Table Of ContentPROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
112(4):661-666. 1999.
Morphological observations on a hatchling and a paralarva of the
vampire squid, Vampyroteuthis infernalis Chun
(MoUusca: Cephalopoda)
Richard E. Young and Michael Vecchione
(REY) Department of Oceanography, University of Hawaii, Honolulu, Hawaii 96734, U.S.A.;
(MV) National Marine Fisheries Service, Systematics Laboratory,
National Museum of Natural History, Washington D.C. 20560, U.S.A.
—
Abstract. We present morphological observations on two very small vam-
mm
pire squids. One, a trawl-caught hatchling of 8 mantle length (ML), had
embryonic features including internal yolk, broad arm-like filaments, and lack
ML
of mantle-head fusion. The other was a 9 rrmi paralarva collected by
submersible and photographed alive aboard ship. Although only slightly larger
than the hatchling, its morphology was much more like that oflarger specimens
than that of the hatchling, except for the oblique orientation of its fins.
The vampire squid, Vampyroteuthis in- Hawaiian Islands on a cruise of the RTV
fernalis Chun, 1903, is the only living New Horizon off leeward Oahu on 1 July
member of the Vampyromorpha, the sister 1996. The collecting gear was an opening-
&
group to the Octopoda (Young Vecchione closing net that fished between 0130 and
m
1996, Young et al. 1998). Through out- 0743 h at a depth of about 1050-1300
group and ontogenetic comparisons, this (Sta. 62). The specimen was sorted from the
species holds important clues to our under- catch soon after collection, and photographs
standing of cephalopod evolution and to the were taken aboard ship shortly thereafter.
reconstruction of ancestral character states. The paralarva (9 mm ML, USNM 816886)
Very little has been published, however, was captured in the eastern Gulf of Mexico
concerning its anatomy, behavior or embry- using a pelagic suction sampler from the
ology. As a result, any new information is manned submersible Johnson Sea Link II
valuable. We report here on two very small during dive 1453, 30 August 1987,
m
vampire squid. One, a hatchling captured 24°30'5"N, 83°45'12"W at 830 depth. It
by trawl, was dead but in excellent condi- was photographed while still alive imme-
tion when retrieved. The other was a para- diately after the submersible returned to its
larva (= "stage 1 larva", Pickford 1949a) support ship.
captured ahve from a submersible and pho-
tographed in a shipboard aquarium. These Observations
are the first observations of a live vampire —
squid paralarva. Together, these observa- Hatchling. The trawl-caught animal
tions support many morphological charac- was clearly a hatchling (i.e., there was no
ters described by Pickford (1949a) from chorion surrounding it), but morphological-
damaged specimens. ly it was an advanced embryo presumably
incapable of feeding except from its inter-
A
Materials and Methods nal yolk supply. large mass of yolk glob-
ules, presumably within a large internal
mm
The hatchling Vampyroteuthis (8 yolk sac, was seen through the transparent
ML, USNM 885891) was captured near the gladius ventral and lateral to the esophagus.
662 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
Fig. L Photographs of freshly collected Vampyroteuthis infemalis hatchling (8 mm ML). A, Lateral view
with dissecting pin laying across mantle to prevent motion from the ship's rolling; B, Dorsolateral closeup of
head and anterior mantle.
During attempts to photograph the embryo lA with Fig. 3), the eyes were very small
aboard ship, a pin was placed on top of the and the mantle was not fused to the head in
mantle to keep the animal from rolling (Fig. the nuchal region (Fig. 2). The eye fold
lA). This resulted in a sausage-shaped ex- formed a circular fold around the base of
trusion of yolk from the buccal region. each eye, not yet enclosing the eye. Al-
The body of the hatchling was very large though squid eyes often are forced out
relative to the head and arms (compare Fig. through circular eyelids during capture, this
Break in tissue
Fig. 2. Schematic drawings of Vampyroteuthis infemalis hatchling, lateral, dorsal, and oral views. From top
to bottom on the oral view the arm pairs are dorsal (Arms I), filaments (Arms II), dorsolateral (Arms III),
ventrolateral (Arms IV), and ventral (Arms V).
VOLUME NUMBER
112, 4 663
was not a case in this instance. The epithe- The animal's coloration was faint pink-
Hal body could clearly be seen surrounding brown and fairly translucent. Black chro-
the lens of the eye even though the lens was matophores were scattered at several points
partially covered by the iris. on the animal, especially on the oral surface
Gelatinous tissue surrounded the arms of the arm bases and anterodorsally on the
A
and separated muscle layers in the mantle eye. light reddish-brown epidermal pig-
but did not cover the mantle muscle exter- ment was present. The pigment was most
nally. At the posterior dorsal apex of the obvious on the covering of the visceral
mantle a small knob (ca. 15 iJim) was pres- mass, the ventral surface of the head and
ent in the epithelium and partially surr- the oral surfaces of the arms. The animal
ounded by a groove. This knob is in the seemed to be neutrally buoyant although
position of the hatching organ of other small bubbles attached to the epidermis pre-
cephalopods but we find it reminiscent of vented actual—determination.
the peculiar circular feature in the photos of Paralarva. ^While nearly the same size
mm
the paralarva (Fig. 3B-D) described below. (9 vs. 8 ML), the morphology of the
The filaments (= "velar filaments", paralarva was very different from that of
&
Hochberg Nixon 1992) were intact. Each the hatchling. Except as noted below, the
was broad, short, of uniform thickness to overall appearance was similar to that of
the rounded tips (Figs. IB, 2), and lacked larger juveniles and adults (e.g., head/man-
both suckers and cirri. Their attachment to tle fusion, pigmentation, etc.). The oblique
the brachial crown was as in the adult ex- angle of the fin noted by Pickford (1949a)
cept that the filaments did not reside in a is confirmed here in photographs (Fig. 3B,
pocket, as a web was virtually absent. A C) of the living paralarva. The fins were the
V
slight ridge between arms DI, IV and first of two pairs to develop (= "juvenile
(Fig. 2) appeared to be the web precursor. fins" or "larval fins". Young & Vecchione
The arm tips were slightly damaged but all 1996); the second pair ("adult fins" Ibid)
seemed to be subequal and armed with cirri were present only as minute precursors an-
and suckers. Four developing suckers were terior to the fin-base photophore. Also ap-
counted on one arm and we assume this to parent in these live photos (Fig. 3B-D) is a
apply to all arms. Suckers had constricted peculiar circular feature at the apex of the
bases but lacked obvious stalks. Four pairs mantle. Examination of the preserved spec-
of cirri preceded the first sucker and the imen, however, revealed no obvious struc-
suckers and cirri alternated as in the adult. ture at this location. Figure 3A shows the
On the oral surface ofthe brachial crown, arms in a forward orientation, and Fig. 3B
two circular lips and a more distal fold sur- shows them in the lateral orientation. The
A
rounded the beak. break in the tissue ven- filaments were very thin and emerged from
tral to the lips and medial to this fold was pockets in the well-developed web, as in
presumably the point where yolk came out. older specimens. The incompletely retract-
Unlike in adults, the large funnel was not ed but coiled filaments are seen most clear-
embedded in the head, but no free adductor ly in Fig. 3C. The eyes of this young vam-
muscles were present. The exact orientation pire squid were relatively small (Fig. 3A,
of the very small, but damaged, fins could C), compared with those of an adult.
not be determined. The pigmented esopha-
gus, where it emerged from the brain, was Discussion
clearly visible through the transparent glad-
ius. The esophagus gradually increased in Pickford (1949a) described a young vam-
diameter posteriorly. The gladius was the pire squid in the same stage of development
same general shape as in adults but had a as the hatchling described here. However,
somewhat narrower median field. her specimen was badly damaged (mantle
664 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
Ee^S^^^I y^
A
/
* k
y/^
BUi.
Filamentyf
y-/i "rv'
M ^
/
/
/
1;
Eye
h"'
3Hf
mm
Fig. 3. Photographs oflive paralarval Vampyroteuthis infemalis (9 ML). All views dorsal. A, with arms
in anterior orientation; B, with arms and web spread laterally; C, showing coiled, partially retracted filament;
D, with arms and web folded posteriorly revealing buccal area.
VOLUME NUMBER
112, 4 665
length was thought to be 5.7 mm) and, as might provide evidence to choose between
a result, some of her conclusions have been alternative hypotheses about octopodiform
in doubt. The description here confirms evolution. However, the photographs of the
some of her more important findings (e.g., paralarva with its arms both spread laterally
mantle free from head; thick filaments). and projecting anteriorly are equivocal on
The vampire hatchling also confirms the this question.
fusion of the head and mantle in octopods Vampyroteuthis infernalis currently is
and vampyromorphs to be independent, as considered to comprise a single panmixic
&
predicted from morphology (Young Vec- species. Therefore, although our specimens
chione 1996). The broad filaments are more were collected in different oceans, we do
arm-like than in older vampire squids and not believe that the morphological differ-
add support to the interpretation that the fil- ences between them reflect interspecific
aments are the second pair of arms. If they variability. The strong differences in mor-
were ocular filaments, as suggested by phology between our two specimens, which
Young (1967), one might expect that they are nearly the same size, demonstrate the
would be especially small at this stage. The changes that occur in the early post-hatch-
embryonic eye fold in cephalopods is con- ing ontogeny of Vampyroteuthis. Pickford
tinuous with the arm bases and the partic- (1949a) described the paralarval develop-
ular arms associated with the fold have ment of V. infernalis. One peculiarity of
been used to determine the homology of this species is that early paralarvae (Pick-
arm pairs in decapods and octopods (Bol- ford's "stage 1 larvae" have one pair of
etzky 1993). Unfortunately, in the vampire fins; then a second pair develops ("stage
hatchling the eye fold does not continue 2") followed by absorption of the original
onto the arm crown, presumably because of pair ("stages 3 and 4"). She observed that
A
its advanced stage of development. fold the fins of the paralarva are set obliquely
surrounding the lips could be the remnant on the body, unlike the horizontal attach-
of a buccal crown that is otherwise absent ment of the adult fin, and suggested that the
in Vampyroteuthis (see Fig. 3D). More like- young vampire hangs head downward in
ly, however, this is the demarcation be- the water. The present observations, which
tween the gelatinous tissue and the more are the first live of a paralarval vampire
muscular region where the arm muscles squid, confirm Pickford's descriptions, such
fuse with one another and has no phyloge- as fin orientation, which were based on pre-
netic significance. served specimens.
Vampire hatchlings may drift freely in The pucker-like circular structure seen
deep water until they change into the form near the posterior apex of the paralarva's
of a typical paralarva. However, the speci- mantle is similar to that recorded in a sub-
men examined here could be an advanced adult Vampyroteuthis videotaped as part of
embryo, hatched prematurely within the a televison program about cephalopods
trawl. Pickford (1949b) stated that the ^gg ("Incredible Suckers"). No discrete struc-
size of spawned Vampyroteuthis eggs is up ture is apparent on the preserved paralarva
mm
to 4.0 in diameter. Clearly the present and we do not know the function of the
hatchling with its embryonic features (e.g., structure.
yolk) was not derived from such a small
Q.gg. An egg size of ca. 8 mm (i.e., com- Acknowledgments
parable to the mantle length) would be ex-
pected. The discrepancy cannot be ex- We thank J. Childress, University of Cal-
plained at present. ifornia, Santa Barbara, for the opportunity
Young et al. (1998) proposed that relaxed to participate in one of his cruises and we
orientation of the arms in Vampyroteuthis acknowledge the keen eye of Eric Thuesen
—
666 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
that detected the small hatchling vampire morphological and behavioral homologies.
amidst a large bucket of midwater animals. American Malacological Bulletin 10:61-69.
Richard Harbison, Woods Hole Oceano- Hochberg, F. G., & M. Nixon. 1992. Order Vampyro-
morpha Pickford, 1939. Pp. 211-212 in M. J.
graphic Institution, provided the paralarval Sweeney, C. E E. Roper. K. M. Mangold, M.
vampire and Ronald Gilmer took the pho- R. Clarke, & S. von Boletzky, eds.. Larval' and
tos. Bruce Collette, Michael Sweeney, Eliz- juvenile cephalopods: a manual for their iden-
—
abeth Shea, and a helpful anonymous re- tification. Smithsonian Contributions to Zool-
viewer provided suggestions for improve- ogy 513:282 pp.
ment of drafts of this paper. The research Pickford, G. E. 1949a. Vampyroteuthis infernalis
Chun. An archaic dibranchiate cephalopod. XL
reported here was funded in part by a grant/ —
External anatomy. Dana Report 32:1—132.
cooperative agreement from the National
1949b. The distribution of the eggs of Vam-
. —
Oceanic and Atmospheric Administration, pyroteuthis infernalis Chun. Journal of Ma-
project #R/MR-51, which is sponsored by rine Research 8:73-83.
the University of Hawaii Sea Grant College Young, R. E. 1967. Homology of retractile filaments
—
Program, SOEST, under institutional grant of vampire squid. Science 156:1633-1634.
No. NA86RG0041 from the NOAA Sea , & M. Vecchione. 1996. Analysis ofmorphol-
Grant Office, Department of Commerce. ogy to determine primary sister-ta—xon relation-
ships within coleoid cephalopods. American
UNIHI-SEAGRANT-JC-99-03.
Malacological Bulletin 12:91-112.
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—
Boletzky, S. von. 1993. The arm crown in cephalopod biodiversity and ecology. South African Jour-
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