Reversible Epithelial Adhesion Closes the Mouth of Beroe, a Carnivorous Marine Jelly

11 Pages·1991·4.4 MB·English

by  S L Tamm

Reference: Bio/. Bull. 181:463-473. (December, 1991)
Reversible Epithelial Adhesion Closes the Mouth of
Beroe, a Carnivorous Marine Jelly
SIDNEY L. TAMM* AND SIGNHILD TAMM
Boston UniversityMarine Program, Marine Biological Laboratory,
Woods Hole, Massachusetts 02543
Abstract. We investigated how the ctenophore Beroe, a adhesion in Beroeshares many structural and functional
carnivore of the marine zooplankton, keeps its mouth propertieswith transientadhesionsformed between mov-
shut to maintain astreamlined body shapeduring forward ing cells in embryos and in culture, and may be a useful
swimming in search ofprey. In big-mouthed, thin-walled experimental system for studying the mechanisms and
beroids we found that mouth closure requires neither regulation ofdynamic cell adhesions.
muscular nor nervous activity. Instead, mouth adhesion
is due to paired strips ofadhesive epithelial cells on op- "Loose lips
posing stomodaeal walls. The twojoined epithelial layers Sink ships." WW
make numerouscloseappositions interrupted by vacuolar -U. S. Navy slogan, II
intercellular spaces. At regions ofapposition, the plasma
membranesarehighlyfoldedand interdigitatedwitheach Introduction
other, and are separated by a uniform distance ofabout
15 nm. Adensecytoplasmiccoatunderliesthemembranes Ctenophores are important members ofthe gelatinous
at such appositions. Synapses of neurites are found on marine zooplankton and are significant predators in
the basal ends of the adhesive cells. We found two or- planktonic food chains (Thorson, 1971). Beroid Cteno-
thogonally different orientations of the stomodaeal ad- phoreshavealargemouthandavoluminousstomodaeum
hesive strips in B. sp. vs. B.forskali, correlated with dif- occupying most ofthebody, and are voracious predators
ferent distributions offeeding macrocilia inside the sto- of other Ctenophores (Swanberg, 1974; Harbison et ai,
modaeum. 1978). Beroeactivelyseekspreybyswimming mouth for-
Mouth opening in response to food requires muscular ward, powered bythebeatingofgiantciliarycombplates.
contractionsofthelips. However,thestomodaealadhesive Yet the mouth remains closed, with the body shape
stripsare not pulled apart all at once, but arepeeledapart streamlined, until prey is encountered. Then the mouth
starting from a site of vigorous muscular tension. The opens rapidly and the stomodaeum expands to suck in
mouth re-sealsafter feeding, orafter beingexperimentally the prey (Horridge, 1965a; Tamm, 1982). Alternatively,
pulled open, showing that tissue adhesion is functionally the lips may spread overthe prey, usingthe saber-shaped
reversible. macrocilia liningthestomodaeum tobiteoffpieces(Hor-
Epithelial adhesion in Beroe appears to be a useful ridge, 1965a; Swanberg, 1974; Tamm, 1983).
method forclosingthe mouth and streamlining the body We haveinvestigated the mechanism wherebya swim-
of a gelatinous predator that spends most of its time ming Beroe keeps its mouth shut. We have found that
swimming mouth-forward in search ofprey. Opening of mouth closure in certain beroids is due to a functionally
the mouth appears to be an efficient process as well, be- reversible type ofadhesion between paired strips ofepi-
causepeelingapartoftheadhesivestripsrequiresasmaller thelial cells on the stomodaeal walls. Muscular activity is
applied forcethan doesseparatingthem all atonce. Tissue not required to keep the mouth shut, but is necessary to
open the mouth in response to food. The adhesive seal is
Received 31 July 1991; accepted 24 September 1991. not separated all at once, but is peeled apart starting at a
*Towhom correspondenceshould beaddressed. site of muscular tension. The mouth ofBeroe may be a
463
464 S. L. TAMM AND S. TAMM
Figure 1. Bernemilrata swimming mouth forward (to the left) with the lipsclosed intoa widecurved
slit. The body is flattened in the stomodaeal plane with a blunt front end and tapering rear. Longitudinal
rowsofciliaryswimmingplates(cr.combrows)extendfromtheaboralendtowardthemouth. Photograph
kindlyprovided by Dr. ClaudeCarre, Station Zoologique, Villefranche-sur-Mer, France. Natural size.
useful model forstudyingthe mechanisms and control of Tracings ofselected video fields were made on matte ac-
reversible tissue adhesions, as well as the biomechanics etate directly from a video monitor.
offeeding behavior in soft-bodied marine animals. Differential interference contrast (DIC) images ofliving
stomodaeal adhesive strips were made with Zeiss 16X or
Materials and Methods 40X objectives and recorded with an Olympus OM-2N
camera on Kodak Tech Pan film by electronic flash.
Animals
Beroesp. wascollected at Woods Hole, Massachusetts, Electron microscopy
in fall, 1990. This unidentified species is similar to B. sp.
collected at Woods Hole in fall, 1985, after Hurricane Closed mouths ofB. sp. and B. forskali were fixed as
Gloria(Tamm and Tamm, 1988). The comb rowsofthis follows. The animals were first relaxed in MgCl:-seawater.
beroid run on high ridges that project from the flattened Simultaneous glutaraldehyde-paraformaldehyde-osmium
fixation was then performed and tissue was processed for
body surface.
B.forskali was collected at Monterey Bay, California, electron microscopy as described previously (Tamm and
by Freya Sommer of Monterey Bay Aquarium, and Tamm, 1985).
shipped to the Marine Biological Laboratory in Woods
Hole. Results
Observations on living material Beroid ctenophores have a conical body flattened in
the stomodaeal plane to varying degrees in different spe-
An isotonic MgCl2-seawater mixture (6.75% MgCK: cies. Beroe:swims mouth forward at speedsofseveral cm/
seawater =1:1) was used to block nervous and muscular sorfasterwhen seekingprey. In flattenedthin-walledspe-
responses in whole animals or in dissected preparations. cies such as B. sp., B. forskali, and B. mitrala, the front
Experimental observations on the stomodaeal adhesive end is wide and blunt with the lips closed into a long
strips of B. sp. or B. forskali were made under a Wild curved slit, and the body tapers towards the rear (Fig. 1).
dissecting microscope and recorded with a Panasonic This streamlined body shape depends on the mouth re-
CCD video camera and GYYR model 2051 video re- maining closed during forward swimming.
corderallowingstill-field playback and analysis. Still-fields We examined how beroids with flattened streamlined
were photographed from a Sony video monitor with an bodies and thin flexible body walls (/.t'.t B. sp. and B.
Olympus OM-2N camera on Kodak Tech Pan film. forskali) keep their mouth shut while swimming. B. sp.
Mouth opening responses ofwhole animals pinned to and B.forskalidifferdramatically from each other in the
Sylgard were induced by a suspension offresh egg white size and arrangement oftheir feeding macrocilia; as we
in seawater(A. Maselli, pers. comm). Responses were re- will show, this difference in macrociliary patterns is cor-
corded with a Nikon macrolens on a Panasonic CCD related with orthogonally different orientations ofmouth
video camera using the procedures described above. closure.
MOUTH CLOSURE IN BEROE 465
Figure 2. Zoneofadhesion between Mg-rela\edlipsegmentsofBtvwsp. underimposedtension(large
arrows). A,B. The paired lip segments(left and right) arejoined symmetrically alonga zone (arrowheads)
ofstretched stomodaeal walls (w). The lip edges and furrowed macrociliary fields (M) are at the top; the
stomodaeum(s)isdown.Notethattheattachmentzoneislocatedashortdistanceaboraltothemacrociliary
fields. B, Continued tension narrows the adhesivecontact between the stretched lipsurfaces(arrowheads).
Ashorttimelaterthelipssnapped apart. C, Face viewofthe adhesion zonebetween stretched, separating
stomodaealwalls(w)bydarkfieldmicroscopy.Theadhesivecontactrunsmedially(arrowheads)andscatters
morelight than thestretched surfaces. Scale bar: A,B. 165 j/m;C, 110nm.
First pattern ofmouth adhesion: B. sp. ifthey were stuck shut. Afterbeing forcibly opened, how-
ever, the stomodaeal walls and mouth of MgCl -anaes-
:
Treatment ofB. sp. with excess MgCl: abolishes con- thetizedanimalsgraduallyclose,andthelipsre-seal within
traction ofthebodywall musclesandblocksneurally me- 10-15 min. Similar observations were made on dissected
diatedciliaryresponses(i.e.. ciliaryinhibition). Mg-relaxed oral ends. These findings show that mouth closure is
animals swim forward continuously with their mouth functionally reversible and requires neither muscular nor
closed. The lips resist being pulled apart with forceps, as nervous activity to maintain or re-establish adhesion.
466 S. L. TAMM AND S. TAMM
Figure 3. DIG view ofthe surfaceofa peeled apart lipofBeroi-sp. in MgCI:/seawater. The lipedge is
to the left; the aboral direction is to the right. The adhesive strip (bracket) runs parallel to, and a short
distance aboral to. the macrociliary field (M). The surface ofthe adhesive zone iscovered with numerous
small vesiclesorcraters. Suhepithelial transverse muscle fibers(tm) run verticallyand appearout-of-focus.
The finer and moreclosely spaced longitudinal muscles (1m, cf. Fig. 5) run horizontally and are visible in
theareabetween theadhesive stripand the macrocilia. Scalebar, 30^m.
The adhesive region in the mouth was located by ex- By DIG light microscopy the surface of mechanically
amining segments ofadherent lips excised from Mg-re- peeled apart lips displays a well-defined tract ofdensely
laxed animals. We found that lip segments are fastened packed vesicles or vacuoles, that coincides with the lo-
togetheralonga narrow zone oftheapposingstomodaeal cation of the adhesive strips (Fig. 3). These vesicles or
walls(Fig. 2). The belt oftissue adhesion runsaround the vacuolesare2-1 ^m indiameter, andappeartobemod-
inside ofthe mouth, a short distance aboral to the band ifications ofthe apical surfaces ofstomodaeal epithelial
of macrocilia encircling the lip edge (Fig. 2). Therefore, cells. The tract is 200-300 ^m wide and runs about 150
mouth closure is not due to Velcro-like attachment of ^m aboral to the band of macrocilia. The stomodaeal
macrociliaonapposinglips, apossibilitythat initiallyhad surface on either side of the adhesive tract is relatively
seemed likely to us. smooth and featureless.
We
next investigated the adhesive properties ofclosed Toluidine blue-stained thick sections through fixed,
lips. Adherent lip segments were pulled apart by forceps, closed mouths show that the stomodaeal epithelium is
starting at one end of the joined pair. Tension initially markedly thicker in the adhesive strips, due to the in-
stretches thejoined stomodaeal walls without separating creased height ofcellsin this region (Fig. 4). Even by light
the adhesive zone (Fig. 2A). Increased tension further microscopy, it is evident that the two epithelial layers
drawsoutthetwoattachedsurfaces, which appearasmir- make numerousclosecontacts, interrupted by many vac-
ror images ofeach other (Fig. 2B,C). Then the adhesive uolar intercellular spaces (Fig. 4B).
stripson eitherside separate at the site ofgreatest tension Correspondingelectron micrographsthrough adherent
and thelipspeelapart. Thisisfollowed byelastic recovery epithelial stripsshow thatapposed cell surfacesare folded
and flattening ofthe stretched stomodaeal walls. and interdigitated with each other (Figs. 5, 6). In such
Darkfield microscopy ofjoined, stretched lips under appositions, the two plasma membranesconform toeach
tension showsthatthezone ofstomodaeal contact scatters other and run parallel, separated by a uniform space of
more light, and thus appears brighter than the adjacent about 15 nm (Fig. 6). The intercellular space frequently
walls(Fig. 2C). Theincreased lightscatteringiscorrelated contains dense amorphous material, but there is no ob-
with the greatly elaborated surface area of the adhesive vious structural continuity between the apposed cell sur-
cells (see below). faces (Fig. 6). The cytoplasmic sides of the membranes
MOUTH CLOSURE IN BEROE 467
Synapses ofneurites are also found on the basal ends
oftheadhesive cells, indicatingthat some function ofthe
adhesive cells must be under nervous control. The pos-
sibility that cell-cell appositions may be neurally regulated
is discussed below.
The stomodaeal adhesive stripsalsocontain cellsbear-
ing actin pegs and onion-root cilia. Such cells are found
in the epidermis ofmany ctenophores (Horridge, 1965b;
Hernandez-Nicaise, 1974;Tamm andTamm, 1991), and
arethought to function aschemo-and mechanoreceptors
(seeTamm andTamm, 1991). In closed mouths, theactin
pegs project into the vacuolarintercellular spacesbetween
apposed epithelial layers. Thecellsbearingactin pegsand
onion-root cilia synapse directly onto underlying longi-
tudinal muscle fibers, suggesting a pathway for sensory
control of stomodaeal muscles in response to food (see
also below).
Glandular cells are abundant throughout the stomo-
daeal epithelium, including the adhesive strips. Large
membrane-bound secretorydropletsarepacked intooval
groups, many ofwhich are larger than the cell nucleus.
B The secretory granules contain finely granular material,
or coalesce and appear electron-lucent with coarse dense
Figure4. Toluidineblue-stained longitudinal thicksections(0.5^m) deposits and fibrils. These gland cells are similar to the
through a closed mouth ofBeroesp. A, Survey view, lip edges at left.
Thestomodaealwallsarejoinedtogetherbypairedstrips(herecuttrans- spumousgland cellsdescribed intheepidermisofvarious
versely) ofthickened epitheha (arrowheads) located aboral to the ma- ctenophores by Hernandez-Nicaise and colleagues (Her-
crociliaryfields(M). S. Stomodaeum. B, Highermagnification ofthick- nandez-Nicaise, 1991).
enedjoinedepithelialstrips. Apposingcellsurfacesmake numerousclose The adherent epithelial layersare structurally identical
contactsinterruptedbyvacuolarspaces.Scalebar.A, lOO^m;B, 17^m. and have a mirror-image symmetry about the plane of
apposition. This suggests that each epithelial strip ofthe
pair makes an equal contribution to adhesion, and that
are coated with dense material and wispy filaments that both surfaces are necessary for adhesion. In fact, the ep-
runparalleltothemembrane. Thesecloseappositionsare ithelial strip ofan excised lip segment will adhere to an
found almost exclusively between plasma membranes of unmodified region ofthe stomodeal wall, but such het-
adhesive cells, being rare or absent between cells within erophilic attachments are weaker than adhesion between
either epithelial layer. two lips.
The regions ofclose apposition alternate with widely
separated, vacuolarspacesbetween theepithelial surfaces Mouth opening
(Fig. 5). The plasma membranes in the widely spaced re-
gions do not bear dense cytoplasmic coats, and so are We investigated how Beroe separates its stomodaeal
readilydistinguishable from closely apposed membranes. adhesive strips to open its mouth so widely and rapidly
The widely spaced regions seen in sections may corre- uponcontactwith food. Eggwhitepipettedontotheclosed
spond to the edges or rims ofthe round vesicles or vac- mouth ofa Beroepinned in seawater first triggersa series
uoles, seenby DIGonthesurfacesofadhesivestripspulled ofbrief, local muscular contractions ofthe lips perpen-
apart by forceps (Fig. 3). diculartotheadhesiveseal. Thesemusculartwitchesoccur
Numerousthin musclefibersrunparalleltooneanother at various locations alongthe mouth edge, until one con-
between the basal ends ofthe adhesive cells next to the traction pulls apart the adhesive strips at that site (Fig.
mesoglea(Fig. 5).Thesemusclesextendinthelongitudinal 7A, B). The stripsthen rapidly peel apart from this point
direction ofthe body for long distances under the entire by coordinated muscular activity of the lips, leading to
stomodaeal epithelium, and are not restricted to the ad- openingoftheentiremouth(Fig. 7C-E).Withoutrepeated
hesive strips. Neuromuscularjunctions are common and stimulation, the mouth slowly relaxes and closes. Similar
show the characteristic presynaptic triad structure of responses to egg white were observed in dissected oral
ctenophore synapses described by Hernandez-Nicaise ends. MgCli-relaxed animals cannot open their mouths
(1973). due to inhibition ofmuscular and nervous activity.
468 S. L. TAMM AND S. TAMM
V'' K
!m
Figure 5. Survey electron micrograph ofadherent epithelial layers in aclosed mouth ot Bcnicsp. The
zone ofadhesion runs diagonally from lower left to upper right (arrows), and consists ofnumerous close
appositions ofthe cell surfaces alternating with vacuolar intercellular spaces (s). The plasma membranes
have a cytoplasmic coat and appear darker at the contact regions (see Fig. 6). Thin longitudinal muscle
fibers(1m)abuttingthe mesoglea arecuttransversely. X9300.
MOUTH CLOSURE IN BEROE 469
Usingtransversesegmentsofthe body ofMgCN-relaxed
B.forskali, we found that the flattened stomodaeal walls
arejoinedby paired macrocilium-free ridgesthat run lon-
gitudinally down the midline ofthe stomodaeum, effec-
tively dividing the stomodaeal cavity into two lateral
pockets (Fig. 9). These adhesive strips begin near the lip
edge and extend 2/3-V4the length ofthe stomodaeal cavity
(Figs. 8, 10).
Pulling the flattened sides of the stomodaeum apart
with forceps shows that the paired longitudinal ridges of
B. forskalipossess adhesive and tensile properties similar
to those of the circumoral adhesive strips of B. sp. In
addition, light and electron microscopy reveals no mor-
phological differences between the adhesive strips of B.
forskali vs. B. sp. We have not yet made observations on
how B. forskali or B. mitrata open their mouths to feed.
In B. mitrata, the macrociliary field covers the entire
oral half of the stomodaeal cavity, except for two bare
zones that extend longitudinally and medially through
the macrociliary fields on eitherwall ofthe stomodaeum.
Although we have no data at present to show that these
macrocilium-free zones are adhesive and keep the wide
mouth closed, their location suggests that they do so in a
manner similar to the longitudinal adhesive strips of B.
forskali.
Discussion
Our curiosity about how a swimming Beroe keeps its
mouth shut led tothediscoveryofa novel, reversibletype
oftissueadhesion. We foundthat the stomodaeum is fas-
tened together by a matched pair of apposed epithelial
strips. The remarkable, and obviously necessary feature
ofthistissue adhesion isits functional reversibility: tissue
bonding is rapidly broken when Beroe opens its mouth
to ingest prey, and is readily reformed after feeding.
B
Mechanism ofadhesion
Figure6. Appositionsofplasmamembranesofadherentstomodaeal Thereversibleappositionsofstomodaealadhesivecells
epithelialcellsinaclosedmouthofBcnwsp.Althoughfolded,theapposed in Beroe are similar in several respects to the transient
plasma membranes run parallel to each other and are separated by a adhesions formed between moving cells in embryos and
distance ofabout 15 mm. Note floculent material in the intercellular inculture(Trinkaus, 1984). In bothcases, apposed plasma
tsepraicael..AT.heXc1y0t8o,p4l0a0;smBi,cXs9id3e,4o0f0t.hemembranesiscoatedwithdensema- membranes typically (1) are highly folded and interdigi-
tated, (2) conform to each other and run parallel over
broad areas, (3) are separated by a distance of 10-20 nm,
Secondpattern ofmonth adhesion: B. forskali and (4) show no obvious structural continuity between
B.forskali and B. mitnita differ from other beroids in them. These features are in marked contrast to the stan-
that they possess considerably larger macrocilia; more dard typesofstructurally differentiated localizedcontacts
importantly for this study, their macrocilia are not re- foundbetween cells, suchastightjunctions, gapjunctions,
stricted to a band around the inside ofthe lips, but cover desmosomes, etc.
a large area ofthe stomodaeal cavity. In B. forskali, the Becausetheapposedcell membranesofBeroeadhesive
macrociliary field comprises longitudinal stripes that ex- cells and moving cells in embryos and culture are not
tend almost half the length of the stomodaeum (Figs. structurally bound to one another, "bonds between the
8, 10). cell surfaces in such appositions would be more readily
470 S. L. TAMM AND S. TAMM
A
Figure8. Surfaceattheoralendofoneofthetwostomodaealwalls
ofB. forska/i(darkheld). Thecurved lipedge isatthe topofthe figure.
Macrocilia appear brighterand extend downward from the lip edge as
tapering longitudinal stripes(s). The adhesive strip runs longitudinally
along the midline ofthe stomodaeal wall (arrowheads). Scale bar. 2.3
mm.
made and broken and remade again than in junctions"
(Trinkaus, 1984, p 171). These cell-cell appositions in fi-
broblasts are believed to be "a prime candidate for the
kind of adhesion that moving cells require" (Trinkaus,
1984, p 171). Similarly, suchappositionswouldseemwell-
designed forthe reversibletypeoftissueadhesion required
to seal Berne's mouth.
The physical or chemical mechanisms ofsuch cell-cell
adhesions are not well understood in any system (Trin-
kaus, 1984). Suggested mechanisms range from non-spe-
cific molecularattraction, such as London-van derWaals
forces (Nachtigall, 1974; Trinkaus, 1984), to chemical
bonding by molecular "glues" or specific cell adhesion
molecules (Takeichi, 1990, 1991; Edelman and Crossin,
1991).
Month opening andpossible regulation oftissue
adhesion
Usingegg-white asa feedingstimulusto induce mouth
opening, we found that the mouth does not open all at
once, as assumed previously (Tamm, 1982), but ispeeled
apart starting at a site of vigorous muscular tension on
Figure7. MouthopeningofBernesp.inducedbyeggwhite(viewed
orally). A. Local musculartwitchespull the left sidesofboth lipsaway
fromtheadhesionzone(lineinsidethelips).B.Musculartensionseparates
theadhesivezone(arrow)andpullsopen the lipson theleftsideofthe
mouth. C, Continued muscular activity peels apart the adhesive seal
from left to right (2 slater). D, Peelingapart ofthe adhesion zoneand
openingofthe mouth hasalmost reached the right side(3.5 s later). E,
Themouthisfullyopenandgaping(6.5slater).3Xnaturalsize.Tracings
ofvideofields from monitor.
MOUTH CLOSURE IN BEROE 471
Figure9. Stomodaeal wallsofBeroeforskaliareattachedbypairedlongitudinaladhesivestrips. A,The
stomodaeal cavity ofa transversely cut body segment is viewed alongthe oral-aboral axis from insidethe
animal. The stomodaeal wallson the left side have been cut and pulled apart (white arrows) to show the
adhesive strips (s) running longitudinally on each wall. The strips are still joined like a spot weld at the
arrowhead. The right sideofthe stomodaeum remainsclosed. B, Frontal viewofadissected mouth being
pulledopenwith forceps.Themiddleofthemouth remainsfastenedbythelongitudinaladhesivestripsthat
dividethestomodaeal cavity intotwo lateral pockets. Scalebar: 1 mm.
the lips. Because peeling apart of two adherent surfaces Mouth opening may also require concomitant
requiresamuch smallerforce, applied overalongertime, changes in the adhesive properties oftheepithelial cells
thanpullingthemapartallatonce(Steinberg, 1964;Vogel, themselves. The presence of synaptic contacts on the
1988), this method islikelytoreduce theamount ofmus- adhesive cells suggests that these cells make some kind
culartension required toseparatethestomodaeal adhesive ofneuronallytriggered effectorresponse. Such responses
strips ofBeroe. may involve changes in thecortical cytoskeleton orcell
TAMM AND TAMM
472 S. L. S.
patterns are believed to reflect differences in feeding be-
haviorandpreytype (Tamm and Tamm, 1990). In B. sp.
and most other species, macrocilia are relatively small
and are restricted to a narrow band around the margin
ofthe lips. The adhesive strips in B. sp. also run around
the lips, just inside the band ofmacrocilia.
Incontrast, B.forskaliandB. mitrata havelargermac-
rocilia that cover a much greater area ofthe stomodaeal
cavity. TheadhesivestripsinB.forskalirun longitudinally
alongthemidlineofthestomodaeum, betweenthestripes
ofmacrocilia. The mutually perpendicularorientation of
stomodaeal adhesive strips in B sp. and B. forskali is
probably due to the different arrangements ofmacrocilia
in the two species, because adhesion between the sto-
modaeal walls seems to require macrocilium-free zones
ofcontact. We therefore predict that the paired macro-
cilium-free zonesthat run longitudinally through thewide
macrociliary fields ofB. mitrata are also adhesive strips.
A B
Figure 10. Diagram ofmutually perpendicular orientations ofsto- Mouth closure in other beroids
modaeal adhesive strips(as. black bars) in Bcroesp. (A) vs. B forskali
(B). The insideofonewall ofthe flattened stomodaeum isshown. Ma- Doall beroids useepithelial adhesive stripstokeeptheir
crociliary fields are indicated by stipple. The number oflongitudinal mouths closed? Our preliminary observations on B. cu-
macrociliary stripes in B forskali (B)is reduced forclarity (see Fig. 8), cumis from Monterey Bay, California, suggest that this is
aOrnadltehendrselaftaicveedwoiwdtnh.oftheadhesivestripsinbothanimalsisexaggerated. not the case. B. cncwnis differs from B. sp., B. forskali,
and B. mitrata in several respects: it is not appreciably
compressed in the tentacular plane, but is round or oval
surface that modify the adhesive properties ofthe epi- in cross-section. Moreover, the body wall is markedly
thelial strips. thickerand firmer, andthe mouthisconsiderably smaller
Ifso, mouth opening may require cellularde-adhesion than those ofthe species described in this report. B. cu-
processes aswell as muscular activity. How might thisbe citmis swims with its mouth closed or slightly ajar, but
controlled? Mouth openingistriggered bycontactofprey we have found by direct observation and dissection of
withsensory receptorsonthelips. The presumedreceptor living animals that neither the lips nor the stomodaeal
cells bear actin pegs and onion-root cilia, and make syn- walls are fastened together in any manner.
aptic contactsonto neuritesofthe nerve net(Hernandez- Evidently, the small oral opening and the relatively
Nicaise, 1974; Tamm and Tamm, 1991). Ifthis pathway thick, rigid body wall ofB. cucumis provide sufficient re-
isconnected to musclesactingon thelipsandalsotocells sistance to maintain normal body shape during forward
ofthe adhesive strips, then food stimuli could signal both swimming without the necessity ofmouth closure mech-
muscular contractions that pull the lips apart as well as anisms. Other beroids with a similar body plan (i.e.. B.
de-adhesion ofthe epithelial cells themselves. ovata) are likely to use the same strategy.
The gradual closure ofthe mouth after food-induced
or experimentally forced opening does not require mus-
cular activity. The voluminous extracellular matrix, or Significance ofstomodaealadhesion
mesoglea, ofctenophores consists ofa ground substance At the moderate Reynolds number ofaswimming Be-
containing muscle fibers and other cells, as well as a felt- roe. the streamlined body shape should be effective in
like meshwork ofcollagenous microfibrils linked to gly- reducing drag (Vogel, 1981). In thin-walled beroids with
coproteins (Franc, 1985). Passive return of this fibrillar stomodaeal adhesive strips, mouth closure does not re-
matrix to the resting state, following stress-evoked defor- quire muscular or neural activity. Epithelial adhesion
mation, mayberesponsible forrestorationofnormalbody therefore seems to be a useful method for closing the
shape that allows contact and adhesion ofthe epithelial mouth and streamlining the body ofan active gelatinous
strips on the two sides ofthe stomodaeum. predator that spends most ofits time swimming mouth
Patterns ofstomodaeal adhesive strips forward in search ofprey. Beroe also appears to use an
Beroidscan be divided into two main groups based on efficient method toopen itsmouth, because peelingapart
differences in macrociliary size and distribution; these the adhesive strips should require a smaller applied force