A.M. ZOOLOGIST, 9:829-835 (1969).
Boring of Shell by Caobangia in Freshwater Snails of Southeast Asia
MEREDITH L. JONES
Division of Worms, Department of Invertebrate Zoology,
Museum of Natural History, Smithsonian Institution,
Washington, D. C. 20560
SV.NOPSIS. Giard (1893) described Caobangia billeti, a freshwater sabellid polychaete,
based on material collected in what is now northern North Vietnam. Up to the
present time it had not been re-collected and Giard's observations that it is hermaphroditic, that its eggs undergo internal development, and that, rather than having a
posterior terminal anal opening, the anus opens far forward, have been questioned
from time to time.
Recently collected material, as well as older material in the collections of the
Division of Molluscs, Museum of Natural History, Smithsonian Institution, has allowed
the confirmation of Giard's findings and the observation of the burrows of
Caobangia in 22 species of molluscs from fast-moving streams in Ceylon, northern
India, Assam, Burma, Thailand, Laos, Java, Sabah, and various of the Philippine
Islands.
Burrowing in snail shells appears to take place subsequent to larval metamorphosis
as young individuals grow posteriorly from a capsule-like structure through the
periostracum and into the calcium carbonate of the snail shell. There appears to be no
differentiated area of the worm which can be implicated as the site of acidic
secretions, and the setae of the worms seem not to be unusually worn, as would be the
case if they were used to wear away the shell material.
Giard (1893) described Caobangia billeli,
a sabellid polychaete, based on material
from the vicinity of Cao Bang in what is
now northern North Vietnam. The specimens were associated with a freshwater
snail, identified by Giard as a species of
Melanin, and were found in blind-ending,
tear drop-shaped burrows in the shell of
the snails. Giard went on to describe a
number of unusual characters of Caobangia: the gut is recurved within the body
and the anal opening is in the anterior
part of the body; the branchial crown is
supported by an extensive internal structure referred to by Giard as a hyaline cartilaginous skeleton (". ,un squelette cartilagineux hyalin. .", p. 424); there are palmate hooks on the first setigerous segment;
I wish to acknowledge the willing assistance of
Dr. Joseph P. E. Morrison, Division of Molluscs,
Museum of Natural History, Smithsonian Institution, who directed my attention to the study material, to Dr. Rolf A. M. Brandt, SEATO Medical
Research Project, Thailand, for freshly collected,
well-preserved material, and to Dr. Marian H.
Pettibone and Nancy M. Cramer, both of the
Division of Worms, for comments and criticisms of
this paper.
there is a broad pigmented area of glandular tissue on the ventral surface of the
anterior region; larvae are brooded internally where they develop seven to eight
setigerous segments and are provided with
cilia and a pair of eyes; although he did
not observe testes, Giard conjectured that
Caobangia was hermaphroditic.
Since the original description, no further
material has become available, and subsequent citations in the literature consist of
unannotated listings of Caobangia as a sabellid of the subfamily Fabriciinae or as a
curious freshwater polychaete (Chamberlin, 1919; Mclntosh, 1922; Zenkevitsch,
1925; Monro, 1939; Hartman, 1951, 1959;
and Wesenberg-Lund, 1958), a note mentioning the polytrochous nature of its larvae (Dawydoff, 1959), a suggestion that a
subfamily, Caobangiinae [sic] be erected
for the genus (Chamberlin, 1919), and as
a point of discussion in the polemics of
Mesnil (1901 a, b) and Nusbaum (1901).
It is of interest to note that three extensive
studies of the Sabellidae (Bush, 1904;
Rioja, 1923; Johansson, 1927) cite Giard's
829
MEREDITH L. JONES
EXPLANATION OF FIGURES
Key to lettering: A, abdomen; AG, ascending
gut; AH, abdominal hooks; AO, anal opening; BA,
burrow aperture on suture line; BC, branchial
crown; BL, burrow lining; CB, lateral band of
cilia; DAH, embedded developing abdominal
hooks; DBC, developing branchial crown buds;
DCS, developing "cartilaginous skeleton"; DG, descending gut; DPH, embedded developing palmate
hooks; EL, eggs and/or larvae; EY, eye; FM, fungal
mat; GA, granular aggregations; GC, enlarged
gut cavity; LM, dorsal longitudinal muscle; LPH,
larval palmate hooks; MR, mouth region; PH,
palmate hooks; SF 1, first setal fascicle; SF 6, sixth
setal fascicle; T, thorax; VP, ventral pigmented
area; X, desiccated remnant of a specimen of
Caobangia sp.; YG, area of remaining yolk granules.
FIG. 1. Adult Caobangia sp. from a decalcified
Rrotia sp. from Thailand; scale line 1 mm.
paper in their bibliographies but do not
mention Caobangia in their texts.
It is unfortunate that Giard's description
is somewhat ambiguous in some places,
for it has led both Nusbaum (1901) and
Hartman (1951) to conclude that the anal
opening is on the ventral surface rather
than the dorsal (see below). Further, it
has caused Banse (1957, pp. 98-99) to conclude that Giard made a bad choice of
words and that Giard really meant that the
posterior end of Caobangia is reflected
under the ventral surface of the anterior
region in much the same manner as is seen
in the Sabellariidae. It will be seen below
that, as Giard has stated, the gut, itself, is
looped within the body of Caobangia and
opens far forward on the dorsal surface.
All other observations of Giard also have
been confirmed in the present study.
The material upon which the present
study is based is part of the collection of
the Division of Molluscs, Museum of
Natural History, Smithsonian Institution,
and is comprised of 24 species of molluscs
of four families (Pleuroceridae, Thiaridae,
Viviparidae, and Unionidae) representing
12 genera (Ganga, Hemimitra, Paludomus
and Tanalia; Antimelania, Balanocochlis,
Brotia, Stenomelania, and Tarebia; Cipangopaludina and Mekongia; and Hyriopsis).
The molluscs were collected at localities
in Ceylon, India, Burma, Thailand, Laos,
Java, Sabah, and certain of the Philippine
Islands; all were collected in freshwater
streams and rivers and, where additional
data were included, at elevations ranging
up to 4,000 feet, in fast-moving water. Although most of the distributions were determined on the basis of dried remnants
of Caobangia (Fig. 8, X), sufficient preserved material was available from Thailand and Sabah so that proper morphological and histological studies could be
carried out; the latter was isolated from
molluscan shells by decalcifying the shell
material with 5% nitric acid in 70% ethyl
alcohol.
GENERAL MORPHOLOGY OF
Caobangia
In spite of indications that there may be
as many as five species of Caobangia represented in the study material, the general
morphology of the genus seems not to
reflect specific differences. As a point of
departure, therefore, specimens from Thailand and Sabah will serve to illustrate
some of the unique characters of the
genus and to confirm Giard's observations.
Adult worms (Figs. 1, 2) are approximately 5 mm in length and about 1 mm
in diameter at their widest region.
The general shape of Caobangia is
somewhat reminiscent of that of a sipunculid or a phoronid in that there is no obvious segmentation and that the area which
might be considered posterior (hereafter
BORING OF FRESHWATER SNAILS BY Caobnngia
BC
GA
831
MR
GA
FIG. 2. View of right side of an adult Caobangia
sp. from Ranau, Sabah.
FIG. 3. Dorsolateral view of a larval Caobangia sp.
dissected from an adult from Ranau, Sabah.
called "basal") is smoothly rounded and
bears no anal opening. The diameter of
the basal third of the body is enlarged to
about twice that of the "anterior" (=apical) region.
Although there are no well-defined segments, seven paired fascicles of setae indicate a thoracic region of seven segments
(Fig. 2, T); this is followed by from five to
12 pairs of transverse rows of avicular
hooks (Figs. 1, 2, AH) which suggest the
beginning of an abdominal region (Fig. 2,
A) and then by numerous paired fascicles
of one or two limbate capillary setae each,
which suggest a continuation of the abdominal region.
The apical end is provided with a branchial crown (Figs. 1, 2, BC) characteristic
832
MEREDITH L. JONES
ofsabellid polychaetes of the subfamily
Fabriciinae, and the oral opening (Fig. 2,
MR) is centrally located at the base of the
crown. A narrow descending gut (Fig. 2,
DG) leads basally to an enlarged cavity
(Fig. 2, GC) which occupies most of the
bulbous basal region. A further narrow intestinal canal departs from the cavity in
the area of the basal end, makes a loop
first dorsally then ventrally and moves apically, internal to the ventral surface of the
animal; the ascending gut (Figs. 1, 2, AG)
runs to about the level of the seventh pair
of setal fascicles (the demarcation of the
thoracic from the abdominal region)
where it moves to the dorsal surface, almost invariably on the right side. The anal
opening (Fig. 2, AO) is thus, on the dorsal surface at about the level of the third
or fourth setal fascicle.
In the region of the basal loop of the
gut, numerous developing eggs and larvae
(Fig. 2, EL) can be seen; histological
preparations reveal that here, too, is an
area where sperm are formed, which
confirms Giard's suggestion that Caobangia
is a hermaphroditic form. There are anatomical indications that it is a crossfertilizing hermaphrodite, rather than selffertilizing.
The setae of adult Caobangia are not
unreasonably different from those of more
typical sabellids; however, certain of those
of the first setal fascicle are quite stout and
are palmate, being provided with a large
central fang and from four to 12 smaller
secondary denticles (Fig. 2, PH).
In the case of preserved material
Caobangia is whitish, but, as Giard noted,
there is a ventral pigmented area in the
region of the first to third fascicles of setae
(Figs. 1, 2, VP), as well as smaller patches
along the course of the apically moving
gut on the ventral body surface, and one
on the ventral surface just anterior to the
ascending gut, at the level of the seventh
setal fascicle.
Larvae (Fig. 3) which have developed
internally are from 0.75 to 0.95 mm in
length and are ca. 0.20 mm wide. They are
provided with a pair of eyes (Fig. 3, EY)
with lenses, and a mouth opening (Fig. 3,
MR) which is surrounded by tufts of cilia;
there is no anal opening. Seven pairs of
fascicles of limbate capillary setae are
present and the larvae have welldeveloped bands of cilia, segmentally arranged (Fig. 3, CB). Just dorsal to the
seventh setal fascicle there are two palmate
hooks on each side which are similar to
those found in the first fascicle of adults
(Fig. 3, LPH). Developing palmate hooks
can be seen internally in larvae at the level
of the first fascicle (Fig. 3, DPH) and
internal, developing, thoracic, avicular
hooks are visible near the seventh setal
fascicle (Fig. 3, DAH). Aggregations of
granular material are present in the basal
region of both larvae and adults (Figs. 2,
3, GA).
BURROWS
As Giard (1893) has observed, most of
the burrow openings of Caobangia are to
be found at the apex of the snail shell.
Quite frequently the entire tip of the apex
is eroded (Figs. 4 and 5) and the
truncated surface is covered by a mat of
fungi (Fig. 1, FM) which is pierced by the
apertures of Caobangia burrows. The
burrows themselves are generally oriented
internally along the axis of the columella
of the snail shell, although occasionally
they are formed in the thinner material
comprising the outer whorl. In addition,
Caobangia apertures are found along more
proximal sutures (Fig. 6, BA) and even
on the outer faces of the whorls.
Internally, the burrows reflect the shape
of the animals in that from the narrow
opening the diameter gradually increases
and the widest part is at the internal end
(Figs. 7, 8). Further, the burrows appear
to be smooth and, when occupied by
Caobangia, are lined with what appears to
be a mucous sheath (Fig. 1, BL).
Xo burrows appear to impinge on or
connect with other burrows (Figs. 7, 8)
and all are restricted to the mineralized
part of the molluscan shell.
Although no observations have been
BORING OF FRESHWATER SNAILS BY Cnobangia
833
FIG. 4. Brolia sp. from Thailand showing the
eroded apex of its shell; scale line 10 mm.
FIG. 5. View of the eroded apex of a shell of
Brotia sp. from Thailand' scale line 1 mm.
FIG. 6. View of the apex of a shell of Mekongia
jtillieiii (Deshaycs) from Laos: scale line 1 mm.
made of burrows being formed, the examination of a number of developmental
stages has allowed some deductions as to
burrowing activities. Larvae liberated
(probably by the rupturing of the adult
FIG. 7. View of a broken surface through the thickness of a valve of Hyriopsis tlelaportei Crossc
and Fischer from Laos; scale line 1 mm.
FIG. 8. View of a broken surface subparallel to the
outer surface of a valve of Hyriopsis delaportei
Crossc and Fischer from Laos; scale line 1 mm.
834
MEREDITH L. JONES
body wall) settle on the periostracum or
on the bared calcium carbonate of a shell.
The settled larvae form a dome-shaped
capsule over themselves and are coiled
within it, with their basal end in the center of the coil. As the larvae grow, the
basal end either penetrates the capsular
floor or continually forms capsular material as it moves through the periostracum
into the mineralized shell. Further growth
in length and girth ultimately result in the
formation of the burrow of the adult.
Whole mounts of developing larvae show
that it is during this period of elongation
that a diverticulum arises from the basal
end of the developing gut. This diverticulum, during the course of its linear growth,
undergoes a looping and then movement,
internal to and within the body wall,
apically; this sets the pattern for the strange
architecture of the adult gut.
As to the actual means of burrowing,
mechanical abrasion by the stout palmate
setae of both the larvae and the adults
would seem not to be contributory, because of the restricted location of the
setae, as well as the fact that, although
certain of the palmate setae appear worn,
they are not sufficiently so to have played a
part in forming the burrow. Acidic secretions for chemically forming a burrow
might originate from the glandular areas
associated with the anterior pigment
patches, but, once again, the source of such
a secretion would seem to be too restricted to account for such activity and, further, larval burrowing takes place before
such a glandular area is formed. Since it is
the basal end of the larva which appears to
initiate burrowing activity, it might be
assumed that acidic secretions are elaborated from this region; however, histological
observations do not reveal glandular tissue
in the basal end of either the larvae or
the adult. A final possible explanation
might be the lowering of the pH of the
fluid of the burrow due to metabolic activities of the worm. This would account for
the close correlation of shapes of body and
burrow, but does not explain how initial
penetration is accomplished, how the bur-
row is restricted to the mineralized shell,
nor how burrows are kept from impinging
upon one another. More definitive suggestions on how the burrow is formed by
Caobangia must await observations of living animals.
A final comment concerning burrowing:
it was mentioned above that Caobangia
has been found 'associated with Hyriopsis,
a freshwater clam (Figs. 7, 8). Of the
several valves available for study, several
came from clams which were alive when
collected and the remainder came from socalled "dead" shells. The latter were obviously dead because of mud stains, as well
as burrow apertures of Caobangia, on their
inner surfaces. Although we have usually
thought of Caobangia as being associated
with living molluscs, the relationship may
not be obligatory. Further, if Caobangia is
not restricted to "living" calcium carbonate then limestone outcrops along river
or stream banks might serve as reservoirs
from which larvae might proceed to "infect" new molluscs.
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