Table Of ContentReference: Biol liu/l 183: 503-506. (December, 1992)
The Zooxanthellal Tubular System in the Giant Clam
JOHHENLEHN. NM.ORLTOONNG1,1 MAANLDCOWLILMLIA.AMSHKE.PFHIETRT2D1,
,
1Queensland Department ofPrimary Industries, Oonoonba Veterinary Laboratory, P. O. Box 1085,
Townsville 4810, Queensland. Australia, and 2University ofGeorgia, Department ofZoology.
724 Biological Sciences Building, Athens, Georgia 30602
Giant clams (family Tridacnidae) are special in that they the digestive diverticular ducts ofthe stomach (Figs, la,
contain large numbers ofsymbiotic dinoflagellates, Sym- b). It passesdorsallyand posteriorlybetween thedigestive
biodinium commonlycalledzooxanthellae which live diverticula, andthen between thecrystalline stylesacand
sp.,
inthedam'ssiphonalmantle(hypertrophiedsiphonaltis- the muscular wall that encloses the digestive and repro-
sues) (1) andare important in its nutrition (2, 3). In 1946, ductiveorgans. Abovethedigestive organs, itdividesinto
Mansour (4) partially described a tubular system arising right and left tubes. These tubes pass close to the dorsal
from the clam stomach, extending into the mantle and aspect ofthe muscular wall, then through this muscular
containing zooxanthellae. However, the eminent scientist wall and into the kidney parenchyma. Both tubes travel
Sir Maurice Yonge (5, 6) disputed its existence. Subse- through the kidney in a more ventral direction, until they
quently. Yonge's views appear to have suppressedfurther leavethekidneyandentertherootofthe middlectenidial
investigations of Mansour's observations. The zooxan- suspensory ligament. The tubes continue to travel pos-
thcllae have been universally regarded as living in the teriorly, where they become embedded in the connective
hcmal spaces ofthe mantle (2. 5, 7. 8. 9). This study, tissuesheathoftheadductormuscle. Whiletraversingthe
however, hasconfirmedthepresenceofthetubularsystem posterior portion ofthe adductor muscle, each tubegives
indicated by Mansour and has shown that the zooxan- offa branch which isembedded in the floorofthe excur-
thellae live within a branched, tubular structure that has rent water chamber. Each primary tube associated with
no direct connection with the hemolymph. The existence the zooxanthellae passes toward the end ofthe adductor
ofthis tubularsystem has important implications for our muscle, and dorsally intotheroot ofthesiphonal mantle,
understanding ofthe symbiosis between tndacnids and before branching both anteriorly and posteriorly. One or
their symbiotic algae. more main branches run along inside the root ofthe si-
phonal mantle close to the circumpallial artery, the cir-
During a study ofthe anatomy and histology ofgiant cumpallial vein, and the pallial nerves. Secondary zoo-
clams, numerous Tridacnagigas. from a few millimeters xanthellal tubes branch into the upper levels ofthe inner
to 35 cm in shell length,weredissected. Tissueswerefixed fold ofthe siphonal mantle, where they terminate in con-
in 10% seawater formalin, processed by routine histolog- volutions of thin tertiary tubes with blind ends. These
ical methods, including serial sectioning, and stained with tertiarytubescontain thezooxanthellae. Othersecondary
hematoxylinandeosin(H& E). Additional stainsincluded branches form tertiary tubes in other organs, such as in
Masson'strichome formuscletissue, periodicAcid-Schiff the connective tissue surrounding the adductor muscle
(PAS)and PAS/diastase forglycogen, starch, neutral mu- and in the connective tissues ofthe bulbus arteriosus of
copolysaccharides and glycoproteins, and an Aldan Blue the heart, the pericardium, the ctenidia, and the lateral
stain to delineate the tertiary zooxanthellal tubes. mantle.
The zooxanthellal tubular system was found to com- The primary zooxanthellal tubes (Fig. 2) have an ep-
mence as a single primary tube, originating from one of ithelial lining of cuboidal to low columnar cells with
long cilia and are surrounded by a thin zone ofmuscle
Received 14 May 1992; accepted 22 September 1992. fibers. The secondary tubes (Fig. 3) are thin-walled and
503
504 J. H. NORTON ET AL.
TZT
SZT
CTN
TZT PZT
SZT
Figure I. Diagrammatic wrivotthepathfallowedbvthezooxanthellaltubethrough agiant clam Theblack, highly
branchedstructureon thesurfaceofthestomach (S) in both a andb isthemass ojdigestivedivenicitlar Notethai the
primaryzooxanlhellaltube(PZT)originatesfromoneofthediverticu/arducts a Medialviewofabissecledclam b Dorsal
viewofabissecledclam.
Abbreviations. AM = adductor muscle. BOF = byssal organ/foot. CTN = clenidia; K = kidney P =pericardium;
PZT = primary zooxanthellal tube; S = stomach; S\l = siphonalmuscle; SZT = secondary zooxanlhellal lube. TZT
= tertiaryzooxanlhellallube
are lined by > Hiated epithelial cells with thin cytoplasm not found in hemolymph samples from giant clams (10,
and small, pro: inent dark nuclei. Similarcellsline the 1 1). Although some elements of the tubular system asso-
tertiary tubes (i . 3), but these cells appear to lack ciated with the zooxanthellae were partially described by
cilia. In naturalh > o "rring bleached mantles, i.e., in Mansour (4), he did not recognize that the tertiary zoo-
mantles lacking zooxanthellae, the tertiary zooxan- xanthellal tubes have blind ends and do not communicate
thellal tubes atrophy. with the hemolymph system. Parts of the tubular system
No zooxanthellae were observed living free in the hemal have been described previously by others (2, 12). but inter-
sinuses, explaining previous reports that zooxanthellae are preted as communicating with the hemolymphatic system.
ZOOXANTHELLAL TUBULAR SYSTEM IN CLAM 505
CCL
wm
- 3* *'
'y.*NP
JB
fryg.
:./ ,^z
K
v
y-
.':'"*
fr
v '"'
:
v
.
. *
Figure2. Aprimary:ttn\aiuhfllalluhc/transversesection. H&Eslain. Bar= 19^m)
Abbreviations. CCL = ciliatedcolumnarepithelium. MSF= musclelibers:Z= :<>u\anihellae
Ourobservations resolve much ofthe controversy that the symbiosis functions. For example, Yonge (16) drew
hasexisted overthe past 50 yearsconcerning the location attention to the need to regulate the numbers of zoo-
and fate ofzooxanthellae in the giant clams (2. 4, 5. 6, 7, xanthellae that reproduce in the siphonal mantle. Yonge
9. 10. 11. 13. 14. 15. 16. 17). Theexistence ofthissystem hypothesized that the algae are culled from the siphonal
simplifies the interpretation ofprevious data on the way mantle by amoebocytes, wherein they are digested, and
_
Figure 3. Secondary and ternary -no\anlhellal tuhes in the siphonal mantle (transverse section, Aician Blue stain.
Bar= 23nm)-
Abbrevtations:SZT= .secondaryzooxonthellalluhc, TZT= tertiaryzooxantheUatlube, 7. = zooxanthellae
506 J. H. NORTON ET AL
that the indigestible remains accumulate in the kidneys 7. Fankboner, P. V., and R. G. B. Reid. 1991. Nutrition in giant
(18). As has been stated before, there is no evidence of culMaemmso(rTiraidlacSnyimdapeo)s.iPupm. i1n9H5-o2n0o9urinqtThSierBCihvaarlv/ieaxMaPurroiceceediYnognsgeo.f
this, and the algae move from the siphonal mantle to the Edinburgh. 1986. B.Morton,ed. HongKongUniversityPress,Hong
stomach. Healthy zooxanthellae observed in thestomach Kong.
(19), pass through the intestine and the rectum (2. 20) 8. kawaguti,S. 1966. Electronmicroscopyonthemantleofthegiant
and are released in the feces; thus these algae, by an un- clamwithspecial referencestozooxanthellaeand iridophores. Biol.
J Okayama L'nn: 12: 81-92.
known mechanism, are able to resist host digestion. This 9. Fankboner, P. V. 1971. Intracellular digestion ofsymbiotic zoo-
route is also available for the mass expulsion of zoo- xanthellae by host amoebocytes in giant clams (Bivalvia: Tridac-
xanthellae from clams exposed to elevated environmental nidae), with a noteon the nutritional role ofthe hypertrophied si-
temperatures (21). Furthermore, there is no direct con- phonalepidermis. Biol. Bull 141: 222-234.
nection between the hemolymph and the stomach, via 10. Yonge,C.M. 1936. Modeoflife,feeding,digestionandsymbiosis
with zooxanthellae in thetridacnidae. Sd. Rep. Great BarrierReel
the tubes associated with the zooxanthellae, that would Expcd lv:,S-lV2V. 1:283-331.
allow digestive enzymes into the hemolymphatic system 11. Mansour, k. 1946. Source and fate ofthe zooxanthellae ofthe
(7). The entire branched tubular system associated with visceral massofTridacnae/ongata. Nature(Loud.) 158: 130.
the zooxanthellae communicates with the stomach via a 12. Fitt,\V. k.,and R. k.Trench. 1981. Spawning,development,and
single opening, which is visible in clams that are only a avaqluviisai)t.ioBnioolfBzuololxan1t61h:el2l1a3e-b2y35.Tridacna squamosa (Mollusca: Bi-
few weeks old (22), and which would appear to explain 13. Goreau, T. F., N. I. Goreau, andC. M. Yonge. 1973. On the uti-
the initial entry ofzooxanthellae into the mantle (12). lization of photosynthetic products from zooxanthellae and ofa
The definition ofthis tubular system has implications dissolved amino acid in Tridacna maxima (.elongata (Mollusca:
for our understanding ofthe nutritional relationship be- Bivalvia). / Zoo/. (Linnl) 169: 417-454.
14. Reid, R.G. B., P. V. Fankboner, and D. G. Brand. 1984. Studies
tween the giant clams and their zooxanthellae. It also re- onthephysiologyofthegiantclam Tridacnagigus Linne I.Feeding
veals that the giant clam-zooxanthellae symbiosis is ac- and digestion. Comp Biochem Physio/ 78A: 95-101.
tually likeotherknown invertebrate-algalsymbioses, being 15. Morton,B. 1978. Thediurnalrhythmandtheprocessesoffeeding
intimately associated with the digestive system of the and digestion in Tridacna crocea (Bivalvia: Tridacnidae). J. Zoo/.
(Loud.) 185: 371-387.
host (23). 16. Yonge,C. M. 1980. Functional morphology andevolution in the
tridacnidae(Mollusca: Bivalvia:Cardiacea). Rec .lust.Mils.33:735-
777.
Acknowledgments
17. Reid, R. G. B., P. V. Fankboner, and D. G. Brand. 1984. Studies
coWmmeentthsankonJ.thLisucpaasp,erD..WYeellaolwsoletesh,anakntdheA.AuRsetreaslifaonr 18. foFiuftnttc,hteiWop.nh.yKs.Ci,oolmGo/.g1yA.oBfiHtoehscelhigenimganat,PchavlnsadimoTlT.r7Ci.8daAWc:anat1s0go3in-g.a1s081L.9i9n2n.e UItIi.lKiizadtnieoyn
Centre for International Agricultural Research, Canberra, ofdissolved inorganic nutrients in growth and manculture ofthe
for financial assistance, and M. Dashorst for artwork. tridacnidclam Tridacnaderasa Aquacullnrc. in press.
19. Fitt, \V. k., C. R. Fisher, and R. K. Trench. 1986. Contribution
ofthe symbiotic dinoflagellate Symbiodinium microadriaticum to
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