Functional Anatomy of Bankia fimbriatula Moll & Roch, 1931 (Bivalvia: Teredinidae)

2008·8.6 MB·English

by  Walter Narchi

THE VELIGER
The Veliger50(4):309-325 (December 16, 2008) © CMS, Inc., 2007
Functional Anatomy of Bankia fimbriatula Moll & Roch, 1931
(Bivalvia: Teredinidae)
MARIA JULIA MARTINS-SILVA and WALTER NARCHL
1
'DepartamentodeZoologiada Universidadede Brasilia, Campus Universitario, AsaNorte, 70910-900Brasilia, DF, Brazil
(e-mail: [email protected])
Abstract. Bankiafimbriatula Moll & Roch, 1931, is a highly specialized bivalve adapted for boring into wood.
Specimenswerecollected alivefrom a mangrove region at Praia Dura, Ubatuba, Sao Paulo, Brazil and maintained in
an aquarium at room temperature (21°C) at the laboratory ofthe Department ofZoology, University ofSao Paulo.
Studies ofthe anatomy were carried out on both relaxed and preserved specimens. Special attention was paid to the
siphons, pallets, ctenidia, labial palps and mantle. The siphons are fairly long, and separated. The inhalant and
exhalant siphons have ciliary activity at the tentacles, as described previously for Nausitorafusticula (Jeffreys, 1860).
Theposteriorctenidiaarehomorhabdic. EachctenidiumofB. fimbriatulaisformed bytheexternal demibranch only,
with the blades in a "V" form. The ctenidia, associated with the rejection tracts of the mantle, present a good
mechanism to deal with largequantities ofparticles, probably an adaptation forlifein turbid waters. The labial palps
areextremely reduced. The functional anatomyofB.fimbriatula suggests that both plankton and wood probablyare
important as food for this species.
INTRODUCTION The genus Bankia Gray, 1842, includes twenty-three
species (Turner, 1971) in the subfamily Bankiinae
TheanatomyofspeciesofTeredinidae has been studied
Turner, 1966, thirteen of which occur in the Brazilian
by several authors, including Quatrefages (1849),
littoral.
Menegaux (1889), Ridewood (1903), Sigerfoos (1908), Among species of Bankia, Sigerfoos (1908) studied
Potts (1923), Lazier (1924), Atkins (1937), Purchon
the anatomy of Xylotrya gouldi [= Bankia gouldi
(1939, 1941, 1960), Nair (1957), Bade et al. (1961, (Bartsch, 1908)], Clapp (1951) made observations on
1964a, 1964b), Turner (1966), Rancurel (1971), Sar-
aswathy & Nair (1971), Lopes & Narchi (1998) and living Teredinidae and described the siphons of B.
Lopes et al. (1998). Some references [Atkins (1937), gmoaunltdli.e BoafdeBaentkiala. m(1i9n6i1m)ail[l=ustBraatnekdiaancdardiensactraib(eGdratyh,e
Purchon (1941, 1960), Clapp (1951), Morton (1970,
1978), Martinez (1987), Lopes & Narchi (1998) and 1827); Turner (1966. 1971)]. Bade et al. (1964a, 1964b)
studied the digestive and respiratory systems of the
Lopes et al. (1998), are restricted mainly to the same species. Turner (1966) described the posterior
structure and function ofspecific organs.
region of B. gouldi, and described the anatomy of
&TRhoechf,unc1t9i3o1n,alisantahetommayionffBoacnuksiaoffimtbhrisiatwuolrak;Mowlel MBoalnlk,ia1s9e3t1,aceaand(TBr.yoanu,st1r8a6l3i)s,(BC.aicmaamnp,ane1l9l2a0)t.a RSaorcahsw&-
analyzed the functioning of the siphons, the muscles athy & Nair (1971) described the anatomy ofB. indica.
associated with the siphons and pallets, and the ciliary Tanetal. (1993)made a studyofthe shelland palletsof
currents related to the selection of food and particles
for elimination. A detailed study of the anatomy and the early developmental stages ofB. gouldi.
This paper presents the first anatomical study of
function ofthe stomach will be presented in a separate
Bankiafimbriatula.
paper.
Bankia fimbriatula occurs mainly in tropical warm MATERIAL AND METHODS
waters around the world (Turner, 1966). On the
Brazilian coast it has been reported from the littoral Specimens ofB.fimbriatula were collected during 1992
zone of Sao Paulo State (Lopes & Narchi, 1998), and 1994 in mangrove trees at Praia Dura, Ubatuba,
Parana State (Miiller & Lana, 1986, 1987; Skinner et Sao Paulo, Brazil (45T5'W, 23°30'S) (Figure 1). This is
al., 1993) and Rio de Janeiro State (Silva et al., 1989; the second most abundant species ofTeredinidae in the
Junqueira et al., 1989; Martins-Silva et al., 1990 and area, living at a salinity range from 0-33%o (Lopes &
Junqueira & Silva, 1991). Narchi, 1993). The animals were kept inside the wood,
in a seawater aquarium with constant aeration and at a
+Dr Walter Narchi (died in 2004) salinity of20%o and a room temperature of22°C, where
Page 310 The Veliger, Vol. 50, No. 4
Figure Map ofthe mangrove region at Praia Dura, Ubatuba, Sao Paulo, Brazil, with indications ofthecollection stations (*1
and 2).
they stayed in good condition for almost two years. weredeposited in the MuseudeZoologia, Universidade
The study ofthe functional anatomy was conducted at de Sao Paulo (MZ USP) under the registration number
the University ofBrasilia where the animals were kept 32061.
alive in an aquarium with artificial seawater. Ciliary currents were studied by the application ofa
Around 50 living and preserved specimens specimens suspension ofCarborundum (F3), carmine and Aqua-
ofall sizes were analyzed. Identification ofthe material dag solutions. To help the observation ofthe different
was based on Clench & Turner (1946) and Turner organs, whole animals were stained with Paracarmin
(1966, 1971). Identification was confirmed by the late and later cleared (Bucherl, 1943).
Dr. Ruth D. Turner, Harvard University, USA. A lot Some of the anatomical details analyzed were also
of 15 complete specimens (shell, pallets and soft parts) obtained by transverse sections 6-8 urn thick, of
M. J. Martins-Silva & W. Narchi, 2007 Page 311
bu m's dd, *pc a
go
i
0,5 cm
Figure2. Bankiafimbriatula. Generaltopographyoftheorgans afterremoval ofthevalveandthemantle fromtheleft sideofthe
body. Abbreviations: a, appendix; aa, anterior adductormuscle; ac, anteriorctenidium; an, anus; as, anterior stomach; au, auricle;
bu, bulblike swelling; ch, cephalic hood; dh, dorsal hood; ddj, dd2, digestive diverticles; ec, epibranchial cavity; ebv, efferent
branchialduct; ex, exhalant siphon; f, foot; go, gonad; i, intestine; in, inhalant siphon; k, kidney; m, mantle; ms, meddian stomach;
p, pallet; pa, posterior adductor muscle; pc, posterior ctenidium; spc, semi-spiral conical projection; vc, ventricle.
animals fixed in Bouin's fluid and stained with fusticula (Jeffreys, 1860). In B. fimbriatula the differ-
Mallory's Triple Stain or Ehrlichs's haematoxylin and ences are only distinct in histological sections.
eosin, according to the method described by Pantin Males and females havemilky white gonads, situated
(1948). at the region immediately posterior to the distal part of
the digestive diverticula.
RESULTS Contrary to what Turner (1966) states for B. gou/c/i,
Bsetacea, B. campanellata and B. australis, the heart of
General disposition oforgans in the mantle cavity B. fimbriatula has two intensely dark brown pigmen-
tated atria. The ventricle is whitish in color and from it
The disposition of the major organs in the mantle arises a well-developed aorta located on the dorsal
cavity ofB. fimbriatula is shown in Figure 2. surface ofthe gonads.
The visceral mass occupies about 60% of the body The kidney is dorsal to the aorta, extending from the
length and the posterior ctenidia and siphons occupy posterior part of the posterior adductor muscle to the
the remainder. distal extremity of the pericardial cavity. The nephro-
The stomach has tworegions; the appendix orwood- stome opens into the interior of the pericardial cavity
storing caecum is well developed and in the live animal and the nephridiopores into the epibranchial cavity,
iseasily distinguished from theother structures because both at the same level of the body. The afferent
ofits reddish color due to particles inside it. excretory duct shows, just behind the nephrostome, a
The digestive diverticula are oftwo types as defined globular dilatation whose internal wall is deeply folded
by Potts (1923) and Morton (1970) for Teredo navalis and ciliated. The two nephridiopores are placed near
(Linnaeus, 1758): the normal type and the specialized each other, being smaller than, and situated posteriorly
type. In live specimens of B. fimbriatula there is no to, the gonopores.
difference between the digestive diverticula in contrast The anal canal lies in the dorsal region ofthe visceral
to what Lopes & Narchi (1998) described for Nausitora mass and extends from the anus to the posterior end of
Page 312 The Veliger, Vol. 50, No. 4
the gonads, connecting to the epibranchial cavity opening whereas the margin is smooth and lacks
through a narrow opening. digitiform projections. The exhalant siphon stretches
and moves more actively than the inhalant, the latter
stayed in the same position for a long period, moving
Shell
only when disturbed or in order to quickly close the
The descriptive terminology of the shell is based on opening by flexing the digitiform projections. This
Turner 1966). Less than halftheexternal surface ofthe movement apparently occurredwithout tactile stimulus
(
shell of B. fimbriatula (Figure 3) is occupied by the and was not regular.
anterior slope. The dorsal region possesses denticulate The cilia on the siphons (Figure 7) occur mainly on
ridges that are eroded by friction against wood; the digitiform projections and the epithelium at the
laterally these ridges are more developed. The umbo- inhalant and the extremity ofthe exhalant siphons and
nal-ventral sulcus is narrow and flat. The dorsal and produce a weak rejecting current that transports small
ventral condyles are obvious, but the umbonal-ventral particles outwards. Thus, these cilia contribute to
ridge is poorly defined. The apophysis is flat when cleaning the tentacle surface, impeding the settling of
viewed transversely, with a sharp extremity near the small particles.
ventral condyle. The posterior adductor muscle scar is Bankia fimbriatula eliminates fecal pellets and
only weakly evident. pseudofeces via small jets. The exhalant and inhalant
siphons, respectively, eject them a short distance away
from the opening in the wood, where generally they
Pallets
accumulate. In the aquarium, large quantities of this
Thepallets ofB.fimbriatula(Figure 4) possess a long waste accumulate, requiring weekly removal.
stalk, ofthe same length as or shorter than the blade.
The pallets areelongateandthe bladesarecomposedof Musculature of the pallets and siphons
numerous cone-like elements on a central stalk; these
elements are separated and easily removed from the The musculature involved in moving the pallets and
stalk, particularly in dried specimens. The cones have a siphons (Figure 8) was described by Turner (1966) for
calcareous base covered with periostracum, which Bankia gouldi and B. setacea. In B. fimbriatula, the
extends as a border. The width and the ornamentation musculature is similar to that ofB. gouldi and includes
ofthe periostracal border vary greatly; the border may the protractors, anterior retractors, median and poste-
be smooth, coarsely to finely serrate, or produced rior retractors and adductor muscles. These muscles
laterally as awns. unique to the Teredinidae are fixed to the proximal
Variations in the form of the blade could not be third part ofthe pallet stalk.
related to the age of the animals or to environmental The protactor muscle (pmp) of each pallet is
conditions. As all specimens came from the same composed of two well-developed bundles, easily seen
population and similarecological conditionsthiscan be externally as an open fan shape, with the narrower part
interpreted as individual variation, as Lopes & Narchi directed to the anterior region of the animal. The
(1998) observed for Nausitorafusticula. muscle itselfis fixed to the stalk and to the calcareous
part ofthe gallery wall.
Siphons The anterior retractor muscle (armp) of pallet is
formed bytwo muscularbundles, thethicker"internal"
As described for N. fusticula the inhalant and and the thinner '"external." The internal is fixed to the
exhalant siphons (Figure 5) are joined for almost half internal face ofthe stalk and the external is fixed to the
of their length (Lopes & Narchi, 1998). Most of the external face ofthe stalk.
specimens have white siphons with small spots of The posteriorretractormuscle(prmp) isslimwithlittle
reddish brown pigmentation from the region of branching. The posteriorretractormuscleendsinside the
separation of the siphons to the aperture. This mantle and is not attached to any hard structure.
pigmentation is more abundant on the ventral sides The adductor muscle of the pallets (amp), the
of the inhalant siphon and on the dorsal side of the extremities of which are fixed to the internal face of
exhalant. the stalk, bring together the two pallets.
The inhalant siphon (Figure 6) is fringed with a row In the body region where the musculature of the
of eight digitiform tentacles, between which the pallets occurs, it is possible to observe two well
epithelium forms simple projections. When the animal developed cylindrical muscular bundles ofthe retractor
is pumping water, the siphons project through the muscles ofthe siphon (rms).
wood, and the digitiform tentacles are kept almost When the animal is pumping water, the pallets
perpendicular to the axis ofthe siphons. remain inside the gallery. Any disturbance in the
The exhalant siphon possesses a relatively narrow environment causes retraction of the siphons. At this
M. J. Martins-Silva & W. Narchi, 2007 Page 313
mm
2
aur
B
Figure3. Bankiafimbriatula. Rightvalveoftheshell. A. Externalview. B. Internalview. Abbreviations: ap,apophysis;as,anterior
slope; aur, auricle; c, chondrophore; d, disc;dc,dorsal condyle; ps, posteriorslope; vc, ventralcondyle;vu, ventral umbonal sulcus.
Page 314 The Veliger, Vol. 50, No. 4
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Figure4. Barikiafimbriatula. Variations in the pallet. A. Pallet withcompletepeduncle. B. External viewofthe pallet. C. Internal
view ofthe pallet. Abbreviations: aw, awns; bl, blade; co, cone; sk, stalk.
time, the pallets are pushed into the opening of the Lopes & Narchi (1998) in N. fusticula, are not present
gallery by contraction ofthe pallet protractor muscles. in B. fimbriatula.
When the disturbanceceases, the pallets retract and the In the hypobranchial cavity at each side ofthe body,
siphons extend out to the exterior. Pallet retraction is the internal epithelium of the mantle has a tract with
executed by retractor muscles at the same time that the well-developed cilia that extends from the anterior
adductors contract, thus moving the pallets' blades regiontothebaseoftheinhalant siphon. Intheanterior
apart, allowing for passage ofthe siphons. During this and median regions ofthe body, thesetracts arelateral.
process, the protractor muscle of the pallet and the Atthebeginningoftheposteriorctenidiatheyapproach
retractors ofthe siphons remain relaxed. one another, meeting and becoming ventral.
The mantle in the epibranchial cavity dorsal to the
Mantle posterior ctenidia, near the siphons, has internally a
thick zone of mucus cells, as also described by Nair
The structure ofthe mantle is similar throughout the (1957) and Saraswathy & Nair (1971) for B. carinata.
family (Turner, 1966). In B. fimbriatula the mantle is
thin and transparent in the anterior third ofthe body. Labial palps
At the median third it is a little thicker, while at the
posterior third, it is very thick. The tissue ofthe mantle The labial palps of B. fimbriatula (Figure 9) are
is filled with a whitish substance. Groups of round attached to the epithelium ofthevisceral mass (Turner,
granules of a reddish-brown color, as described by 1966). They are inconspicuous, the external and the
M. J. Martins-Silva & W. Narchi, 2007 Page 315
Figure 5. Bankiafimbriatula. Siphons and pallets as observed in living animal removed from the wood. Abbreviations: fp, fecal
pellet; in, inhalant siphon; ex. exhalant siphon; p. pallet. The arrows show the direction ofthe inhalant and exhalant currents.
internal ones occupying, respectively, dorsal and a groove. Identification ofthe palpswaspossible only for
ventral positions. The dorsal palp is reduced to two flat some specimens.
folds. The ventral palp is reduced to a small, long and The ciliary currents were observed only in a few
narrow elevation extending from the ventral border of specimens. Ciliaryactivitywasslight and movements of
the mouth to the anterior extremity of the marginal the particles near the mouth were not detected.
Page 316 The Veliger, Vol. 50, No. 4
A
MM' 3
h 3
B
Figure 6. Bankiaftmbriatula. Detail oftheaperture ofthe inhalant siphon with eight digitiform tentacles. A. Siphon opened with
extended tentacles. B. Siphon showing tentacles bending across the aperture.
Ctenidia in live ones removed from wood. The posterior part of
the body is more affected by this contraction and the
The terminology adopted for the description of the ctenidia become shorter and folded. The posterior
ctenidia ofB.ftmbriatulais the same used by Ridewood ctenidia ofB.fimbriatula are similar to those described
(1903); Atkins (1937); Purchon (1939) and Lopes & by Lopes & Narchi (1998) for N. fusticula.
Narchi (1998). The posterior ctenidia are represented only by the
The anterior ctenidia have from eight to nine external demibranch [Purchon (1939, 1941) and Lopes
filaments that correspond to those of the external & Narchi (1998)].
lamella ofthe demibranch (Figure 10). Each filament is The demibranchs of B. fimbriatula are eulamelli-
reduced to a simple bar,joined throughout its length to branch and homorhabdic. Each demibranch has a V-
the epithelium of the visceral mass. The first and the shaped form; the apex possesses a marginal groove
last filaments are really semi-filaments because there is 95 urn deep.
complete ciliation on only one of the lateral faces, as Each filament of the posterior ctenidia measures
Sigerfoos (1908) described for B. gouldi. 40.8 um in width alongpractically itsentirelength. The
Depending on the condition ofthe bodycontraction, free extremity is slightly dilated. Each filament
the ctenidium may become strongly folded, simulating (Figures 12, 13) has two bands of frontal cilia (fc)
a plait (Figure 11). The body of B. fimbriatula can laterally disposed, each of which measures around
contract to halfits length in preserved animals or even 6.8 um in length, bordered by two rows of lateral-
M. J. Martins-Silva & W. Narchi, 2007 Page 317
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Figure 7. Bankiafimbriatula. Rim ofthe inhalant siphon showing one digitiform tentacle and one simple projection occurring
between two tentacles. Abbreviations: c, cilia; tc, cilia tufts.
frontal cilia (lfc) of around 50 |J.m in length; laterally, by their respective ctenidial axes, separate at the
between the base ofthe filament and the lateral-frontal posterior region of the visceral mass. The filaments
cilia, thereare lateralcilia (lc) around 23.8 urnin length become progressively smaller until they are reduced to
forming on each face a strip about 20.4 urn in width. the marginal groove. This groove is situated laterally
The frontal cilia of the lateral regions of the free on the visceral mass it extends to the anterior ctenidia,
extremity of the filaments are the same length and and is bordered by ciliated cells.
cover the top ofthe filaments. In this region, there are In the anterior and median regions of the body the
no large cilia which could be identified as being ctenidiaarereducedtoamarginalgroove.Thequantityof
terminal. The rows of lateral-frontal and frontal cilia material transported inside the marginal groove is
end at the marginal groove base and are of similar generally small. Excess particles are conducted to the
length as the frontal cilia. anterior region where they accumulate, surrounded by
The posterior demibranchs of B. fimbriatula, joined mucus, and formed into large masses, which flow from
Page 318 The Veliger, Vol. 50, No. 4
4 mm
Figure 8. BankiaJimbriatula. Diagrammatic view of the muscles associated to the pallets and siphons. Abbreviations: amp,
adductormuscle ofthe pallet; ex, exhalant siphon; in. inhalant siphon; p, pallet; pc, posteriorctenidia; pmp, protractormuscles of
the pallet; rms, retractor muscle ofthe siphon; rmp, retractor muscle ofthe pallets.
ch
dip
/ Vll
Figure9. BankiaJimbriatula. Frontalviewoftheanteriorextremity. Abbreviations:ch,dorsalhood;dip,dorsallabialpalp;f,foot
sole; mo, mouth; s, shell; vc, ventral condyle; vlp, ventral labial palp.