutemooffMCaormipnaeraantdivCeoaZsotoallogSyc,ieHnacrevsa,rdP.UnOi.veBrosixty2,31Ca,mRburtigdegres,UnMiavsesrasicthyusNeetwtsB0r2un1s3w8i,ckU,SNAewJersey08903, USA
'PresentAddress; National OceanicandAtmosphericAdministration, National Marine Fisheries Service, Northwest Fish-
eriesScienceCenter, ConservationBiologyDivision,2725MontlakeBlvd. E.,Seattle,Washington98112-2097
63
64 GUSTAFSON ETAL
TABLE 1. New species andtype localitiesofmodioliform musselsfrom the Gulfof Mexico.
Newspecies Location Latitude Longitude Depth (m)
Bathymodiolus heckerae West Florida Escarpment
Bathymodiolus brooksi
Bathymodiolus brooksi
"Bathymodiolus"childressi
"Bathymodiolus"childressi
"Bathymodiolus"childressi
Tamu fisheri
Tamu fisheri
"Idas"macdonaldi
NEW DEEP-SEA MUSSELS 65
FIG. 1. Location ofsubmersibledivesites inthe Gulfof Mexicowhere rnusselswerecollected.
and tissues were made either freehand or tion using the statistical computer program
with the aid of a camera lucida. JMP 3.0.2 (SAS Statistics Inst., Inc, Raleigh,
North Carolina).
Morphological Terminology
SYSTEMATIC SECTION
The "horizontal branchial septum" is a thin,
membranous horizontal shelf separating in- Family Mytilidae
current and excurrent chambers, posterior to
the posterior adductor (commonly extends Subfamily Bathymodiolinae Kenk & Wilson,
from the ventral side of posterior adductor to 1985
the base ofthe excurrent siphon). The "valvu- Typegenus; BathymodiolusKenk&Wilson,
larsiphonal membrane" is an extension ofthe 1985
branchial septum formed by fusion of right
and left mantle lobes ventral to the excurrent Revised Diagnosis: Shell smooth, modioli-
siphon and extending a variable distance into form, with subterminal umbones; adult hinge
the pedal-byssal gape; a small centrally edentulous, juvenile hinge with small den-
placed papilla issometimes presentatthean- ticulations anterior and posterior of ligament;
teriorend ofthe valvular siphonal membrane. posterior byssal retractors divided into ante-
rior and posterior portions with separate in-
sertion points on the adult shell producing
Morphometries separate muscle scars; intestine short, either
straight or with a very short recurrent loop;
Shell measurements used to statistically demibranchs of hypertrophied ctenidia thick
discriminate among the five new species and fleshy, inner and outer demibranchs of
wWere: L= length of valve; H = height of valve; equal length, filaments broadly thickened.
= width of valves, G = length of the liga- Ctenidia associated with symbiotic bacteria.
ment; and A = anterior length or the distance
from the anteriorshell margin to an imaginary Remarks:Asoriginallydescribedthissubfam-
line drawn vertically from the anterior edge of ily contained the single genus Bathymodiolus
the beak or umbonal bulge (Fig. 2). Measure- (Kenk & Wilson, 1985). Eight members ofthis
ments were made with hand-held calipers subfamily have been previously described:
(±0.1 mm). All analyses were performed on B. thermophilus, B. brevier, B. elongatus, B.
Iog10 transformations of the original vari- puteoserpentis, B. platifrons, B. japonicus, B.
ables. Multivariate analyses were performed aduloides, and B. septemdierum (Kenk & Wil-
on standardized variables with Varimax rota- son, 1985; Hashimoto & Okutani, 1994; Cosel
66 GUSTAFSONETAL
FIG.2. Diagramdepictingmeasurementstakenandgeneralizedshellcharacters.A,anteriorlength(distance
from anterior shell margin to anterior edge of umbo);AA, anterior adductor:APR. anterior portion of poste-
rior byssal-pedal retractor; AR, anterior byssal-pedal retractor; H, shell height; L, shell length; G, ligament
length; PA, posterioradductor; PL, pallia! line; PPR, posterior portion of posterior byssal-pedal retractor; W,
width ofshell valves.
etal., 1994).Thecurrentcontribution addsthe posterior and anterior portion, retractor scars
genus Tamu and the species T. fisheri, B. separate; labialpalpsuspensorsandpedai re-
heckerae, and B. brooks! tothe subfamily. tractorspresent;demibranchsofctenidiathick
All members of this subfamily have hyper- and fleshy; filaments broadly thickened, with
trophied gillsassociatedwith symbiotic bacte- reduced ventral food grooves, containing in-
riathatresideeitherwithincertaincellstermed tracellular bacterial symbionts; intestine
"bacteriocytes" or on the gi.ll surface (Fisher, straight without recurrent loop; rectum enters
1990: Fisher et al., 1993; Cavanaugh, 1992; ventricle anteriorto the auricularostia.
Cavanaugh et al., 1987; Cavanaugh,
pers. comm.). The simplified alimentary sys- Remarks: The manuscript name Bathy-
tem, hypertrophied gills, and symbiosis with modiolus was introduced as a nomen nudum
sulfide-oxidizing or methanotrophic bacteria, by LePennec et al. (1983: 70) and subse-
indicative of a different feeding mechanism in quentlyappeared in Le Pennée & Hily (1984),
this group, separates members of this sub- Laubier & Desbruyères (1984), and Smith
familyfrom all other known mytilids. (1985; publication date. May) priorto its valid
introduction, under the rules of the Inter-
Bathymodiolus Kenk & Wilson. 1985 national Code of Zoological Nomenclature
(ICZN), by Kenk & Wilson (1985; publication
Bathymodiolus LePennec et al. 1983: 70; date, 9 July).
Le Pennée & Hily, 1984: 517; Laubier & Des- The extremely reduced pedal gape of B.
bruyères, 1984: 1507; Smith, 1985: 1068 thermophilus appearsto be a derived charac-
[nomen nudum]. ter, absent in other species referred to this
Bathymodiolus Kenk & Wilson, 1985: 255 genus (Hashimoto & Okutani, 1994; Cosel et
(type species, by original designation, Bathy- al., 1994, 1997). Bathymodiolus brevior, B.
modiolusthermophilus Kenk & Wilson, 1985). elongatus, B. puteoserpentis (Cosel et al.,
1994), and "Bathymodiolus" childressi have
Revised Diagnosis: Shell large (maximum been referred to Bathymodiolus on a provi-
size greater than 90 mm), smooth, modio- sional basis. The final systematic placement
liform,withsub-terminal umbones;adulthinge of these species, and others placed in Bathy-
edentulous, juvenile hinge with small denticu- modiolus, mustawaitcomplete morphological
lationsanteriorandposteriorofligament(Figs. analyses and molecular studies on the entire
3-5); posterior byssal retractors divided into group of deep sea mytilids.
NEW DEEP-SEAMUSSELS 67
Bathymodiolusthermophilus Kenk & Wilson, description of this species, under the rules of
1985 Figures 3-5 the ICZN, by Kenk & Wilson (1985; publica-
tion date, 9 July).
Bathymodiolus thermophilis (sic) Laubier & Kenk & Wilson (1985) described Bathy-
Desbruyères, 1984: 1510 [nomen nudum]. modiolusas having asmall pedal gape result-
Bathymodiolus thermophilus Smith, 1985 ing from extensive ventral fusion of the inner
(May): 1068 [nomen nudum]. foldsofthe mantle lobes. Thisfeature is pres-
Bathymodiolus thermophilus Kenk & Wil- ent in the type species B. thermophilus, but is
son, 1985 (9July): 255, figs. 2-13 (type local- lacking in other described members of this
ity, "Mussel Bed" hydrothermal vent, Galápa- genus (Hashimoto & Okutani, 1994; Cosel et
gos Rift, 0°47.89'N; 86°9.21'W in 2495 m, al., 1994), as well as in all other known
ALVIN Dive 879; holotype USNM 803661). mytilids. As pointed out in Kenk & Wilson
(1985: 260), the dorsal ends ofthe ascending
Description: Shell large, up to 180 mm long, lamellaeareattachedtomuscularlongitudinal
modioliform,withsub-terminal umbones,ellip- ridgesonthesurfacesofthe mantle lobesand
tical in juveniles, arcuate in older specimens. the visceral mass. These muscular longitudi-
Ventral shell margin nearly straight in young nal ridges are also unique to B. thermophilus
specimens, slightly concave in specimens and were not evident in any other mussel ex-
largerthan 10 cm. Adult hinge edentulous, ju- amined forthis report.
venile hinge with small denticulations anterior The hinge of B. thermophilus was originally
and posteriorto ligament. Posterior byssal re- described as edentulous (Kenk & Wilson,
tractorsdivided, retractorscarsseparate;sep- 1985). However, in specimens of B. ther-
mm
arate pedal retractors prominent; slender mophilus smallerthan about 10 there are
labial palp suspensors extend anteriorly from up to 25 "vertical striations" or denticles im-
anteriorretractorstosupportthemusculahzed mediately posteriorofthe ligament and about
labial palps. Ventral palliai line with a dorsally 6 denticles located immediately below the
directed concavity in byssal region aboutone- umbones (Fig. 3-5). Other deep-sea mussel
third of the distance from the anterior end. species described herein (Figs. 6-28) also
Inner fold of mantle lobes fused in postero- have hinge denticulations as juveniles (Figs.
ventral and antero-ventral midline creating 8-10, 18-20, 23, 25-27). These denticula-
valvularsiphonal membrane, with papilla, and tions are lost in adult members of the genus
an extremely reduced pedal gape. Dorsal Bathymodiolus
edgesofascending lamellaeattachedto mus- Although Bathymodiolus was described as
cularlongitudinal ridgeson surfacesofmantle lacking ventral food grooves on the ctenidia
lobe and visceral mass. Horizontal branchial (Kenk & Wilson, 1985), we observed reduced
septum, extending fromthe baseoftheexcur- food grooves in all specimens of B. ther-
rent siphon and the ventral side of the poste- mophilus we examined. Food grooves were
rior adductor, separates incurrent and excur- first described in B. thermophilus by Le Pen-
rent chambers posteriorly. Inner and outer née et al. (1983), Le Pennée & Hily (1984),
demibranchs essentially equal-sized, thick and Fiala-Médioni et al. (1986).
and fleshy, filaments broadly thickened, with Kenk& Wilson (1985) describedthe perios-
reduced ventral food grooves. Ctenidia con- tracum of Bathymodiolus as "hirsute"; mean-
tain intracellularsymbioticbacteria. Muscular- ing hairy, bristly or shaggy. However, these
ized inner palps long and slender, attached "periostracal hairs" are probablyof byssal ori-
over mostoftheir length to visceral mass, ex- gin (Bottjer& Carter, 1980; Ockelmann, 1983)
tending farther posteriorly than smaller mus- and not of taxonomic value. The original de-
cularized outer palps. Intestine straight with- scription of Bathymodiolus described the
out recurrent loop; intestine/rectum enters labial palps as "small," whereas the labial
ventricle anteriorto the position ofthe auricu- palps of B. thermophilus specimens we ex-
larostia. amined, from the type-localityand elsewhere,
were large and muscular.
Remarks: The manuscript species name Ba-
thymodiolusthermophilis (sic) was introduced Range: This species appears confined to the
asanomen nudum byLaubier& Desbruyères area of hydrothermal vent activity on the
(1984) and as B. thermophilus by Smith Galápagos Rift and along the EPR at 9° to
(1985; publication date. May) priortothevalid 10°N, 11°24'N and 13°N (Table2). In addition.
GUSTAFSON ETAL
FIG. 3. Bathymodiolusthermophilus Kenk & Wilson. Juvenile hinge lineofspecimen 4.5 mm in length.
FIG. 4. Bathymodiolusthermophilus Kenk & Wilson. Hinge denticles, located immediately posteriorto liga-
ment injuvenile specimen4.5 mm in length.
FIG. 5. Bathymodiolusthermophilus Kenk & Wilson. Hinge denticles, located immediately belowthe umbo
injuvenilespecimen 4.5 mm in length.
preliminary comparison of mtDNA CO! se- "Mussels" - Florida Escarpment Cruise Par-
quences between B. thermophilus from the ticipants, 1984: 32, fig. 1 [musselsvisible
type locality and mussels collected from 17°S in habitat photo].
on the EPR revealed essentially no differ- "Large mussel" - Turner & Lutz, 1984: 60,
ences (R.C. Vrijenhoek, unpublished data). figs. 1 (site #9 = Florida Escarpment, dia-
gram of mussel shell), 5, 6, [mussels vis-
Bathymodiolus heckeraeTurner, ible in habitat photo], 8 (left) [micrograph
Gustafson, Lutz & Vrijenhoek, new species of prodissoconch].
Figures 6-13 "Large, elongate mussels" - Turner, 1985:
29, figs. 4B-C, 6.
This species, known since 1984, has been "Mytilid" - Southward, 1985: 673.
referred to in literature concerning seep and "Mytilid mussel" - Pauli et al., 1985: 710.
vent biology but was never formally de- "Large mussels," "large golden-brown my-
scribed. The following is a list of these refer- tilids" - Hecker, 1985: 465, 466, figs. 2,
ences. 4, 5, 6 [musselsvisible in habitatphotos].
"Large mussels" - Grassle, 1986: 338.
"Mussel" - Pauli etal., 1984: 965, fig. 2 [mus- "Seep mussels," "Florida Escarpment mus-
sels visible in habitat photo]. sel" - Cavanaugh et al., 1987: 346, 347,
NEW DEEP-SEAMUSSELS 69
TABLE 2. Specimensof Bathymodiolusthermophilusexamined.
70 GUSTAFSONETAL
TABLE 5. Specimensof"Bathymodiolus"childressi examined.
Numberand conditionof
Dive Date Depth Latitude; Longitude specimens
JOHNSON SEALINK-I Dives, Gulfof Mexico - LouisianaContinental Slope - Bush Hill
1877 27 Sept. 1986 548 27°46.9'N; 91°30.4'W 5 -shell &tissue
3108 31 Aug. 1991 548 27°46.9'N; 91°30.4'W 3 -shell &tissue
3129 15 Sept. 1991 546 27°46.9'N: 91°30.4'W 119 - shell, 59 - shell &tissue
JOHNSON SEALINK-I Dives, Gulfof Mexico - Louisiana Continental Slope - Green Canyon-272
3133 17 Sept. 1991 737 27°41.3N; 91°32.5'W 4- shell
3137 19 Sept. 1991 723 27°41.rN; 91°32.2'W 44-shell, 8 -shell & tissue
JOHNSON SEALINK-I Dives, Gulfof Mexico - Louisiana Continental Slope- Brine Pool NR-1
3145 27 Sept. 1991 650 27°43.4N; 91°16.6W 29 -shell
ALVIN Dives, Gulfof Mexico -AlaminosCanyon
2211 13April1990 2222 26°21.3'N;94°29.7'W 31 - shell, 8 - shell &tissue
TABLE 6. SpecimensofTamu fisheri examined.
Numberand condition of
Dive Date Depth Latitude; Longitude specimens
JOHNSON SEALINK-I Dives, Gulfof Mexico - LouisianaContinental Slope Bush Hill
3108 31 Aug. 1991 548 27°46.9'N; 91°30.4'W 6- shell, 3- shell &tissue
3129 15 Sept. 1991 546 27°46.9'N; 91°30.4W 3 - shell & tissue
JOHNSON SEALINK-I Dives, Gulfof Mexico - LouisianaContinental Slope NearGarden Banks-386
3131 16 Sept. 1991 701 27°50N; 92°10W 1 - singlevalve
3149 29 Sept. 1991 650 27°50'N; 92°10'W 6 - shell
MCZ No. 296151 (TexasA& M University, LouisianaSlope, Cruise#85-6-5, Trawl #5)
L2787 (rightvalve)
L2788 (leftvalve)
L2789 (leftvalve)
MCZ No. 296152 (TexasA& M University, Louisiana Slope, Cruise #85-6-5, Trawl #10)
L2742 (rightvalve)
L2743 (leftvalve)
L2744 (leftvalve)
L2745 (leftvalve)
TABLE 7. Specimensof"Idas"macdonaldi examined.
Numberandcondition of
Dive Date Depth Latitude; Longitude specimens
JOHNSON SEALINK-I Dives, Gulfof Mexico - Louisiana Continental Slope
3149 29 Sept. 1991 650 27°50'N; 92°10W 4 - shell, 6 - shell & tissue
fig. 1a-b [micrographs of bactehocyte "Deep-sea mussel, cf. Bathymodiolus" -
and symbiotic bacterium]. Hook & Golubic, 1990:240.
'Mussels (cf. Bathymodiolus) - Hook& Gol- "Mytilid" - Petrecca & Grassle, 1990: 281.
ubic, 1988: 348, fig. 1 [mussels visible in "West Florida Escarpment mussel (com-
habitat photos], fig. 2. mon)" - Craddock et al., 1991: p. 302.
"Mytilid bivalve," "seep mussel" - Gary et al., "Florida Escarpment mussel" - Dahlhoff &
1989:411. Somero, 1991:475 (table 1).
NEW DEEP-SEAMUSSELS 71
D
FIG. 6. Bathymodiolus heckeraeTurner, Gustafson, Lutz & Vrijenhoek. Holotype,ANSPA18846.A, anterior
view; B, posterior view; C, dorsal view; D, ventral view; E, lateral view of right valve; F, lateral view of left
valve.
72 GUSTAFSON ETAL
2.5 cm
FIG. 7. Bathymodiolus heckeraeTurner, Gustafson, Lutz & Vrijenhoek. External viewsofagrowth seriesof
shells illustratingontogeneticchange in shape.
"FLmytilid" - Cavanaugh, 1992: 316. Shell Morphology: Shell large, up to 190 mm
"Bathymodiolus-like mussels" - Hook & Gol- long, modioliform, thin, fragile, essentially
ubic, 1992: 120. equivalve, elongately elliptical. Anterior mar-
"Seep mytilid Va" - Fisher, 1993: 609. gin sharply rounded; posterior margin broadly
"Deep-sea mussel (an undescribed new rounded; ventral margin straight in young
genus similarto Bathymodiolus)" - Hook specimens, with a slight ventral concavity in
&Golubic, 1993:81. medium sized specimens, concavity more
"SM Va" - Fisher et al., 1993: 278, 284. pronounced in larger specimens; dorsal mar-
"FL/Va" - Craddock, et al., 1995: 479-483. gin broadlyconvex, more or lessstraightover
"Seep Mytilid Va" - Nelson & Fisher, 1995: span of the ligament (Figs. 6, 7, 11, 12). Um-
table 3. bones often eroded; prosogyrate; subtermi-
nal, positioned between 6% and 16% of the
Types: Holotype ANSP AI8846 from ALVIN length ofthe shell from anteriorend. An indis-
Dive 1343 along the base of the West Florida tinct, raised, broadly rounded ridge extends
Escarpment in the eastern Gulf of Mexico at from umbonal region to posterior-ventral mar-
26°03N; 84°54'W, in 3270 m. Paratypes are gin.
from ALVIN Dive 1754 at 26°02.4'N: External sculpture lacking; surface smooth
84°55.3'W in 3303 m (USNM); ALVIN Dive except for concentric growth lines; fine radial
1755 at 26°01.5'N; 84°55.3'W in 3300 m lines in periostracum extending from umbo to
(MOZ); ALVIN Dive 2196 at 26°02.4'N: ventral margin, most prominent posteriorly;
84°54.4'Win 3314 m (ANSP400772;, USNM, and fine radial periostracal corrugationsalong
HMNS, MNHN); ALVIN Dive 2197 at the ventral margin in the region of the byssal
26°02.2'N;84°54.5'Win3314 m (HMNS);and gape. Shell dull-white, periostracum straw-
ALVIN Dive 2542 at 26°01.8'N; 84°54.6'W in yellow to light-brown in young specimens,
3314 m (ANSP 400771 400773; MNHN). older specimens have dark-brown perios-
,
