University of the Pacific Scholarly Commons
University of the Pacific Theses and Dissertations Graduate School
1969
Structure and function of the alimentary tract of Batillaria zonalis and Cerithidea californica, style-bearing mesogastropods
Andrew Locke Driscoll University of the Pacific
Follow this and additional works at: https://scholarlycommons.pacific.edu/uop_etds
Part of the Biology Commons
Recommended Citation Driscoll, Andrew Locke. (1969). Structure and function of the alimentary tract of Batillaria zonalis and Cerithidea californica, style-bearing mesogastropods. University of the Pacific, Thesis. https://scholarlycommons.pacific.edu/uop_etds/1684
This Thesis is brought to you for free and open access by the Graduate School at Scholarly Commons. It has been accepted for inclusion in University of the Pacific Theses and Dissertations by an authorized administrator of Scholarly Commons. For more information, please contact [email protected]. · SfRUC1'URE AND FUNCTION o:J? THE AIJUIENTAHY ~.'RAOt.e OJ?
~ --
2;------:::------::-:-:-:- ~------STYU~ ... B}iARING 1-I.F~ SOG ASTIWPODS
!------·------;;cc_=--=----==ccc=-
A Thesis Presented to ------Scrte:nces Untverstty of the· Pacj.f1.c
------
------
------
In Ps.rtial Fulfillment of the Requirement:3 for the Dee;ree Master of Science
by AndrevJ J:,ocke D:riseoll June 1969 M----- §
·~~--~------
This thesis, written and submitted by
Andrew Locke Driscoll ------·-· .. -·---~-~--' j-~------" --,-_c__ -c·c~ccc·=-
is approved fo:r:· recommendation to the
Graduate Council.ll University of the Pacifico
------Departm~\t--·0rmi.rma~ OJ:' Dean:
>" ~£11/ ----~---·-~------
------Thes:ts COllU11ittee:
___[D}LJ_j[ __u_, Chaizmn
VV( ~ s;;;;d(d_.~--.-~~- ------_j,O_.~~~-lC.().:DJL_~- T.ABLE OJ? CON TENTS
CHAPTER PAGE h-----=----
1 co I IN1RODUCTION .. ~ • ~ e • • o ~ • ~ e e • • • • • • •
II. M..ETHODS AND HATEHIA.TJS., 0 Cl • • ofJ • ~ 0 • ~ • • • • • 2
III. HABI9~AT. • • • • • • • .. • • • ...... " 6
;~------__c;"'r' "'"---"'"' ~_.,.:o."T"\T~.- o·L_6 ~~"'-----=----c:--c----::-----:- J. V" J.'.lV.lLJ.:'l1.VlJVl:r.l e> e • • o e • • • 0 .. • • • o e • • • • • g------[~~~~~
Buccal Complex. • C> • lit' e • o • .. . • • • e e e • 9
Esophagus .. • • • 0 .. 0 .. • 0 • • 0 • • .17
Stomach end Style Sao • • • 0 • C\ e • o • e • • ..19
Digestive Diverticula .. .. • • .. 0 • • • •
In.t'~ st:i.11n • .. 0 " .. • 0 • • • .35 v .. .. • • • • •
Buec:al Complex. .. • .. .. • • , 0 • ~ • • • •
JtJsophagus • • • • • • e ., 0 • • • • • • . . .. • .39
Stomach ru1d Style Sac .. .. • ~ • e • $ • • • • •
Digestive Diverticula •• ~ e • o • • • • • o &
IntesM.ne • • • ... 0 • • 0 " • 0 • • • •
.VI. ACKrrm·TLEDG:HENTS .. • • It . .. • • • • • • • • BIBLIOGRAPHY • • • • • • • • • • • • • • • • • • ~~-- -~~-~~---~ -~ ~-
t-..l !l-~--~---.- l!.,IGURE PAGE 1. Map of Tomales Bay and Drakes Estero . . . shmving collecting stations -. e e • 0 • • 0 • • • • 5 2. A., Diagram of the alimentary tract of
.____~------;Batillal~La_Z_o:na_l~Ls_._R._nLa~tr_am_o_f.______...~ ==~=== • - .."(><" ... .,.,.~-- -
} • Diagrrunmatic l.ongl tudi:nal se ctio:n of the
buccal region of ].§:.:~t~.?:~ .:'?.• ~mal :i.s shovring the inside of the buccal cavity
a.ncl a por~;ton of the inside of the esophagus .. • .13
lF. Dtagram of' a. cross section through the middle ------;--_----- of the buccal mass of }3atil1aria zonall.s ., • e • 0 15 ~~·~-"""~~""'""'""'- __...... A'-'...__..... ,_
5· Diagram of the stomach of .Jla.t!_~ ~~alis.. • • " .. 21 6.. A cross section of tJ:w style sac and
intestinal groove in ~.la~~ ~on~is •••••• 25
7. D5.agram of the stomach of Ceri t.hj.. de~
californica. • • • • • . . . ~ . . . . • • • • 28 ~-~------~~- . .
8. Cross section of the style sac in C~llh~§5: a
-'cali.fo ______rni _.._.. ca. • • • .. • • • • • • • • • • • • • • • 31 I. INTRODUCTION
-~---
n~~~ "' · 2~he family Potam.idtdae is represented on the California ~-- coast o:f North America by t1;o genera, each represented by a ~ -~------single species~ Batillaria zonalis Bruguiore and Oerithidea - .. - ... -----~""-- --~-- .£ ~if..2£.n~. .£§: Haldeman.. The use o.f the name,· Bat~l}a_&§.J; _?~el~s, is in accordance vri th the conclusions of Hanna (1966).
------."------Refe:r.en.ces in the literature concerning these two species are primar:i.ly taxonomic i'l'i th thl"l exception of bro papers on the gross morphology of ..Qo _s~J:r£.r.~~tc_~ by Br·ight (1958, 1960) .. This study d.escrtbes the structure and funetion of partl.mxla:r· emphasis on the stomach and style sac reg1.on$ Both
-- specles. -vmre fm.:ro.d to be generally simi.lar to other style ;:::: ____- ____- bearing ·mesogastropods in that they have little or no develop'4 ment of glandular tissue in the esophageal reg:l.on and a functfonal style is present in the stomach. The stomachs of both species are specialized to tr1":::nsport and digest a continuous supply of detrltus by means of complex ridges, grooves and ciliary currents. .Q• ca2:-l:£9rEJ._c_~ appears more highly specialized for feeding on fine, highly organic detrital mater1.al tha.Yi B. EOnali:.~ due to slightly more complex stomach morphology. A posi t1.ve correlation is postulated beti'l'een the length of the crystalline style' relative to shell. hetght, and the percentage o.f organic matter in the detritus ingestede II. 1-1E'l'HODS AND MAT:E:RIALfi
Specimens of Batil~. .?_:ri~ zonaJJ.E_ ranging tn length
;::;------:_ .from 25 to 46 mm vrere collected along the shores of Tomales u
Bay (Fig. 1, B.z.) while those of Ce~!_~b.i.~~-~ ~fornic§); (c.c •. ) ranging tn length from 25 to 32 rom were ,_::ollected tn Drakes Estero, Oaliforn:i.a. All 'the collecting statl.ons ·were sampled
;-~---'------~------'-' ~- ~ -~--~-- from 7 to 10 times betvreen March, 1966, and July, 1967. t;--- Specimens used for histological examination vrere removed from their she,lls and relaxed in 1% propylene phenoxytol i.n sea water before being killed and fixed in
Boutn' s fi.xat1ve. Pa.raffln sections, 10 and 12 microns thick, were sta5.ned with Ale tan Blue$ Mayer's Haeroalum and counter··
------stained Hith :foiosln using standard techniques found in Humason =------(1962). Both living and preserved specimens were dissected. Living specimens were dissected :tmmediately after collection and after being starved for 3 to 4 weeks in the laboratory. Ciliary currents were determined with the aid of carmine and graphite particles suspended in sea water. Sediment samples from each collecting station were taken, dried. and weighed. They were then resuspended in
\'later and analyzed by vTet slev~.ng using five sieves ranging
from 1 to .065 rom mesh. The five fractions were then dried
and weighed separately to obtain the p~rt1cle size distribution
of the substratum. 3 All laboratory \'lork \vas done at the Paclfic !•L'J,rlne
------"""! ------Statio:n, Dillon Beach, Oaltforniao .,-- ~
=------;_: ------
~---
------
=------rr §
~ ------
~------~------~~------~=--~~~
Figure 1.
I'iap of 'l'omales Bay ancl Drakes Estero shovd.ng ------collecting stations. B.z., Batillaria zonalis, 1-i'lalker Creek Delta, 2-:~rD.lcnr Pol:11:-t;--·o-:-o~:'7cert tbJ de a .S..Gll:!.foY:'.n ~-2!:' 1,_Schooner Bay, 2-John s·Jn-Oys' ter... :,;0[~'i)7i:rfi.
:-: ------
------· --·-- 5
------'j------
~ -
Location of Tomales Bay in California
BAY PACIF'IC ------
OCEAN
. '
'' III. HABI ~'A1'
------
].~~J.:.§Lria ~'?_n~~~l~ is nattve to Japan and.. according
_;::;----_ .to Barret·t (1963) may have been introduced to 1'omales Bay =------as early as 1928 when the first experimental sets of
.QF....§:.~-~-~!.?,j;rE]_§.'!; £i..hs.?.:~ were planted ln the bay. However, the first observation of this species along the coast of 1--~----~------'-'------Californta was reported in 1930 (Bonnot 1935a). C:r.assost:cea -·
_gl-.s;a~ was also introduced to Drakes Estero and Bodega Bay in
1932· (Bonnot 1935b) but no specimens of B. ~lt~ 1vere observed at either locality.
-~· Keen· (1963) stated that the range of _Q_~rj.._~.h:~~ll;
££:::,l.tf£.!-'E-l£§. extends from Baja~ northward to Bolin as, Oalifornla.
;t:n th1.s stud.y .Q• .£§9.:.. !.[
C. c~lif..2££~·-911: in Tomales Ba..y but did not collect any. Both B. zonal is and 0. cal:i.fornica inhabit intertidal -----
brackish mudflats and marshes. ]• ~~ 11as collected on the Walker Creek Delta (Fig. 1, B.z.-1) and next to Willow Poi.nt at the head of Tomales Bay (B.z.-2). At both localities the animals ex:perienced wide fluctuations in temperature and salinity._ On the Walker CJreek Delta animals 1·rere found in pools of 2 t.o 5 em depth, in tidal channels, and. on detritus covered rocks and gravel. Occasionally the substratum -rras dry where t.he. animals were found. A sediment analysts of the delta surface mud shov-red 50% of the particles were 7 bet-vreen .. 065 and .25 mm in diameter and 50% -rrere less than .065 mm in dfameter. Less than 50% of' the surface sediment ~--_- --
;::;-.-__-_-,-_------:: was organi.c in nature. Durlng cold weather the snatls 11er~· :__: ______--- . found 1 to 2 em beneath the surface. The length of ]• .z~on.2:.~~is rarely exceeded 25 mm at this station. Young snails with a lengt.h of 2 ro.m were flrst :noted in ~Iayo
The WTTlow Point collecting area t-ras an aband.oned!------~".:c::·::.c:·~::.::::.: m.an~made ditch which was about 5 to 7 m wide ru1d at least 0.5 m deep., The ditch water was stagnant except for slight ti.dal exchange an.d. the sediment "i·Tas slmi.lar to that on the - _-__- __ -_,-_..-._ Walker Creelc Delta.. In contrast to the speci.mens collected a.·t the \la."l.ker O:r.·~;ek Delta, the an:i.mals tn this area were
=------noted. Ce:d.thidea californi.ca was collected at the north end --...... ~~- -·.. ----- of Schooner Bay i.n Drakes Estero (c.c.-1) in a marsh area
---- -· ------and in small man-made pools next to the Johnson Oyster Company (CGc.-2). ·:Both localities experienced fluctuati-ons in temperature and sallnLty. At the Schooner Bay loca11.ty the animals were found along tidal channels which rrere 2 to lt- em deep, and in the marsh.. Some areas of the channels were quite densely populated wj.th the sna:tls. Snails were never found on a dry substratum. A sediment a~alysis of the surface mud shm-Ted 5% of the particles were between .065 and .. 25 rom i.n diameter and 95% were smaller than .065 mmo ------During co1d weather t.he animals were found just beneath the
surface. The length of .Q• .9-~lifo:r~ rarely exceeded 25 rom here or at the second locality. Developing larvae stlll within their protective egg cases were collected in June.
pools rre re dug :i.n to the marsh just above me an high tide so there rfaS little d5.rect exchange I.Vi th the estero Watere ':J.lhe
pools 1-TCre 3 to 1.~ m tn diameter and had 5 to 10 em of water in them. ':Phe pools were carpeted with live and dead snalls
>and the Bed:trr;en t ~vas s~Lmilar to that; found at Schooner Bay.
In :no instance was either -~· .~£!la11:.~ or c •.ca.l:i.:.f.CL£11!£~ -· =-=·-=-=-c.-=------;found coexisting in trw localtttes sampled., l,facdonald (1969} . 5- . -
stated that although c. -~~E_ni.s..§:: vras present in Tomales Bay, it was not found in the samples where B. zonaJ.is was
collected. IV & !•10RPHOLOGY ...,.--
The alimentary tract of B. zonalls (J?ig. 2A) and of - ~--- C. ca}-t.f..£En:i.c§;; (Fig. 2B) can be conveniently divided into five reg5.ons: ( 1) the buccal complE;x includlng radula and mucous e;la.Y.J.ds, (2) the esophagus, (3) the stomach and style
Bl!_~"h .Q.ol!!E.l~!
In B .. ~on~1is (Fig .. 3) the mou.th (mo) opens into the
buccaJ. cavity (be) the anterior limit bel.ng the pair of horny ------jaws (hj) on the anterior dorsal surface and the posterior limit being the point at which the radula. sac (rs) is
---- separated f':rom the lumen of the gut (Graham, 1939). Posteri.or ------to the jmvs, the dorsal surface of the buccal lining, con~ sisting malnly of columnar epitheli.um, becomes folded longitudinally (Fig. 4, lf). The pair of dorsal grooves (dg) created by the dorsal longitudinal folds is heavily ciliated and conspicuous mucous cells are present in the lining of the grooves. The dorsal folds extend beyond the posterior limit of the buccal cavity forming the beginning of a dorsal food groove. The lateral lining of the buccal cavity is smooth anteriorly and becomes folded posteriorly., The ciliated epithelial layer thickens posteriorly. The floor of the buccal cavj.ty is covered by a thick cuticle with the excepti.on of the extreme edges of the cavlty where there are ~------
._. ______----- ~------f;---
Figure 2.
A. D5.agram of the alimentary tract of Batillaria zonalis: B. Diagram of the ali.mentary tract o:rccl:-:rtEiclea ------£:~9.1:~L£'E· The bou.ndries of. the major rt:1g.ion.s .o"Itne"""- al ~m"'rlJ.. l \;...... ~'.C"4.-t "'r··r J -'··r"'•r•tJJ .... ~v <;l.J..,..,~e ...r~a-rlrc,r1 !J. ... .I\..~,\ .... TTl',. _ .p.,\..1.!.l. "'r-.11o .....,...,. __ (1~ ...,.,"'f'"' \.o.~... ..\.:..;..,::.:> ~ ...... 'o'"' ::.J' 1·••hnc•J•..JJ..-4.\..r .... u ... oav~.ty; dd,. o3.gestive divo.rticu113.; ero, esopha;:r;u.s; i:r1s in.tes-·.· ..... '""".,...... ,...,.....,. ..- . _...,...... ,. ti.ne; ...nw:p ~:A :mn.cous t;1ands; ...... mo 1 mouth; ...... :-cd, ra\J.ul8.; ...,..._r;s~ ~1t;yJ.e r•• c.+. !':'·'·onn·~o·}·l' VC'd v~•nt·,.·a·l Cl.llC·'- r•f' ... llt'' c·'·ige"•+i·'~' ·i·'~u~r Sa ..- ' ,!.?.., ...~ s- ...., V . , ~:.t. ' 50...,...,.,.~- s t; ,..t., .. ,. V v \J. ~ .l . .F ..,.., ·v \.; -· '"- J... v ·~ - t 3.ott1a~
--~--~ 11
ln /___ - ~ ss st --'- ~=-;-.::--=~-' - I ~------~:::-i
dd
::;------_---=-=--- ' - ---
B
Figur.o'-' 2 . ~------~
-- ~ ~
L ______:______-----:- _____~------:------:::_,=-.=-··-·_'=.cc-
Diagrammat:i.c longi.tud:l.ns~ section of the buccal region of Batillaria zonalis showing the inside of the buccal cavi:ry-and.-~apwn:·anof the inside of the esophagv.. so ------b,9, _buccal cavity; E:.~:g, dorsal food groove; .£__~, E!SOJ;hagus; liJls horny jm·r::.~; !..:..Lr 1atc:eal foldn; m~~ mucous glands; El9.' mouth; nr1 nerve r:i.i:1g; ods od.ontophor~:; orng, OlJ~H1i.n.g of 'the duct from the mucous gla71ds; .:r::.£r radu1a; -"I:~~ radu.la sac.
-:------13
~----_
~------;....:--~------
Cl.l ('lJ
sbO -'===== 0 ~ 0 • •rl..::t +' 0 •
0 ,.a
s0 ~~~ ------11!-.-.- "'
~~------
h---
Ftgure 4.
:..: ------~- Diagram of a cross section through the middle of the buxmal,m::u::.:s of ·Bat5:112.:I:'~.a zon.ali.s. c-o, ciliated pockets; d 0' ,!' . (";'.~~"'I 0' ., ~-'.v._;'~~~-;·,..,:,...... ,..~,...,.--~1 :-..:.<.:Q~""'.,-,-'"·~r: ·t}' ·-~~~" ~ 1...... r Cf' ·c~ • ) f d 0 "' 1 __ _u, o.or"'ou .6 roov.:.o, .:!:.~.-~,, .. ~J.men o... it. eSOJ)ua":1 U.:>, _;;.._, r,_,a_ long:l.:tu.dina:t. fold; -~~(, odontophore; .f.£, re.dula.
-~------
, ____ ------·-_::--·- 15
.~·
------~-- les
Ed
Figure 4o two small ciliated pockets (op) of unknown function. The
~=--=--=------entire buccal mass is surrounded by a thick layer of complex 'j------musculature.
B -~------
the cuticu.l'ar lining of the buccal cavity and a patr of odontophores (od).
:::;: ___- __,__
=------In etght spec:tmens of B. ~Q.ll~J.i.s the shell length ranged .from 28 to 45 mm and the radula length ranged from 2.5 to 3 mm and never exceeded twice the length of the buccal cavity. The average ratio of' radula length to shell length rlas 0.11 which is lower than the lo·west ratio reported by
Fretter and Graham (1962) of 0.30 for _Nucel1_f!: ~EJ.l!.~· Fretter and Graham indicated that radula length, as measured by the above ratio, appears related to the substratma type. The radula is long where the substratum is coarse causing heavy wear and is short ivhere tbe substratum is soft. Dorsal to the opening of the radula sac and lateral to the dorsal ciliated grooves, a pair of ducts from the 17 palr of buccal mucous glfu"'l.ds {mg) open into the buccal cavity.
Each o.f the buccal mucous glands lying along the dorsal
~-- surface of the esophagus (ez) is composed of three to four Ei ------small convoluted tubules.
The. morphology and histology of the buccal complex
of c. ca.Jl-f.~Fnica as descrtbed by B:c1.ght (1958) is sj.rnllar ·=------'t-e-t-11-a--t-e-f R--.-z-Gn-a-l-i.-£-.------
In five specimens of C • .£~~.for:~.§: the shell length ranged from 28 to 30 mm and the radula length ranged from 2. 5 to 3 mm. The average ratio of radula length to shell length was a low ratio of 0.09. A relationship between short
raduJ.a. 1engtb. and soft substratum seems evident in this
spec1.es a.lso ~ ~Phe paired buccal :mucous glands composed. of
------three to f01.ll~ srr~all tubules are very s:tm:l.lar to those in B. zonal is.
Other mesogastropods with similar buccal complex
morphology are ~J_:thynj:!!:: t~_p.t~~ and. Pomati.§-~ e:l,;_~~~ - --~~--~~
farr:ily Hydrobiidae and~~ ~JZ...~ and M.~.lanta
~~N:i.~~ family ]IIelaniidae (Graham, 1939). All possess the
beginning of a dorsal food groove as found in B. ~~1l.~a
!.~.¢J2h~£;ll§.
The esophagus of B. ~a~J.:..i?.. (Fig. 3, es) ls a tube which begins at the opening of the radula sac and extends to
·the stomach.· As in other style-bearing gastropods, a dorsal
food groove (dfg) is formed by tvro lateral folds (lf) vThich
art;: continu.atlons of t;he lateral folds in tho dorsal 1·1all of 18 the buccal cavity. Posterior to the nerve ring (nr) the
,..--,------lateral folds tHist to the lef·~ a.'.ld the groove becomes ventrally·located due to torsion. The lateral folds end § ___ ~------at a point mid.i·ray bet>:reen the radula sac opening and the stomach. The epithelial lining of the dorsal food groove
:~------'c e-±1~t-a-l-n-s-e-e-B.-S-}3--3:;-e-tl-e-l1-s-ra.-t-l-e-o-CJ.-s-e-E:~-l-l-s-zt:L~t-d-i-s-s-11-r-x~-o-tt11-d-e-d-b-y-rt;------2~~:=::::.:~
layer of muscle. ~he ventral esophageal lining is non ciliated and surrounded by a thin muscle layer. .rmte:riorly, the ventral lining i.s partially composed of large eolumnar
------cells unlike those lining the dorsal food groove. ~hese
cells, ~vhtch appo ~n- slandular in nature,. form small longitud:i.nal rhls;es o:J. the vent:cal 'iiall and. on tb.e ventral - =--=-=·=·=-=-- .. ------side of the lateral folds in the esophagus. Posteriorly~ the large columnar cells are replaced by typical columnar epithelial cells. The function of the large columna.r cells is unknown. Graham (1939) describes similar specialized
cells of v~known function occurring in the ventral esophagus
style-bearing m8sogastropods. The posterior esophagus of
It:.~.!.~~~-~ is thin w·alled, ciliated, and folded longitudinally just before entering the stomach. In c. californica the esophagus has been divided into three regions by Bright (1958); a pre-esophagus, a mid-
11 11 esophagus -vri th a large expanded region call a crop . 19 and a post--esophagus. 'J.lhcse divisions are based on differences
..--.--- - is g:r;oss morphology and histology only. Graham (1939) stated that; the. e,sopha,gus of style-bearing gastropods performs. the
~ingle function of food transport and since this was also
found to be the case in C. call.fornioa no divisions will be - -;".._,..... ,..,...... ,...... ___..,. strfJssod tn this func·U.ona1 approach.
of .9..!. c2).Lr~.9a ends after becomlnz ventrally located as the whole esophageal lining becomes longitudinally folded. This foJ.ded area may be a VE)stlge or a suppression of the
glandular pouches of non- style- be ~ring gastropods (Graham,
1939). 9:h,.:.: .. wall of thG e~wphagus bncomes spirally ridged
';· j l:tst befo:c~ en.te:ring the stom:::tch, unlike the longi tudtnal ---
------
lining in 2....:.':. _£:~~-ifor~~ca there are conspicuous mucous cells. No large. oolwnnar cells were observed as vrere seen i.n
B. zonal is.
_[1;0~~£!9~§..~~~ 'J:n B.· zonalis the stomach (Fig. 5) is the largest
organ i.n the body whorl. The stomach, when opened by a
· dors~l longitudinal slit, is sac-like with the esophagus
entering mid~ventrally (eso), and the intestine opening topographically anteriorly ( tn). Adjacent posteriorly andi
topographlcally to the right of the esophageal opening is '~ ~~--=------
~------
"---
Figure 5.
------m.agram of the stomach of ]£JJJ.:. .:1:.l?.d:iS!: ~Jl§1L§.. The dorsal w:~tll i.s cut open longU;u.d5.naJ.:Ly and laid ba-.::k to the r:i.gb.t 8.nd left.., The arro'i'rs re:p:r.-?.Hien t dire ctio:a. of' cD.i.a::cy beat.. dt, <'lorsal 'typhlofwle; eso, esophageal 0 {"l i I' 0 •C' ,.,.,-'"J: .•. ['>t i• ''V>t(}M'f~'"-'l• •,. ~ t"><"•·ti-n< Op .... n"'_r,g, _.S_>::, 6 as1.1. i·'>·'~ ~H13.f~.··1"· ,.,,_~E;l 1., ... ~-"'" "J.ne) :1:·-lS.! J.:n -·~··': .... a.1 groov·e; J.ni,~ int8sthu::.l tyiJhl.osole; J.rs large r1.d~o; od.dJ ------. ·~ ·, openil'.l_g ·:to-thEl d.:tgesti.ve diverth~l.l.la·;-Ha, sorting ... a.:rea'·o·n the dorsal 'YH.l.ll; -~' small ridge; SS, style sac; . vt, ventral typhlosoleo -- --
------···- - --
.·.,. ~~.·
--- F------
---
F3.gur·e 5. 22 the opening to the duct of the digestive diverticula (odd)e
The adjs.cent positions of these openings is common to many §------~ ~-- - style-bearing mesogastropods such as ~ilsor~lJ:~ .£~~!~ ~------
( Se shatya, 1930), _H;y:dro_bia sp. and J3J:~thY.:ni~ j;en~acula ta: . - (Graham, 1939). Mid-ventrally, to the right of both openings is a large muscular stomach ridge (lr) extending almost the full length of the stomach proper. The posteri'-.o-r-----~----=- end of the large ridge becomes smaller an.d thinner (sr) curving to the left and extending anteriorly to the opening to the duct of the di.gestive diverticula. The lateral groove formed by this stomach ridge channels food matertal from the Bsophagus toward the gastric shield. To the right of the anterio:r half of the stomach ridge lies the gastric ------!., shiel~ (gsJ, a smooth cuticularized area of the stomach lining. The shield provides a firm surface against which the style rotates. The dorsal wall of the stomach (sa) has many small closely set ciliated ri.dges vrhich begin on the -======~ right side and extend to the left toward the opening of the intestine. These ridges function as a sorting area for food
The lining of the stomach is composed of columnar . epi theliu.rn v.rhich is ciliated except for the area of the gastric shteld and the ventral stomach wall between the gastric shield and the opening to the style sac. Beneath ---- the epithelial lining is a thin but distinct layer of muscle 23 which plays an important role in moving food through the . ------.--.--- stomach and the digestive diverticula. The presence of a mus.cle layer in the_ stomach wall is similar·~ to Nysor~.ll"~
.£.£E.lli~~ra (Seshaiyap 1930) but is in contrast to
E~z·u ~~~!:,~_§. l?.§:P..~~.~ (1'1.orton, 1951) i'TbJ.ch .lacks any stomach musculature. and 6) contains the ventral (vt) and dorsal typhlosoles (dt), intestinal groove (ing) ,-and the style sac (ss). The ventral typhlosole begins as a muscular bulge at the anterior edge
------of the stomach proper and narrows as it extends posteriorly to the end;.. of the style sac. Th1.s is in contrast to most stylep·bea:t:'lng mesogastropods whtch 1:.ave a prominent ventral ------
------typhloso1e ;~rhich begins near the esophageal opening (Graham, 1939). At·the posterior end of the style sac the ventral typhlosole continues i.n to the intestine (in t) • The dorsal typhlosole extends from the stomach proper and terminates at the posterior end of the style sac. The two typh.losoles come into contact v-ri th each other and functtonally block commtmication bet'"i·reen the style sac on the ri.ght stde and the intestinal groove on the left side (Fig. 6). Only at the anterior end of the style sac is there a sufficie:a.t opening for .material to move between the style ~ac and the intestinal groove. The style sac is lined with ciliated cuboidal epithelium (Fig. 6, se) exce·pt along the sides of ~------
g__
JPigure 6.
------25
~~--=~-- ---
=
ing vt sse
Figure 6, 26 the typhlosoles ivhe:re the surface i.s composed of tall cU.iated columnar epithelium (se)· and style secreting ep1thelium (sse)., The int.estinal groove (ing) is lined wi"th ciliated columnar eptthelium. The style sac contains the style (s) which is a tapered hyaline rod. In cross section the style is a spLral cotl of ma:Ltn·i.al usually cons1.sting of thr·ee or four layers
wi. th the outer layer being the thickest. The small posterior end of the style sometimes contains a few food,particles from the intesttnal groove v-rhich are bound into the style material. Tho· style ts spongy ancl di.ssolves rapidly in sea "rater or al,cohol so.on after it is removed from the an1.mal.. In 11
~ -- - spe ctrnenEJ the lt)ng'Gh o:f the style ranged from 4 t.o 6 mm and ---- . th..:e height .. of the shell ranged from 28 to 46 mm. 'l'he ratio of style length to shell height was 0.13 ..
The stomach of Q• ~n1~ has been described and figured in general terms by Bright (1958). Bright described - the esophageal opening as occurring at the anterior end of ------the stoma.ch and so figured 1 t. Observations made during this study on ,fifty specimens,. both live and preserved. indicate that the esophagus enters miclventrally rather than
anteriorly (:F'ig. 2, es; Fige 7, eso). Wtthin the stomach of c. californtca (Fig .. 7) there is a large mid.ventral stomach ri.dge (lr) which originates to the rtght of the opening to the duct of the dl.gestive G . !;j___ _ iiL:-::------ g --:_
~:-:=----
=------~------~------~------
Figure 7 e
. ~~' .'28 ~ ·'
,.
n - ss g~ . ~
~- ---
I ;
vt
-·-·gs
-~ ..
( ,.
------
/'
I I I t I
t I I t I I I I I t I 1 I I 1 1 1 1 1 1
I I ·. I I · .. ~I ... · .. • t • I I I I I I I I I I I I 1
Figure 7. 29 di.ver-t1.cula (odd) and extends posterlorly' ending near the base of the· stomach. This is in contrast to the large
- '{ stomach ri.dge :tn B .. zon1lJ.tE! i'lhich curves anteriorly after c'---- nearing the base of the stomachQ In addition to the midventral stomach ridge there are
t1w smalle:r· ridges (sr1 and sr2 ) h1 _9. ••£-Ed.J.JoEJ:c~~" The
=-----.a-n-t-e-i~-i-;0-r-p-e-rt-i-G-!l-e~f-t-h-e-f-iJ~s-t~sm-a-l-l-r-i-d-ge-(-s-r~-,--j-f~o-rra-s-a-V-1·l-~1-t-hc----- tb.e apex pointed toward the intesti.nal opening and the angle of the V abutting the esophageal opening.. This ridge prevents food entering from the esophagus (esc) from being carried
by cillary currents directly into the intestine. ~~he second
small ridge ( sr2 ) extends from a polnt bet"Yreen the esophageal oper1tng axid the opening to the duc:t of the digestive dtvertlcula posteriorly around the base of the large ridge and then anteriorly toward the gastric shield (gs) ending about the rai.ddle of the large ridge. Seshaiya (1930) described
a single long V shaped ridge in }i_ysorell..§ .£_osj.;i~ which functions in the same manner as the two small ridges in ..Q • .<2.P:-ll.££.t"ni ca. The stomach lining in c. californica is composed of - ---... -~... ~~- columnar epithelium rrhich is ciliated except for the areas of the gastric shield and the ventral wall betw·een the gastric shield and the opening of the style sac. The anterior extension of the stomach in o. californica
consi.sts of a style sac (Fig~ 7, ss; Fig. 8) .. The style sac ~~------
~------~----~-~··--~
Figure 8. Cross section of the style sao in Ceri thi.dea calif'orni.ca .. c' ciliary lining of style sac; dse' dorsa"lsty·le secret:l..ng"'-~·-· epithel5.Wl1; s, style; Be, style sac; erJttheJ.tvm; Vg, Ve:o.'traJ. groove; ~£,-·ventr~D. st:~=le secreting cpltheJ.itu:n~~ ...,~
::' 31
q----
----- ~ s c se
5
dse vg vse
Figure 8. 32 opening is next to the opening of the intestine (ino) and communicates ·rri th it for a distance of le.ss than 1 mm. n ~--- Postertorly the style sa.c ~d i.ntestine are completely sep .... arated. There is a prominent longitud.inal ventral groove (vg)
in the style sac which -rras not describ£~d by Bright (1958). The groov•3 ts bounded on b(>th sides by several rows of tall
cells~ ·These cells 'are similar to those found on the edge of the typhlosoles in the style sac of 12· E.££?-].Js and the1.r function is also similar.. There is a ventral typhlosole
present in .Q• .£.§:._~ in the form of a muscular bulge ':·.(Fig .. 7, vt) betvreen the openings of the style sao and the · ..\ intesti.ne but it cloes not extend into the intesttne. Horrever, <=:---
------in the style s::3.c the specialized cells along the right side 5 of the ventral groove appear to be a remnant of the ventral
typhlosole (Fig. 8, vse) ~ The dorsal typhlosole is not evi-
dent in the stomach of Q• ~l-J._fgr11!.91!;, hoiiever, 1. t appears that the spectalizcd cells along the left side of the ventral groove in the style sac may be remna.nts of the dorsal ty- phlosole ( dse) • The cells lining the remainder of the style sac are
heavily ciliated cubotdal epithelium (se) just as in ~· ~a~lli· The arrangement of a separate style sac containing a ventral groove is not unique. Graham (1939) described a sim
ilar si tua.tion in lih..S~€?0_~ ~ar~ family Rissoacea. Seshaiya 33
(1929a) described a style sac groove in the species ']----
J:.alud£I~ .!-:...~2:!l_Ch~~:.~..9.2:' in the genera Melanoicles, Mysorella and .A..mir.Licola (Seshaiya, l929b), and. in the species Potamides . ---~- .£1.n.f:;.~.L~ family Oeri thiidae ( Seshaiya, 1932). - .. ~the style is crystalltne and proteinaceous in nature (Bright, 1958). In five specimens the length of the style
ranged. from 14 to 16 mm and the hei.ght of the shell ranged from 28 to 30 mm. The :catio of style. length to shell hei.ght
was 0 o 51 • The style normally extends the length of the style sac and into the stomach where it dissolves as it rotates against the gastric shield. Of 25 live dissections, two revealed uxJ.usua.l style positions. In one case the style
·extended beyond the gastric shield to the base of the stomach. =--- . In the othex· case, the style did not touch the gastric shl.eld at all. The style entered the stomach to the left of the large stomach ridge and extended over the openings to the ducts of the digesttve diverticula terminating at the
posterior end of the large ridge~
The crystalline style of c. califo:t;EJ:.c.~ is firm but flexible and does not dissolve in sea '\vater, 70% isopropyl
• I alcohol or Bouin's fixative$
In the stoma.ch of c. _calif..2£nic~ the intestinal opening (lPig. 7, ino) is to the left of the style sac open ing. Several ciliated tracts lead to the intestinal opening
al('Jng the stomach rralls as in ]• E.,?~i~. ~- - 1 g_
The openi.ng to the duct of the digesti.ve diverticula ~-- " -- in B. Z£~ (Fig. 5, odd) leads into a s:i.ngle main duct. (Fig .. 2, vdd) 'tvhich extends to the tip of the visceral hump
along t,hf3 ventral· side. The main duct is lined ~~-1 th non- ciliated columnar epithelium.. :b,rom the main duct there are :numerous smaller ducts leading :i.n to the digestive diverticula tissue., These secondary ducts split once or tw·ice and lead to sinuses lined by ti"TO types of cells 1-rhioh are very similar· to those descri.bed to be digestive and excretory tn nature
in Bi thynia tent~wulata (Fretter and Graham, 1962) and i.n ,,, ~, ~ ' ' ...,..,_,._ .... -.w.... .-...~•· .,..._,..,.~·~.._~ .... .-.-.--,.-,._~._., ...., < ; Struthiolar:i..a. papuJ.osa (Horton, 1951). The excretory cells .... ~ ----... ,...~ .. -~ ...... ,...... -.'>"J>S~><··--· ...... ~----:- ..
'" are cl!.aracteri?;ed by the presence of what appear to be ~--- excre"'Go::t7 spherules ..
The digestive diverticula in c • .£§1J..J.'.~rn1.ct?; is similar
to that o.f ]• z~I?, in having a single ventral main duct (Fig. 2B, vdd), lined. with ciliated columnar epithelium as
described by Brlght (1958). Also, the digestive diverticula
of Ce 2~1JJ_~£§ has a branching duct system leading to .the
sinu8es ltned v-rit.h the same types of. cells fountl in ]• ~}!.~b'L?.•
~'he presence of a single ventral main duct in the digestive diverticula is reported to be common by E. H. Smith (personal communication) although Fretter and Graham (1962) commented that in many prosobranchs a pair of ducts is .f.requently foundo 35
--·~...._.Intestine ___ _ ,, 1'he intestinal groove in ]• _?onaJ._i_~ (Fig. 5, ing) L .• 6::--: leads di.rectly into the intestine. The intestine makes a loop and then extends ante.riorly along the right side of the mantle cavity and ends just inside the mantle edge at the anu.s, The first third of the intestine ls characterized
~----hy-t-he-pxe-se-nee-o1'-a-ve-nt-.:cal-i-n-te-s·i:;-hra:l-typh:t-osore-(-tn-t-)------:---- ~"' _:______::______:_____:: which is an anterior extension of the ventral typhlosole of the stomach and style sac regions. The middle third of the. intestine lacks the typhlosole and is the region w·here ,fecal pellets are formed. The last third of the intestine
has folded. ·walls capable of expanding to hold several fecal '~ pellets at one time. The intestine is lined with ciliated
;:..... ______coltt!.nn.ar epitheli.um and scattered mucous cells.
In the stomach of c. ~..9E2J.ca, the intestinal. opening (Fig. 7, ino) is to the left of the opening of the style sac. There is a longitudinal ventral typhlosole
present in the first section of the intestine, as in ]• ~li~, but it does not connect with the ventral typhlosole in the stomac:h. Present w1.th the typhlosole are five longitudinal ridges. The fold and ridges end after the first loop of the 1ntestineo The. next region is characterized by its resemblance to a triangle when seen in cross sectton due· to three thickenings in the intestinal wallc This is the pellet molding region. Morton (1951) described a similar triangular region in Struj;J:!Jo}ari~ ~..E_lo~ which has the
same function. The posterior portion of the intestine is· r;------ ~~~ ~=-:~~ =-~:_-~=~-=::--~--::-~ similar to that in E._, ~2D§1ll• The intestine .ends just inside the right edge of the mantle cavity at the anus. The entire intestine is lined wlth ciliated columnar ep:i.theli.um as BJ."ight (1958) described,
;------~------~------~----- V • Ji'UNCTIONAL MORPHOLOGY
B£££§:1 Co~l~!. ~---- ~at~l}_~~~ ~9~~lis feeds by scraping a fluid mixture
of mud ~L~d detritus into its mouth with a radula. The radtLl a rasps con tinualJ.y lThlle the animaJ. is on a moist
dry· substratum. The radula dra:i-TS the food material under and against a chitinous jaw vri thin the mouth which caune s the aggregated food particles to be broken into smiller pieces. · Posterior to the jaw, the food particles are p1.ckecl up by - · c).ltary currents in the dorsal lateral grooves. As the
-~ particles proceed toward the esophagus, muctis is added from a pair of small buccal mucous glands. IJ:'he dorsal lateral grooves become a single dorsal food groove in the esophagus. The radula tn Ce rl thide a californica functions in ---~.---- the same· manner as the radula in B. zonalis.. Horrever, the substratum on which c. californica feeds is finer and more
uniform than that of B. ~~a~~ and it was always moist, resulting in a more continuous feeding habit than that of
]• ~o~l-~· Food is carried past the ja1v, mixed with mucus from the small ,buccal .mucous· glands and moved posteriorly by ciliary currents to the dorsal food groove of the esophagus. Both B. zonalis and c. californica have short radulae which appear to be correlated to the soft substratum on 38 which the animals feed (]'retter and Graham, 1962). In h n addition, both species possess only one pair of mucous ~---- secreting glan·ds in the buccal complex. These glands are small apparently because the food mixture· is quite fluid and therefore mucus is only needed to bind the food into a food string a:nd not needed to lubricate the radula. Tht; probablli ty
(1939) stated that since proteolltic enzymes from the buccal mucous glandB wlll interfere with the functi.oning of a crystalline style, the function of the glands is accordingly modJ.fied in style-bearing prosobranchs. In addition, lt,rotter a:nd Graham (196i2) reported that few prosobranchs secrnt d_lgestJ.vc.; enzymes in the muc-v.s from buccal mucous glands. Ciliary currents constitute the major means for transporting food material in the alimentary system of both species and the dorsal lateral grooves in the buccal complex are the beglnning of this ciliary transport system. The currents created by the ciliary beat in the grooves efficiently channel the food material away from the radula and toward the esophagus thereby preventing the buccal cavity from becoming clogged .. The functional morphology of the buccal complex of
~l..S~d!.£1: ~~~ (Seshaiya, 1930) and Struthiol~ ~£1.}1.9.~
(Morton, 1951) is quite similar to that of ~· -~-o_!l_aJ_is and
0 .. californ1.ca. M.. .£OS!:!M~' a freshvrater Hydro bid with a 39 crystall5.ne stylet feeds on fine moist detrital material in
!:) ___ Indi.a and .§• J?.~£..~.1~.~, a marine style··bearing ciliary feeder iii------"'~ ~ in New Zeala.n.Q., also tnge sts fine detrital material.
In ]• -~~.12-...?dl.~s food enters the dorsal food groove of
1______,t_he_e_s_n_p__).~_agu_a_f_r_Qm_th!L_j;-wo dfrrsal lateral grooves of the ... --- buc:cal cavity and 1-s carried postertorly by ciliary currents. Almost no food ts found in the anterior non-ciliated ventral
portion of' the esophagus.. Although glandular-~like tissue is present in the ventral esophagus its func-tion is unknown .. Throughout the length. of the esophagus mucus is ad.ded to the food mixtt.'!.re creating a food string. Ciliary currents continue to tra.nsport the food st::r·lng posteriorly through the esophagus to the stomach.
In ~· £?~ir£~n~~~' as in B. zonal~, food in the esophagus is carried by ciliary currents almost excl.usi vely in a dorsal food groove. Ventrally there is no glandular tissue as vias found in the ventral esophagus of ]• zona11E_ ..
Unlike B. zonalis the dorsal food groove of c. califo1~ica ~ .. ._ ...... _...... ' - -~...... "" blends into a mul tifolded expanded region just posterior to the area of torsion. Glandular ti.ssue is absent, however, mucus is added to the food i.n the expanded region. Ciliary currents continue to carry the food stri.ng posteriorly to
-~--- the stomach. 4·0 These findings agree specifically with those of Graham
(19~?9) concerning the modification of esophageal gftandular !'.!" E ·_- areas in style-1?earing gastropods. Graham reported thB.t the gla.nd~J.lar are as were either sup pressed (1,1hich is the case in. • I
].!. ~~:!1~) or replaced by ciliated and mucous cells \'lith the walls retaining their expanded ::mc1 folded nature (vrhtch is the
a series of gla~ndular esophageal structures are alternative mechanisms, mutually tnconsistent, for helping in the digestion of food.
In B. ~~o:nali.s food is carrl.ed into tho stomach mid~·ven trT-tJ.ly from the o sophagus. Once in the stomach, the ;:... __ ------Govements of food are affected by o1liary.beat (Fig. 5), stomach .morphology, rotation of the style, muscular activity of the stomach ·walls and internal fluid pressures. Nevi techniq_ues such as the use of X-ray, need to be developed before the effect of muscular activity of the stomach wall and the internal fluid pressures can be studied sinee it ts impossible to study their functioning once the stomach has been disse,cted. Ciliary currents on the ventral surface of the stomach carry the food posteriorly to the base of the stomach and then ant.er.iorly tov-Ta.rd the gastric shield and rotating style. l~1 The stomach ridge ( sr and lr) keeps the food string in the groove leading to the gastric shield. The style which is rotating clocbrise (seen from a posterior view) against the gastric shield is slowly dissolving and apparently releasing digest:tve enzymes one of which is probably amylase (Yonge, 1932). Tall slender glandular cells along the edge of the typhlosole (:b'ig& 6, sse) lv·ithin the style sac produce the style mater:i.al vrhich then i.s e.dded to the efttire length of the style as it rotates. The style is rotated by a strong ciliary current wi·thin the style sac and at the same time pushed against the gastrtc shield by the \. constant addi tio:a. of style material to 1. ts tapered surface. '· The style material dlssolves because the hydrogen ion :>.,.concantratj.o:n. of the stomach is higher than that of the style sac causing a change in viscosity of the style material (Yonge, _1932). The food material is caught in the dissolvi.ng end of the style and moved clock\rise with it. The enzymes from the style begin digestion of the food by breaking dovm \ the larger usable particles. The food particles are swept away from the style by ciliary currents on the dorsal wall vihich flow parallel to, but in opposite direction of the style 1 s rotation. The d.orsal wall of the stomach (Fig .. 5, sa) is composed of numerous closely set ridges which serve as a sorting area for the food materlal·. Larger particles, ·which would 1!·2 include most of the unusable material, break loose from the mucus and food mixture and are m•rept into the grooves of the
~~---" ~ sorting area and then transported dj.rectly to the intest:l.nal
groove ~(ing) and then to the intestine (in) by ciliary
curx·ents.
!•lorton (1953) has suggested. that the slit bet1-reen the
=-~~~-;s-ty-1-e-~-as-s;;-aE!.-i-n-t-e-s-t-1-na-l-g~~~)-ev~e-i-s-f-tb.~G-t:-1-ena-l--J;-y-i-m-pe~p-ta-n-t-i-n~---- t! ___
providing for the possible retrieval of undigested food
material leaving the stoma~ch. In B. g'i..9..:~..li.§_ the position of the typhlosoles and the ciliary curl"ent; on the surface of the ventral typhlosole functionally block communication
·" betvreen the lntestine and the style sac. There appears to
1 . :; be no retrieval mechanism in the stomach and. style sac :i:·egion
H
The smaller particles remain in the lumen of the stomach 11rhere the enzymes from the style continue to act on them. .r.1ultidirectlonal ciliary currents on the surface of the large rld.ge keep the stomach contents in motion. Periodically, muscular contractions of the stomach force food material into the digestive diverticula (odd) where digestion
and absorption takes place·. As the stonu.wh wall relaxes the food mixture ls d.raw·n out of the diges·tive diverticula and picked up by ciliary currents on the floor of the stomach and carried anteriorly to the intestinal groove. In c. californica food material enters the stomach . ------· mid-·ventrally (Ftg. 7), It is pre~rented from being carrled 43
dlrect1y 1.nto 'the intestinal opening by a small ridge (sr ) o 1
This feature is absent i.n B. z.9.£~]:J.§!.• The material is g: __--
------carried touard the gastric shield and rotating style by ~, __ cD.iary currents on the ventral rrall of the stomach groove. The groove is bounded medially by two stomach ridges (sr ' 0G and ·lr) wh1.ch is in contrast to the single stomach ridge in
--B. __zonalls ...__..,.._ .. The style in c. ~l_f_9.1:n~ca.: rotates clockwise, slovrly
dissolvlng and releaslng digestive enzymes as ~n ] .. ~_o~~_ia~ Tall slender glandular cells found along the ventral groove = of the style sac of .Q• _9a~.lf2XE)·S1Z (]11.g. 8, vse a.rt.d dse) secrete style material throughouJc the style sac but primarily
- at the distal end. These glandular cells along the ventral ---- groove al'C homologous to the gls.:n.dttlar cells on the ty:phlosoles
of the style sac in B. zon.~~~. This homology is supported by Morton (1951) who described the secretion of the style in
St~th~-~ri~ .R.~J?Ul2E~ as coming from a narrovr strip of tall cells along the typhlosole. The drawings of Kubomura (1957) diagraillllling cross sections of the style sacs of the
tectibranch, _!h_ili.fl!:. ~.S:Es>~ica, and the mesogastropod,
2.~~~~JLE.ia ~~9~~~~, show an area on the typhlosole of
small slender cells similar to those in both ]• ~is and
c. ~~Z~rntc~. Seshaiya (1930) found tall slender cells - . along the typhlosole of the fresh water style-bearing
gastropod, l1:LE~.l~.a -~~~' but did not discuss their 44 function. Also, Fretter _and. Gra.harn (1962) stated that most of the style ·substance ls derived from the gland cells on the typhlosoles. Food materiaJ. is m·rept away from the rotating style by currents on the dorsal 1-rall of the stomach {_:Fig .. 7, sa). The dorsal wall acts as a sorting area and larger particles ~------~~~-.------~------~~~----~~------~~~------:~are moved tnto the grooves of the sorting area and are ___ ----- transported by ciliary currents int_o the opening to the intestine. The smaller particles rematn in the lumen of the stomach 1-1here digestive action continues and 1vhere ciliary currents and muscular contract5.ons can. move them into the
dv.ct to the d5.gesM.ve diverticula. In .contrast to B•. ~.2,paJ.iE!_,
in the stomach of c. s:aJJfo.:r:~.L~ a cil5.ated ventral groove (vg) r ----n- i.· is present betw·een the t-vro ventral ridges (lr and sr2 ) vrhi.ch
allows some of the food particles to re-enter the ch~~nel leading to the gastric shield and.' hence be re-sorted and
digested further. Material leaving the digestive diverticula is carried by ciliary currents tmrrard the j_ntestine channeled by a small
ridge (sr2) whtch prevents mixi.ng of the materj.al entering and leaving the stomach. The basic functional morphology of the stomach and
style regions of both B. zonal is and .Q • .£§l:-1.J:...forni~ are . s imtlar to most style-be ari.ng mesogastropods. However, as Yonge (1932), Graham (1939) and 1-'Iorton (1953) have stated, 45 the stomach in style~bearers is the region most highly specialized for sorting and digesting a continuous st:rea.m of fine detrital material, In light of the apparent differences in substratum and hence in ingested food in the species in ~------this study, it is relevent to examh1e the detailed functional morphology of the stomach regions for possible correlations
i'Ti th food type • .---~----~--~------~----~ As noted above, the food material ingested by ,_------
g_. ~f'2_tni£§:_ is very fine and is composed of over 80% organic material. The ridges (sr and sr ) present in the 1 2 stomach of c. californica are specialized structures which channel food mater:i.al toward the areas of sorting and
) digestj.. on. The first ridge (sr1 prevei1ts the incoming
food material from becoming immedis:tely mixed '\~Ti th the out- :--- going material and thus lost for digestive purposes. The
second ridge (sr2 ) serves to channel food material which
has already passed over the dorsal sorting area back into ----- the groove leading to the gastric shield and style w·here additional digestive material may be added to the mixture. In contrast, in B. ?Onalis, the food material ingested is not well sorted and is of lov'f organic content and the -stomach mc;'rphology is less complex. Food material is moved through the stomach as a vaguely defined mass with few
channeling ridges and with no recycling currents. The food --- material does not warrent specialized morphological features 46 to prevent premature loss of food material nor does it need recycling to add further style enzymes for complete digestion.
~- This study suggests a relationship betHeen style
length and the composition of the ingested food. A general correlation bet"t-reen food type and functional morphology is well established. Mackintosh (1925) postulated that the
~--~~~~~pre-s-e-nc-e-o-f-a-s-tyxe-:tn-gas-tropod-s-rr.Lay-be-corr·e-1ated--v7-tth-the~~~~-"~-- L ______
ingestion of diatoms and similar micro~·o:rganisms·. Yonge (1930)
stated that the presence of a style in gastropods is corr~lated with either a ciliary or a rasping mode of feeding and formulated the rule that the presence of a style means the animal is a specialized herbivore. Yonge (1932) examined this correlatlon further and noted that i'Jhile the style is restricted to herbivorous gastropods it is not true that all herbivorous gastropods possess a style. Only those which supply finely divided food continuously to the stomach possess a style. Graham (1939) stated that the style developed in those animals which feed conti.nually on unicellular or small multicellular algae. Morton (1953) stated that the crystalline style sac in the Lamellibranchia remains generally longer and more .specializ"ed than in the Gastropoda. In the Lamellibranchia the gills sort the food material and reject the larger :and heavier particles in "pseudofeces" before they enter the· mouth, In comparison, g_, cali:f2grnica feeds on a substratum which is already quite well sorted and highly organic in compositlon and correspondingly it possesses a relatively
long style. In contrast, B. zonali~ with a short style ~- feeds on a. substratum i'Thich is not a·s well sorted and which has a low organic content. An enzyme supply sufficient to fully digest the avaiTEili---re rooa. would be advantageous for a slow continuously feeding mollusc. It may be possible that an increase in available enzymes is brought about, in those I..amillebranchia and Gastropods \'ihich digest well sorted and highly organic food material, through elongation of' the style sac v·ri th a corresponding increase in style secreting tissue and style length. Assuming a falrly similar even rate of style
· 1. procluction from species to species the tncrease in style length would provide an increase in the supply of digestive enzymes.
~±gestive Di~rti~~~
In B. zona~ pa~ticles entering the digestive diverticula are i'Iell mixed with style mucus, This mixture is pumped do-w·n the main duct of the digestive diverticula (Fig. 2A, vdd) by contractions of the stomach. No ciliary currents were observed to aid food movement in the main duct. Following each contraction the stomach relaxes and the material in the duct moves toward the stomach. These movements in the duct were observed only in intact specimens. The 48 material in the secondary ducts moves in and out in an
irregular manner which 1-s independent o.f the movement in the e--=----::------~-- maln duct a.lld indicates that the stomach contractions do not move mate:ri.al into the secondary ducts. Since there are. no muscles in the digestive diverticula tissue it appears that regulated ci1tary currents may be responsible for movement
In Ce .£_alt_fornic§! material is pumped in and out of the maln duct of the digestive diverticula (Fig. 2B, vdd),
as in B. ~ne3:1:_1~, by stomach contractions. Also, materia.l appears to enter and leave the secondary ducts by ciliary means, as in B.. £Ql~?,;;t.:l.~. In c • .£.illf~~c~, however, there is a definite rhythm and timing to the movement withln the secondary ducts whtch ts independent of the movement in the main du.ct. In both B. zonalis and c. californtca the movement
---- of material through the branching system of the digestive --- diverticula first by muscular contractions and then by ciliary beat, functions to steadily bring the food material into contact liTith the digestive epithelium where i.ntra--cellttla.r dtgestion apparently takes place. The excretory spheru.les
present in the epithel:l.um, described previously, appear to --- be carried out of the tubules into. the main duct of the digestlve diverticula and from there into the ciliary currents on the ventral surface of the stomach which enter the 49 intestine. 'l1he functi~ming of the digestive diverticula in both B.. ~nalis and .Q • .£5!dj.fornica appears ve.ry similar to that described by Morton (1951) in Struthiol~ .£§]2-g]~~· -Intestine In B. zonalis, after leaving the stomach, undigested ,f'!"!!"l. ---- and undigestible materj.al enters the intestine where it ls
carried posteriorly by ciliary currents. The i.ntestine ..;::;------appears to function solely to compact the food materlal into fecal pellets. Hyman (1967) stated that the hydrogen ion concentration in the intestine is higher than it is in the stomach. This results in an increase in the viscosity of the intestinal mucus which serves to bind the fecal matter.·. The function of thf) ventral typhlosole tn the anterior third of E the intestine of B. ~ is v.nclear. The mtd-portion of the intestine molds the fecal matter into fecal pellets through.the peristaltic action of the muscles lining the intestine. In the posterior portion the final mucous coating .is added ·t;o the fecal pellets and the expanded region just anterior to the anus allm·rs room for the pellets to be stored briefly vThile the mucous coating hardens. The fecal pellets are expelled periodically by peristaltic action and c1.liary currents carry them away from the mouth along the right side of the foot and head. In .Q• californica the intestine also appears to function solely for compacting and transport1.ng the fecal 50 matter out of the body cavity. The viscous intestinal mucus g---- binds the fecal matter as in B. zonalis. The ventral typhlosoie, ·in c .. californica~ appears to function some"'i'Tha.t ~-- as a channel for the fecal material slnce the majority of the fecal matter was observed massed along the left side of the typhlosole. In addition, the five ridges present in c. ~for:-9:1;.£§; may be specialized mucous secreting areas ;..2 ------since the ridge tissue appears glandular tn nature. The f'ecal material is molded into pellets in the mid-in.testine and the mucous coating hardens in the expanded posterior region as in B. zonalis. The pellets are expelled and carried away from the mouth in the smne manner as in B.
- - _zonal_,__._, is. __ ~----
--- VI. ACKNmH,EDGMENTS
I wish to thank Dr. Edmund He Smith for his invaluable advice and help during my research and the preparation of this thesis. · I· also want to thank Dr. John Tucker, Dr. Gary Brusca and Dr. Michael Kaill for their help and Dr. Iviyra Keen who .verified the ident:i.. O.cation of the tvTo species studi.ed.
~------
=
:-;------
"'_::::______--- - - ·- BI BJ.~ I OG RAPHY ~-- ci- f'ii~-== -_ --- Barrett, Elinore M~ 1963. The Califo.rnia oyster 1.ndustry. The Resources Agency of. Calif., Dept. of Fish and Game Fi.sh. Bull. 123., . Borillot, Paul., 1935a.. A recent introduction of exotic species of molluscs in California -waters from Japan. · Nautilus. 49(1):1-2. .
:~----~~~--·· t9.35b_.____The_C_al_if_o_rn_La_QYS t_e_r industrY~·-~C~a=l=i=f~·------" Jf:Lsh and Game. 21 ( 1): 65·~80., v - ~------Bright, Donald B. 1958. Morphology of the common mudflat snail, Cerithidea ca.lifornica. Bull. So. Cal. Acad. sci o s7T3riT27~~f39:"
-----· 1960. ~forphology of the common mudflat snail, Cerithtdea ca.lifornica, II. Bull .. So., Cal. Acad. · ·sc-r:·-~59 IT) T9-='"rs:--- Fretter.t Vera and Alastai_:r Grah.am. 1962. British pro so branch molluscs j the j.r functional anatomy and. ecology. 'l'he Ray Society, London. 755 p. ;--n-•• Graham, Alastair. 1939. On the structure of the alimentary canal of style~bearing prosobranchs.. Pro. Zool. Soc. of London, Series B. 109(1) :75-112. Hanna, G. Dallas. 1966. Introduced mollusks of 1'-lestern North America. Occasional Papers of the Calif. Acad .. --- of Sci. LJ.8. 108 p. Humason, Gretchen L. 1967. Animal tissue techniques. w. H. Freeman and Co., San Francisco. 569 p. Hyman, JJlbbie Henrietta. 1967. The invertebrates, Volume VI, Mollusca I. McGraw~Hill Book Co., New York. 792 p. Keen, A. :Hyra. 1963. Marine molluscan genera of ·western No'rth America. Stanford Uni v. Press, Stanford, Calif. 126 Po Kubomura, Kazuko. 1957· Some Japanese gastropods with the crystalline style. Sci. Rept. Saitama Untv., Series B. (Bicl.) 2:269-279o ----- 53
Macdonald, Ke 1 th B. 1969. 1,1olluscan faunas of Pacific coast salt marshes and tidal creeks. Veliger. 11 (1+) :399-l!-05.
l-1ackintoshp N$ A. 1925.. The crystalline style in gastropods. Qus..:r.t. JoUl"'., Ivlicr. Sci. 69:317~342. 1-Iorton, J. :r.::. 1951. Ecology and digestive system of the Struthiolariidae. Quart. Jour. Micr. Sci. 92: ·1-25.
-n~-··--~·· 1953.. The functtons of the gastropod stomach. Proc. Llnn~ Soc. Lond~ 164:240-246.
~~------~------~----~---- Seshaiya, R. V & 1929a. The stomach of Paludonms tra..YJ.shaurica (Gmelin). Rec. Indian N:us., 31:7-12.------~--,·-----
• 1929b. The style-sac of some freslnvater gastropods. -R:ec;-~· Indian 11us .. 31:101-105 ..
-----· 1930~ Anatomy of !:'!Y.!l.E.E~lla ~~g_e}:§: Kuster. Reo. Indj_an Nus. 32: 1-28., • 1932. The style-sees of some more gastropods. -nREi'c-. Incl5.an. Ivius. 34-:171-175 ..
=- '/ .Yonge, Charles ,Maurtc:e. 1930o The crystalline style of the ----- mollusca and a carnivorous habJ. t cannot normally co-existo Nature, London. 125:444-445o • 1932o Notes on feeding and digestion in Pterocera ---ancrverruetus, with a discussion on the occurrence of the crystalline style in the gastropoda. Sceo Rep. G. Barrier Reef Exped., Brit. Mus. (Nat. Hlst .. ) .. 1:259-281. ---