A new arabellid polychaete living in the mantle cavity of deep-sea wood boring bivalves (family Pholadidae)

9 Pages·1992·5.1 MB·English

PROC. BIOL. SOC. WASH.
105(2), 1992, pp. 224-232
A NEW ARABELLID POLYCHAETE LIVING IN THE
MANTLE CAVITY OF DEEP-SEA WOOD BORING
BIVALVES (FAMILY PHOLADIDAE)
Harlan K. Dean
Abstract.—A new species of polychaete, Pholadiphila turnerae (Family Ar-
abellidae), is described from the mantle cavity of two species of wood boring
bivalves (Family Pholadidae, Subfamily Xylophagainae). This is the first re-
ported association between an arabellid polychaete and a mollusk. This species
shows reductions in jaw structure and setal development similar to the reduc-
tions observed in many endoparasitic arabellids. The jaw apparatus consists
ofthree pair ofmaxillae, a short, slender maxillary carrier, and well-developed
mandibles. Setae are ofthree types: acuminate, capillary and spinous. Ecological
aspects of commensal/parasitic polychaetes living in a bivalve mantle cavity
are discussed.
Woody plant material washed into the Family Arabellidae Hartman, 1944
deep sea is rapidly decomposed by wood Pholadiphila, new genus
boring bivalves of the family Pholadidae, —
Diagnosis. Body slender, elongate, flat-
subfamily Xylophagainae, and acts as a
tened dorso-ventrally, segmentation dis-
center for organic enrichment communities
tinct. Prostomium small, conical, antennae
at abyssal depths (Turner 1973, 1977, 1981;
and palps absent, eyespots lacking. Prosto-
Wolff 976; Grassle 987). As part ofa long-
1 1 mium indistinctly separate from the first
term study of these communities by Dr.
DSRV segment. Peristomial ring indistinct. Three
Ruth Turner, the Alvin has been uti-
pairs of equal maxillae; MI falcate, bifid;
lized to place "wood islands" and associ-
Mil ctenoid with appressed, blade-like pro-
ated wood panels in the deep sea and re-
cesses; Mill small avicular. Maxillary car-
cover them after varying periods of time.
rier short, slender tripartite anteriorly.
While studying the polychaetes associated
Mandibularplates large, smooth, shield-like;
with the recovered wood panels, several
united medially. Parapodia uniramous,
specimens were encountered living in close
conical, cirri absent. Setae simple, 3 types:
association with the wood boring bivalve
stout, emergent spines (Fig. 3C); more slen-
mollusks. Specimens oftwo members ofthe
der acuminate setae (Fig. 3D); and capillary
subfamily Xylophagainae (Family Pholad-
setae (Fig. 3B).
idae), Xyloredo ingolfia Turner, 1972 and Remarks.—The Arabellidae Hartman,
an as yet undescribed genus and species 1944 and Oenonidae Kinberg, 1865
(Turner, pers. comm.) were found to harbor (emended by Colbath 1989a) are separated
a previously undescribed species of Ara- from other eunicoids by their prionognath
bellidae within their infrabranchial cham- jaw pattern and the possession ofunminer-
ber (Fig. 3A). This paper describes the ar- alized jaws (Colbath 1989a). The prionog-
abellid species, Pholadiphila turnerae, and nathjaw pattern ischaracterized by two long,
discusses its ecology. slender maxillary carriers and what is usu-
VOLUME 105, NUMBER 2 225
ally termed a ventral "third carrier" (or lig- probably due to setal modifications corre-
ament by Colbath [1986]). Three genera of lated with its lifestyle. Similar reductions in
predominantly endoparasitic arabellids are setae have generally been associated with
exceptional in that the maxillary carriers are commensalism in the Polychaeta (Blake
fused along much of their length while the 1990) and with parasitism in other mem-
third carrier may (Haetnatocleptes Wiren, bers of the Arabellidae (Pettibone 1963,
1886, Labrorostratus Saint-Joseph, 1888) Uebelacker 1984).
or may not {Oligognathus Spengel, 882) be
1
evident. The possession of a slender max-
Pholadiphila turnerae, new species
illary carrier with indications ofa tripartite
Figs. 1-3
anterior end (Fig. 2E) by Pholadiphila tur-
nerae strongly suggests fusion of what was Material examined.—WHOI Deep Ocean
originally a prionognath maxillary carrier Station No. 2: 38°17.5'N, 69°35.2'W, 3602
pattern. The reduced number of maxillae m. Wood Panel N-30; submerged 5 Sep 1975
and the fused, short (but not broad) max- {Alvin Dive 601), recovered 23 Sep 1977
illary carrier are believed to be the conse- (Alvin Dive 790): HOLOTYPE (USNM
quence ofa commensal or parasitic lifestyle 145086) removed from the infrabranchial
similar to the jaw reductions seen in other cavity of Xyloredo ingolfia Turner 1972
parasitic genera within the Arabellidae. The (Family Pholadidae). Paratype (USNM
smalljaw apparatus ofP. turnerae is a trans- 145087) specimen with anterior end ex-
lucent amber structure showing no indica- tending out ofthe exhalent siphon ofa pho-
tion of the mineralization seen in labidog- lad belonging to an undescribed genus of
nath jaws, again in agreement with the the subfamily Xylophagainae. Paratype
prionognath jaw type. (MCZ 20008) specimen with anterior end
In addition tojaw structure, several other extending out of the excurrent siphon of a
characteristics associate P. turnerae with the pholad belonging to an as yet undescribed
family Arabellidae. Arabellids are charac- genus ofthe subfamily Xylophagainae. Wash
terized as having a cylindrical body ofnear- material from recovery box carrying panels
ly uniform width, a reduced prostomium N-30 and N-42; panels submerged 5 and 6
lacking appendages and uniramous para- Sep 1975 {Alvin Dives 601 and 602, re-
podia (Hartman 1944). Members of the spectively), recovered 23 Sep 1977 {Alvin
Oenonidae Kinberg, 1865 (emended by Dive 790): Paratype (USNM 145089).
Colbath 1989a), which also have prionog- Wood Panel N-83; submerged 23 Sep 1977
nath jaws, differ from P. turnerae in the {Alvin Dive 790), recovered 3 Aug 1980 {Al-
possession of one to three antennae, elon- vin Dive 1031): Paratype (USNM 145088).
WHOI
gate postsetal lobes, prominent dorsal cirri, Deep Ocean Station No. 1, 39°
and geniculate setae (Colbath 1989a). 45.3'N, 70°41.2'W, 1767 m. Wood Panel
Hartman (1944) described the Arabelli- N-68; submerged 17 Aug 1976 {Alvin Dive
dae as possessing simple, limbate setae 685), recovered 29 Jul 1977 {Alvin Dive
sometimes accompanied by projecting acic- 773): Paratype (MCZ 20009).
ular spines (or ventral setae [Colbath Description. —Specimens, preserved in
1989b]). Capillary setae have also been de- alcohol, light yellow to buff. Body long and
scribed for some of the parasitic species of slender (Fig. 1A), flattened ventrally and
Arabellidae (Pettibone 1957). The thick weakly arched dorsally. Body tapered an-
emergent spines and capillary setae of P. teriorly from about setiger 10, sides parallel
turnerae are both compatible with its inclu- for most ofbody, tapered near the posterior
mm
sion within the Arabellidae. The character- end. Holotype 163 setigers, 15.4 long
mm
istic limbate setae are absent in this species, with maximum width 0.23 excluding
226 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
B
USNM
Fig. 1. Pholadiphila turnerae: A, Entire worm, holotype 145086, anterior end on the left and the
body has been twisted several times (Scale bar = 1.0 mm); B, Pygidial region, p = pygidium (Scale bar = 200
Aim); C, Anterior end (Scale bar = 100 nm)\ D, Median parapodia, anterior view (Scale bar = 20 nm).
VOLUME 105, NUMBER 2 227
CD-:
Fig. 2. Jaw apparatus ofPholadiphila turnerae drawn from a squash preparation ofparatype MCZ 20009:
A, Maxillae I, bp = basal plate, a = alae; B, Mandibles; C, Maxillae II; D, Maxillae HI; E, Maxillary carrier
(Scale bar = 20 jum).
parapodia. Largest specimen examined 262 illae; MI gracile falcate, bifid with a pro-
mm
setigers, 19.2 longwith maximum width nounced gap between the falx and the
mm
0.27 excluding parapodia. Prostomium smooth base (Fig. 2A), MIR with a thick-
conical, indistinctly separated from setiger ened low cylindrical boss (basal plate, sensu
1, antennae, palps, andeyespots absent (Fig. Wolf 1980) possessing a pair of short alae;
1C). Prostomium and peristomium fused. Mil with 6 appressed, blade-like processes,
Cuticular jaw apparatus: 3 pairs ofmax- 5 posterior with a pair oflow bosses on the
PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
228
USNM
Fig. 3. Pholadiphila tumerae: A, paratype 145087 with its anterior end extending from the siphonal
opening ofa specimen ofan undescribed Xylophagainae (Family Pholadidae), most ofthe body may be seen
coiled within the branchial chamber ofthe pholad (Scale bar = 1.0 mm); B, Capillary seta; C, Stout, emergent
spine; D, Acuminate seta (Scale bars B-D = 5 yum)-
medial border, basal portion unarmed, ex- stout spines and capillary seta (Fig. 3B) be-
tendingposteriorto the base ofMI (Fig. 2C); ginning on setiger 3; a stout, sub-acicular
Mill small, avicular, with wide base and 2 spine added at setiger 10; 2 stout, supra-
sharply pointed teeth (Fig. 2D). Maxillary acicular spines, a supra-acicular capillary
carrier slender, short (shorter than MI sensu seta and 2 sub-acicular acuminate setae (Fig.
Colbath 1989b), cylindrical, recurved, an- 3D) beginning at setiger 19 or 20 (the su-
terior with a pair of dorsal bosses and a perior acuminate seta formed by transfor-
single ventral extension (Fig. 2E). Mandi- mation of one of the stout spines with in-
bles a pair of large flat plates united poste- termediates occurring on setigers 18 and 19)
rio-medially; anterior border of each plate and continuing to the pygidial region. Final
slightly convex with single weak tooth at setiger with two short, supra-acicular spines;
anterio-medial margin (Fig. 2B); each man- 2 preceding setigers with 2 stout, supra-acic-
dible with a slightly curved, free end ap- ular spines and a sub-acicular, acuminate
proximately equal in length to the plate. seta. Capillary and acuminate setae hirsute
Parapodia conical, with single stout acic- throughout, stout spines weakly hirsute pos-
ula (Fig. ID); with 1 stout spine (Fig. 3C) terior to setiger 20 (Fig. 3B-D). Posterior
and a small, supra-acicular capillary seta region with 7 (9 in the largest specimen ex-
(often broken) on setiger 1; 2 stout, supra- amined) distinct, asetigerous segments and
acicular spines on setiger 2; 2 supra-acicular an undifferentiated cylindrical region ante-
VOLUME NUMBER
105, 2 229
rior to the pygidium; anus terminal (Fig. maxillary carrier of P. turnerae being ap-
IB). proximately equal in length to the maxillae
Etymology.—This species is named in while those ofall other arabellids are much
honor ofDr. Ruth Turner in recognition of longer than the maxillae.
both her extensive work with the wood bor- Reductions in the arabellid setal pattern
ing bivalve mollusks and the support and are seen in the parasitic species Drilonereis
encouragement she has shown me. benedict Pettibone, 1957 which has no
i
Remarks. —In some respects Pholadiphi- emergent setae and in the two species ofthe
la turnerae has a less reducedjaw apparatus genus Haematocleptes, H. terebellidis Wi-
than many of the parasitic genera in the ren, 1886 and H. leaenae Hartman & Fau-
Arabellididae. The well-developed, dia- chald, 1971, which possess slender, distally
mond-shaped mandibular plates that are pointed setae rather than limbate setae. The
fused along part of their length are similar setal arrangement ofPholadiphila turnerae
to the mandibles offree-living arabellids. In agrees with that of the above mentioned
the genera Labrowstratus, Haematocleptes species as all other members ofthe arabel-
and Oligognathus the mandibles are re- lids (parasitic or free-living) possess limbate
duced to small plates and they are entirely setae with a well-developed blade (sensu
absent in the parasitic species ofDrilonereis Colbath 1989a). The acuminate setae and
Claparede, 1870. The 3 pairs of well-de- the strong spines of P. turnerae may be an
veloped maxillae (MI falcate, Mil and Mill adaptation to the parasitic or commensal
toothed) ofP. turnerae are most similar to existence of this species, affording strong
those of the parasitic species of the genus purchase against the body of its molluscan
Drilonereis that possess 4 pairs ofmaxillae host. These setae are more highly developed
and to those of the free-living arabellids than the setae seen in other parasitic ara-
which possess 5 pairs of well-developed bellids being more robust, more numerous
maxillae. In the remaining parasitic genera, and extending out much further from the
the maxillae ofOligognathus have been re- parapodia.
—
duced to 3 pair of unidentate hooks while Ecology. Endoparasitism among the
those of Labrorostratus and Haemato- Polychaetes is known to occur almost ex-
cleptes have been reduced to 2 pair ofsmall clusively in members ofthe family Arabel-
cuticular pieces. lidae. A review ofthe known endoparasitic
Whereas the maxillae of P. turnerae are arabellids (review by Pettibone 1957, Day
less reduced than those of several parasitic 1960, Hartman & Fauchald 1971, Emerson
Wu
arabellids, its maxillary carriers are greatly 1974, Amaral 1977, Uebelacker 1978,
&
modified. Free-living arabellids and both et al. 1982, San Martin Sarda 1986) re-
free-living and parasitic members ofthe ge- veals that, with the exception of Oligog-
nus Drilonereis possess a pair oflong, slen- nathus bonelliae Spengel, 1882 (found liv-
der maxillary carriers with a third carrier ing within the body cavity ofthe Echiuroid
attached ventrally. The paired maxillary Bonellia viridis Rolando), all the known ar-
carriers have been fused in Labrorostratus, abellid parasites have been found within the
Haematocleptes and Oligognathus with the body cavity or gut (in the case of Haema-
third carrier retained in the former two gen- tocleptes terebellidis) of polychaete hosts.
era and lost in Oligognathus. The maxillary Pholadiphila turnerae is unlike most ofthe
carriers of Pholadiphila turnerae are fused parasitic arabellids in that it lives external
along their entire length and the ventral ex- to the host's body cavity (within its mantle
tension may represent a vestigial third car- cavity) and is the first arabellid reported to
rier. There is also a size reduction in the form an association with a mollusk.
230 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
It is not clear if the association between sively from the mantle cavity of a shallow
P. turnerae and the wood boring bivalves water bivalve host.
is commensal or parasitic. Ifthe polychaete With greater sampling effort in the deep
utilizes the host's mantle cavity simply as sea close associations between polychaetes
a refuge from predators (as Pettibone [1984] and bivalves arebeingnotedwith increasing
suggested may be true of the Polynoidae frequency. Pettibone (1984, 1986) has de-
found in the mantle cavity of deep-water scribed two species of Polynoidae living
seep and vent mussels), then this would be within the mantle cavity ofmytilid mussels
an example of commensalism. There are from both the Galapagos Rift hydrothermal
several indications, however, that this as- vents and the Florida Escarpment methane
sociation is actually a parasitic one. The seeps. Three species belonging to a recently
mouthparts ofP. turnerae are reduced in a described family, the Nautiliniellidae Miura
similar manner to those ofother arabellids & Laubier, 1989 (emended by Miura & Lau-
known to be parasiticandargues forreliance bier [1990]), have been described from Jap-
upon a host for nutrition. Possible food anese cold-seeps living within the mantle
sources within the pholad mantle cavity are cavities oftwo species of Calyptogenia and
the gill filaments, the mucus coat on these a species ofSolemya. Blake (1990) has also
filaments, or perhaps partially digested ma- described a fourth species of Nautilinielli-
terial within the pholads wood storing cae- dae from the Laurentian Fan in the Western
cum. The mere presence ofsuch a large or- North Atlantic (3800-3900 m) living in the
ganism in the mantle cavity (Fig. 3A) may mantle cavity of Thyasira insignis. Phola-
impede water flow to such an extent that a diphila turnerae is yet another example of
significant stress is placed upon the pholad a deep-sea polychaete which has taken up
host. Ifthis is the case then this association existence within a bivalve mantle cavity.
must be considered a parasitic (parasite lives The presence ofcommensal/parasitic poly-
at the expense ofits host) ratherthan a com- chaetes in the bivalve mantle cavity seems
mensal (host is unaffected by the associated more common in the deep sea than in shal-
species) relationship. low water environments.
Despite a large sampling effort in shallow
waters, there have been few reports ofpoly-
Acknowledgments
chaetes living as commensals or parasites
within the mantle cavity of bivalve mol- The pholads were collected, dissected
lusks. A specimen ofthe syllid Parasyllidea from wood panels, and the photographic
humesi Pettibone, 1961 was reported from work carried out as part of R. D. Turner's
the mantle cavity of the intertidal bivalve studies of deep-sea wood-boring commu-
Tellina nymphalis Lamark, however this nities supported by the Office ofNaval Re-
must be considered as a fortuitous associ- search, Contract no. N00014-84-0258 with
ation because only one ofthe approximate Harvard University. The SEM pictures were
200 specimens of this polychaete collected taken by R. Pinto (Museum ofComparative
by Pettibone (1961) was found within the Zoology, Harvard University) and A. Cole-
bivalve, the remainderwere free-living. The man (Museum of Comparative Zoology,
polychaeteAntonbruunia viridis Hartman & Harvard University) did the photographic
Boss, 1965 (Family Antonbruunidae) has work. Carpenter (Organismal and Evo-
J.
been described as a commensal in the man- lutionary Biology, Harvard University)
tle cavity ofthe bivalve Lucinafosteri Hart- provided the use of photomicrographic
man & Boss, 1965 collected in 68-82.3 m equipment. Insightful review by B. Hilbig
offMadagascar. To date this is the only re- (Science Applications International Cor-
port ofa polychaete species collected exclu- poration, Woods Hole) improved an early
VOLUME 105, NUMBER 2 231
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6:1-327.
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