Some Aspects of the Biology, Population Dynamics, and FunctionalMorphology of Musculista senhausia Benson (Bivalvia, Mytilidae)1

BRIAN MORTON 2

THE MYTILACEA with the Dreissenacea areperhaps the most specialized and most suc­cessful heteromyarian bivalves. Their simi­larity is probably not phylogenetic, as sug­gested by Purchon and Brown (1969), but isthe result of convergence and the adoptionof similar habits (Yonge and Campbell1968). Thus, the European dreissenidDreissena po/ymorpha and the Asianmytilid Limnoperna forlunei have bothadopted a mode of life involving the coloni­zation of hard surfaces in fresh waters (Mor­ton 1969a in press).

The evolution of the heteromyarian con­dition in these bivalve lines probably pro­ceeded from different isomyarian ancestors,with the neotenous retention of the larvalbyssus by the adult (Yonge 1962). This pro­cess, occurring in shallow coastal waters,must have enabled the ancestors ofmodern-day species initially to colonize theintertidal zone. Here the Mytilacea havebeen extremely successful and inhabit rockyshores the world over. Other mytil ids maybe found sublittorally, e.g., Crenella(Soot-Ryen 1955); in estuaries, e.g.,Xenoslrobus (Wilson 1967); in fresh waters,e.g., Limnoperna (Morton, in press); andeven as highly specialized commensals, e.g.,Fungiaeava (Goreau et al. 1969). The Dreis­senacea by contrast have not undergone thisextensive adaptive radiation and are re­stricted to estuaries, e.g., Congeria (Wolff1969) and fresh waters, e.g., Dreissena(Morton 1969a). Within their spheres of in­fluence, however, both of these bivalvelines cause problems as fouling organisms,e.g., Dreissena (Morton 196ge) and Mylilus(Haderlie 1968).

I Manuscript received 15 May 1973.2Department of Zoology, The University of Hong

Kong, Pokfulam Road, Hong Kong.

19

In Asia Museulisla senhausia Benson isalso a fouling organism (Kawahara 1961)and has been introduced into the UnitedStates (Smith 1944, Hanna 1966). In Chinathe species serves as a source of food andattempts have been made to culture themartificially (Cheung et al. 1962). Little in­formation, however, is available in the pub­lished literature on the biology of this ani­mal. Accordingly, a study has been under­taken of the functional morphology of theanimal and the biology and populationdynamics of a colony occurring in Tai TamBay, Hong Kong. The results of this inves­tigation are reported here.

DISTRIBUTION AND HABITS

Museu/iSla senhausia forms large col­onies in intertidal mud flats in many parts ofthe Far East. The type locality is Chusan,China. Cheung et al. (1962) reported it asbeing of very wide distribution in the west­ern Pacific and recorded it from the SouthChina Sea, the East China Sea, the YellowSea, and the Sea of Japan. It has been re­ported from Japan and Singapore by Kira(1961) and Chuang (1961), respectively.

In Tai Tam Bay, Hong Kong, the animalwas found in a dense colony at around mid­tide level in numbers of up to 2,500/m2

• Theanimal lies buried vertically in the mud, an­chored in position by a well-developed bys­sus. The byssus is also woven into a nest inwhich the animal is almost completely en­closed (Fig. 1). Such a habit is unusual in theBivalvia, although it occurs in a few othermytilid genera such as Modiolus andAmygdalum (Soot-Ryen 1955). The processof nest building in Musculus and Lima hasbeen reported upon by Merrill and Turner(1963). The similarity of the nest ofM useulisla to that ofMusculus suggests that

20 PACIFIC SCIENCE, Volume 28, January 1974

FIG. I. Mllsclliis/{/ sen!l{/lIsi{/. A diagrammatic rep­resentation of the animal in its nest in the mud. Thepositions of the inhalant and exhalant currents are alsoindicated.

they are constructed in a similar manner.The byssal threads are not attached to theshell but initially to sand grains, therebyforming an anchor. Thereafter, furtherbyssal threads are wrapped around the shelland attached to sand grains, thereby formingthe nest itself. Unlike the nest of Musculus(Merrill and Turner 1963), that ofM usculistahas a permanent posterior aperture.

The shores of Tai Tam are characteristi­cally composed of coarse sand. A few cen­timeters below the colony a similar coarsesand is found. Only the surface material iscomposed of fine mud. There was no evi­dence of empty shells of past generations ofM usculista, either bound up in the colony orin the underlying sand. The colony wasprobably a newly formed one and mucus­bound feces and pseudofeces produced bythe colony were likely responsible for thecreation of the mud flat. The byssal nest

serves as a matrix stabilizing the particles.In Hong Kong the same species has col­

onized wooden test panels suspended 3 to 4meters in the sea. Such animals did not builda nest as do their littoral counterparts. Sig­nificantly, Hanna (1966) found specimenswith no nests living attached to pilings in SanFrancisco Bay. Furthermore, the relatedM uscullls discors has been reported to be anintertidal species by Tebble (1966), whereasMerrill and Turner (1963) have reported it asliving sublittorally.

FUNCTIONAL MORPHOLOGY

Shell and Ligament

The shell ofM IIsculista senhausia (Fig. 2)is equivalve and heteromyarian. It is a dullolive green in color but above the umbonalkeel is delicately patterned with 15 to 16radiating brown stripes, originating at theumbo. One of the central stripes is typicallythicker than the others. Irregular verticalbands of brown pigment also pattern theshell. Internally the same patterning can bedistinguished. The blue-white nacre of theinterior is uniformly distributed.

The outer periostracallayer of the shell issmooth, shiny, and thin. The umbones aresubterminal and the dorsal ligamental mar­gin is straight or at most only slightlycurved. The ventral margin of the shell isslightly concave. The anterior region of theshell is somewhat inflated, rounded, and dis­tinctly crenulate. There are no hinge teethand no byssal notch.

The internal opisthodetic ligament (Fig.2B, L) commences anterior to a number ofweak crenulations reminiscent of the muchmore pronounced crenulations of Septifer(Yonge and Campbell 1968). The ligament iscomposed of two layers with similar stainingreactions to that of Mytilus edlllis (Trueman1950, Beedham 1958). The outer layer stainsred and the inner layer blue with bothMallory's triple stain and Masson's tri­chrome. Other mytilids-for example,Modiolus, Lithophaga (Yonge 1955),Sept(fer (Yonge and Campbell 1968), andLimnoperna (Morton, in press)- also pos-

Museu/ista senhallsia Benson-MoRTON

3mm~

2\

PBR (1) PBR (2)

FIG.2. MIIsCIIlis!a sellhallsia. External and internal views of A, the right shell valve and B, the left shell valve,respectively.

ABBREVIATIONS USED IN FIGS. 2,4,5,6, AND 7: A, a cell layer of style sac; AA, anterior adductor muscle;ABR, anterior byssal retractor muscle; A P, appendix; AU, auricle; B, byssus; B" B, cell layer (minor typhlosolelof style sac; BG, byssal gland; BS, branchial septum; C, C cell layer of style sac; CI, cilia; CS, crystalline style; 0,o cell layer of style sac; DO, digestive diverticula; DOD 1-5, ducts of the digestive diverticula opening into thestomach; DH, dorsal hood; DHT, dorsal hood tract; OS, dorsal septum; ES, exhalant siphon; F, foot; Fe,food-sorting cecum; GS, gastric shield; G U, gutter of style sac; lA, inhalant aperture; 10, innerdemibranch; IG,intestinal groove of major typhlosole; IP, inner labial palp; L, ligament; LP, left pouch; LT, left duct tract; M F,point of ventral mantle fusion; MG, midgut; MIG, intestinal groove of minor typhlosole; MM, mantle margin;MT, minor typhlosole; 0, oesophagus; 00, outer demibranch; OP, outer labial palp; OY, ovary; PA, posterioradductor muscle; PBR (I) (2), posterior byssal retractor muscles; PL, pallial line; PPR, posterior pedal retractormuscle; R, rectum; RP, right pouch; RT, right duct tract; SP, sensory papillae; SS, style sac; T, major typhlosole;U, umbo; US, unsolidified style material; Y, ventricle.

22 PACIFIC SCIENCE, Volume 28, January 1974

sess a ligament with a similar structure; it issignificant that in all of these genera and inMuseulista senhausia the periostracum ex­tends over the ligament. Such an ar­rangement must, therefore, be typical of theMytilacea in general.

The overall dimensions of the shell areregular for the population of M. senhausiasampled from Tai Tam Bay, a fact which ismost clearly demonstrated by the ratio ofwidth: height: length, which is: 1 : 1.28 ±0.15 : 2.65 ± 0.35. The ratios of shell width:length, shell height: length and shell width:height have been calculated as being 0.38 ±0.04, 0.49 ± 0.04, and 0.78 ± 0.08, respec­tively.

The shell of M. Senhausia is thin as com­pared with a number of other Hong Kongmytilids from a variety of habitats (Table 1).In relative terms the shell is only one-halfthe thickness of Limnoperna lortunei, aninhabitant of fresh waters, and only one­quarter of the thickness of Septilerbiloeularis, an inhabitant of exposed rockyshores.

Mantle

Mantle fusions are of the inner folds onlyand, thus, are of type A (Yonge 1957). Man­tle fusions occur dorsally above the exhalantsiphon and between the exhalant siphon andthe inhalant aperture. The mantle also fusesanteroventrally and here an elongate adduc­tor muscle (AA) links the two valves.

The outer mantle fold is small and theperiostracum that is secreted by the innersurface of the outer mantle fold is composed

of three layers. The outer layer achieves athicknes s of 7.5 I.t and s ta ins pink inMallory's triple stain and Masson's tri­chrome. The middle layer is only 5 I.t inthickness and is composed of a yellowishsubstance that is unaffected by the routinestains used in this study. An inner laminatedlayer ultimately achieves a thickness of25 I.tand stains blue with Masson's andMallory'S stains. The structure of theperiostracum and of the epithelium that se­cretes the component layers bears a closesimilarity to those possessed by Mytilus(Beedham 1958) and Limnoperna (Morton,in press).

The dorsal region of each mantle lobecontains, as in other mytilids, much of thegonadial tissue. The sexes are separate, andspawning in the population inhabiting TaiTam Bay occurs from January to March orApril. Spat were first observed in the popu­lation in mid-January (Fig. 3). In northernChina the species breeds in July and August(Cheung et al. 1962).

Siphons

Only the siphons protrude through themud to the water above (Fig. 1). The exhal­ant siphon (Fig. 4, ES) is formed by tissuefusion between the inner mantle folds only,this being type A (ii) (Yonge 1957). The in­halent aperture (IA) is not separated fromthe pedal/byssal aperture by mantle fusionsand thus cannot be regarded as a siphon.The exhalant siphon is devoid of tentacles,though the inhalant aperture bears on eachlobe a number of somewhat branched papil-

TABLE I

A COMPARISON OF THE THICKNESSES OF THE SHELLS OF FOUR SPECIES

OF HONG KONG MYTILIDS

SPECIES MAXIMUM RECORDED MAXIMUMSHELLSHELL LENGTH THICKNESS

(MM) (MM)

RATIO OF SHELLTHICKNESS: SHELL

LENGTH(%)

MIISClllista senlwlIsi(/ BensonLimnopern(/ forlllnei (Dunker)Brachidonles (/Ir(/Ills LischkeSeplifer biloclliaris Linnaeus

28371658

0.250.650.352.05

0.971.702.273.53

Muscu/ista senhausia Benson-MoRTON 23

DECEMBER 1971 SAMPLE SIZE: 1012

~1~~l\--,.-----,---,

SAMPLE SIZE=790

SAMPLE SIZE=851

SAMPLE SIZE: 533

::1'''''"''' '"20

15

10

5

SAMPLE SIZE:466

~,

1972 SAMPLE SIZE:821

20 AUGUST 1972

::L----.-------r"~=---------.----I ----,--------,

::100'0"" '''' ...~"" ~,,<.."

::L, -,--,--..ALr I I

5 10 15 20 25 30 35 40

SAMPLE SIZE:7Bl

SAMPLE SIZE:643

SAMPLE SIZE=691

20 25

!\

1510

:n~~T'_Y_19_7T2--,=J,-~-,__,--,=S~AM_,PL_E_S_IZ,E_:_9_7-,1

FIG. 3. Length-frequency histograms showing the composition of monthly samples of the population ofMusculisla senhausia at Tai Tam Bay. Open histograms represent live animals, black histograms empty shells.The x axis represents shell length in millimeters; the y axis represents the number of animals of a given sizeexpressed as a percentage of the total sample.

FIG.4. MllsclI/isla senhallsia. A posterior view ofthe animal when actively filtering clean seawater. (Seelegend for Fig. 2 for abbreviations.)

24

ES

BS

IA

R

ES

BS --..;p.;""-i-";;;

PACIFIC SCIENCE, Volume 28, January 1974

lae (SP). Each mantle lobe is cream coloredand patterned by radiating brown bandswith small patches of white pigment. This isparticularly noticeable around the inhalantaperture. A large branchial septum (BS) re­stricts the size of the inhalant aperture and(Fig. 5, BS) connects the ctenidia (ID, aD)to the mantle at the point of fusion separat­ing the exhalant siphon from the inhalantaperture and, thus, the suprabranchial from

SP the infrabranchial chambers.

Musculature

The anterior adductor muscle (Fig. 5,AA) is relatively large and elongate and islocated on the anteroventral floor of theshell valves. It is thus in a similar position tothat of Limnoperna (Morton, in press),.X enostrobus (Wilson 1967), and Mytilus(White 1937). The anterior byssal retractormuscles (ABR) are very small and originateon the anterodorsal roof of the shell valvejust underneath the umbo (U). The posterioradductor muscle (PA) is approximately

PBR(2) 5S

5mm

----u

OP

F

FIG. 5. MllsclI/isla senhllllsia. The organs of the mantle cavity. The right shell valve, mantle lobe ctenidium,and labial palps have been removed. (See legend for Fig. 2 for abbreviations.)

Museu/ista senhausia Benson-MoRTON

twice the size of the anterior adductor mus­cle and is located posterodorsally. Theposterior byssal retractor muscle is largeand is divided into two component units(PBR[I], PBR[2]) as in Limnoperna(Morton, in press) and X enostrobus ineon­stans (Wilson 1967). There is a small pos­terior pedal retractor (PPR).

Ciliary Currents of the Mantle,Visceral Mass, and Foot

The ciliary currents of the mantle, vis­ceral mass, and foot are all rejectory in na­ture. Those of the mantle pass unwantedmaterial posteriorly to be ejected via theinhalant aperture (Fig. 5, IA). Such materialis not ejected by the rapid phasic adductionof the adductor muscles as in many eulamel­libranchs but by cilia passing it dorsally tobe finally ejected by the outward flow ofwater from the exhalant siphon (ES). In thisrespect Musculista senhausia is very similarto Limnoperna (Morton, in press) andAdu/a(Fankboner 1971).

The ciliary currents of the visceral masssimilarly pass unwanted material poste­riorly, where it accumulates at a point im­mediately posterior to the byssal gland(BG). From this point it falls on to the man­tle for rejection by the mantle cilia.

The foot (F) is long, lanceolate, and veryactive. The ciliary currents on the surface ofthe foot pass material dorsally. The footconstructs the nest.

Ctenidia and Labial Palps

The ctenidia comprise two somewhatsubequal demibranchs of which the outer(Fig. 5, aD) is the longer. They are not aslong as those of Limnoperna (Morton, inpress). The ctenidia are flat, homorhabdic,and filibranchiate; and at their dorsal edgesthe ascending lamellae of both the inner andouter demibranchs are attached to the vis­ceral mass and to the junction of the visceralmass and mantle, respectively, by ciliaryfusions. Filamentary cohesion is achieved,as in all mytilids, by ciliary discs. The ciliarycurrents of the ctenidia are of type B(I) (At­kins 1937), in which acceptance tracts lie in

25

the ventral marginal food grooves of bothdemibranchs, the ctenidial axis, and at thejunctions of the dorsal edges of the ascend­ing lamellae of the inner and outer demi­branchs.

The ctenidialllabial palp junction is oftype I (Stasek 1963), and the mechanism bywhich material arriving at the ctenidial ter­minii of the food grooves is sorted is essen­tially the same as that described by Morton(in press) for Limnoperna. In Limnoperna,however, the anterior filaments of the innerdemibranch are shorter than are those of theouter demibranch. In Museu/ista the fila­ments of the outer demibranch are the short­er. However, this modification fulfills thesame function in both species. Material ar­riving at the labial palps on the crests of bothventral marginal food grooves is thus pre­sented to the sorting surfaces of both labialpalps. Such a modification thereby dramati­cally increases the sorting potential of thelabial palps.

As noted by Fankboner (1971) for Adu/a,the outer demibranch of Muscu/istasenhausia is some 4 to 5 filaments shorteranteriorly than is the inner demibranch.This adaptation, apparently characteristicof all mytilids, further enhances the sortingmechanism described above.

The labial palps of M. senhausia arecomparatively large. Other burrowingspecies living in soft mud, such as membersof the Tellinacea (Yonge 1949), also possesslarge labial palps. The ciliary currents of thelabial palps bear a close resemblance tothose of Adula (Fankboner 1971) and thuscan be considered to be of the typical mytilidtype.

The lips of the mouth are large and fleshy;they possess ciliary currents similar to thoseof Dreissena polymorpha (Morton 1969a)and serve a rejectory function. They can beclassified as "simple" (Bernard 1972).

Alimentary Canal

The stomach is located under the an­terodorsal margin of the shell and is sur­rounded by the dark digestive diverticula(Fig. 5, DD).

26 PACIFIC SCIENCE, Volume 28, January 1974

The oesophagus enters at the anterior endof the stomach, whilst from the posteriorend arises the midgut (MG) and a separatestyle sac (SS). The style sac passes back­ward between the posterior byssal retractormuscles (PBR [1] [2]) and terminates dorsalto the posterior adductor muscle (PA). Themidgut does not, as it does in other mytilids,e.g., Mytilus (White 1937) and Limnoperna(Morton, in press), pass between the byssalretractors conjoined to the style sac. Beforereaching them the midgut turns upon itself,loops on the right side of the body, passesunder the posterior edge of the stomach, andthe.n penetrates the ventricle (V) of theheart, extending posteriorly as the rectum(R) and terminating in an anus posterior tothe posterior adductor muscle.

The style sac when seen in transverse sec­tion (Fig. 6) is very different from that of thetypical mytilid as exemplified by Mytilus

B, 0

FIG.6. Musculis/a sell!lausia. A transverse sectionthrough the style sac with crystalline style showing thedistribution of the different epithelia. (See legend forFig. 2 for abbreviations.)

Galloprol'incialis (Giusti 1971). In Mytilusthe style sac and midgut are conjoined but inMusculista senhausia the style sac is sepa­rated by a fusion of the minor typhlosolewith the epithelium of the midgut. The majortyphlosole of the stomach passes directlyinto the midgut. Such an arrangement re­sults in a style sac with a structure that issimilar to, but convergent with, the separatestyle sac of many of the Eulamellibranchia,e.g., Dreissena polymorpha (MortonI969a ). Kato and Kubomura (1954) have de­scribed the structure of various bivalve stylesacs and recognize that the epithelium con­stituting the sac is divisible into a number ofzones which they have termed A, B, and C.A further zone, 0, was recognized by Mor­ton (1969a) and regarded as the secretoryregion of the major typhlosole. InMuscltlista senhausia the same zones can berecognized, although because the typh­losole is the minor typhlosole the term B1has been used. The cells of the A cell layerare 25 J.L tall and possess a dense ciliaryborder oflength 15 J.L. The cells of the B1 celllayer are 70 J.L tall with a somewhat lessdense and shorter ciliary border between 12to 14 J.L tall. The cells of the C cell layer are20 J.L tall with short (5 J.L) cilia arranged indistinct groups. Internally the ciliary root­lets are discernible. The cells of the 0 celllayer are 12 J.L tall and possess cilia 10 J.L long.

The stomach of M. senhausia (Fig. 7) iselongate and bears a close resemblance tothe stomachs of other mytilids, e.g.,Lithophaga (Purchon 1957, Dinamani1967), Mytilus (Graham 1949, Reid 1965),Perna (Dinamani 1967),Adula (Frankboner1971), and Limnoperna (Morton, in press)and thus belongs to type 111 (the Gastrotri­teia) and section I of the stomach typeselucidated by Purchon (1957) and Dinamani(1967), respectively. The nomenclaturalsystems of Purchon (1957) and Reid (1965)are adopted here.

The structure of the stomach of variousmembers of the Mytilacea seems to be re­markably constant and in this descriptiononly those points in which MlIsclilistasenhausia differs from the others will becommented upon. The stomach of M. sen­hallsia possesses a distinct appendix, as

Museulista senhausia Benson-MoRTON 27

lmm

FIG. 7. Muscu/isla senhausia. The interior of the stomach viewed from the right side after having been openedby a horizontal incision. The ciliary currents of the stomach (dark arrows) and of the food sorting cecum (brokenarrows) are indicated. (See legend for Fig. 2 for abbreviations.)

does Mytilus (Reid 1965). In other mytilidsthis structure is not so well developed (Pur­chon 1957) and may be vestigial or absent.Lying next to the appendix are a group ofducts which communicate with the digestivediverticula (DOD 2) located at the termina­tion of what Reid (1965) has termed the rightduct tract (RT). On the left side of thestomach the left duct tract (LT) terminatesin the ducts of the digestive diverticula(DOD 3, DOD 4) constituting the leftpouch (LP) into which a spur of the gastricshield (GS) is located. It would seemreasonable to call the ducts on the right sideof the body, the right pouch (RP). As­sociated with the right duct tract are otherducts of the digestive diverticula (DOD 1,DOD 5) which are also present in othermytilids, e.g., Lithophaga (Purchon 1957)and Myti/lls (Reid 1965), although in Adll/a(Fankboner 1971) and Limnoperna(Morton, in press) some of these ducts(DOD 5) are to be found just inside the

food-sorting cecum. In Museulistasenhausia the food-sorting cecum (Fe) issmall and terminates under the left pouch.In other mytilids it is long and in such gen­era, e.g., Limnoperna (Morton, in press), itis thought that a long cecum gives greaterefficiency to the processes of collection andsorting offood material. The ciliary tracts ofthe food-sorting cecum are similar to thosedescribed for Mytilus (Reid 1965) andLimnoperna (Morton, in press).

POPULATION DYNAMICS

It has been shown earlier that the shelldimensions of Museu/ista senhausia are re­latively constant. It was, therefore, decidedto attempt to establish the number of agegroupings within the population by means ofa length-frequency histogram. Such histo­grams have been used successfully in thepast for the analysis of populations of othermolluscs, e.g., Monodonta lineata (Desai

28 PACIFIC SCIENCE, Volume 28, January 1974

1966), Monacha cantiana (Chatfield 1968),and Dreissena polymorpha (Morton I969b ).Accordingly, a large sample of animals wascollected from Tai Tam Bay in earlyNovember 1971 and the shells were mea­sured along their greatest length to thenearest I mm (Fig. 3). In November thepopulation comprised a single age groupingof mean length 22 mm. Such a result findsaccord with an earlier conclusion that thecolony was a new one, this conclusion hav­ing been reached because of an absence ofempty shells within the population. Similarsamples of 500 to 1,000 animals collected inthe first weeks of December 1971 andJanuary 1972 showed a similar populationstructure. By mid-January 1972 a spatfallhad occurred on the fringes of the existingcolony and young individuals had alreadyestablished themselves in nests. In subse­quent monthly samples the new age groupassumed increasing importance. In thesummer of 1972 they grew very rapidly.Their parents grew at a slower rate. By Sep­tember 1972 the primary adult age group hadall but died out. This was evidenced by theoccurrence of very many empty shellswithin the population. In early October 1972it was found that the entire population haddied. The shell of Musculista senhausia isextremely thin, so that even after such ashort period of time most of the empty shellshad been broken up. However, a small sam­ple of intact valves was collected and whenmeasured revealed that the young animalshad died when 25 mm in mean length.Perhaps significantly the primary adultpopulation had also died when approxi­mately this size earlier in August to Sep­tember.

By separately plotting the mean length ofthe age groups within the population (Fig. 8)as revealed by the length~frequency histo­gram, one can see that the primary adult agegrouping did not grow between the monthsof November 1971 and May 1972. They didgrow, by approximately 4 mm, between ~he

months ofJune to August 1972 but then diedout. By contrast the young age groupachieved a high rate of growth in the earlymonths of their life-January to March1972-but slowed down somewhat in

30

•25 •00

0 0 000 0 0 aa

E 20 0e:;

II>- I(9n 0

0

a(f) 10a a

a0

5

N 0 J F M A M J J A S 01971 1972 MONTHS

FIG. 8. Average length of each age group in themonthly samples of Muscu/isla senhausia. Open cir­cles indicate live animals, black circles empty shells.

March. However, in April the animalsstarted growing again and from then untilOctober 1972 when they had died they grewfrom 9 mm to 25 mm in length. Theyachieved in 9 months, i.e., from spatfall todeath, a size which it had taken theirparents-if one assumes that the time ~f

spatfall for this generation was approxI­mately the same as that of their offspring,i.e., January-20 months to achieve. Theadult population had bred after approxi­mately 1 year of life to produce the youngergeneration; the young generation, however,died before becoming sexually mature andthis, together with the death of the primarygeneration, resulted in the death of the en­tire colony. This occurred in October 1972.By mid-October that area of beach previ­ously occupied by the M. senhausia colonyhad virtually returned to an ecological con­dition similar to that of other neighboringunaffected beaches.

DISCUSSION

The Mytilacea exhibit a wide degree ofadaptive radiation and the more successful

Musculista senhausia Benson-MoRTON

genera such as Mytilus and Modiolus are tobe found on many of the shores the worldover. This habit can be related to the evolu­tion of the heteromyarian condition. Othermytilids such as Crenella are sublittoraland,judged by their shape, infaunal (Tebble1966). Perhaps bridging the gap betweenthese two extremes are such animals asMusculus discors and Musculista sen­hausia. Musculus discors is found livingintertidally amongst algae (Tebble 1966), al­though Merrill and Turner (1963) found thesame species living sublittorally. SimilarlyHanna (1966) found Musculista senhausiawithout a nest living attached to pilings andthis species has also been found attached totest blocks hung 3 to 4 meters in the sea inHong Kong, again without a nest. LikeMusculus discors, however, Musculistasenhausia also occurs intertidally and formslarge colonies in estuaries and shelteredbays. The colony inhabiting Tai Tam Bay,Hong Kong, formed a mat developed by thenest-building activities of the colony mem­bers. In so do-ing they also bound them­selves to sand grains and, when in largeenough numbers, to the nests of each other.The nest completely encloses the animal ex­cept for the posterior margin of the shellwhere the inhalant aperture and the exhalantsiphon open to the water above. The gre­garious habit of M. senhausia results in thecolony accumulating around it a fine mudderived from the feces and pseudofeces.Cheung et al. (1962) have suggested that theformation and expansion of a colonydramatically alters the fauna of a sandyshore. This was true in Tai Tam Bay wherethe colony (Fig. 3) was judged to be newlyformed. Typical sandy shore bivalves, e.g.,Cyclina orientalis, Paphia euglypta, andmore importantly Anomalocardia squa­mosa, apparently had been unable to com­pete with the growing Musculista sen­hausia colony. Only empty shells of thesespecies were found. Cheung et al. (1962)report that the layer of M. senhausiaeffectively prevents other bivalves fromprojecting their siphons through to thewater above.

The very wide distribution of this species(Cheung et al. 1962) and its occurrence in a

29

variety of both intertidal and sublittoralhabitats would seem to suggest that it is anopportunist bivalve, settling whenever andwherever it can. Once settled, the animalrelies upon the production ofa large numberof eggs (Cheung et al. 1962) and a rapid rateof growth to colonize quickly all availablesuitable sites.

In 1971 the colony comprised a single agegrouping. A further spatfall, which occurredin January to April 1972, settled on the sea­ward periphery of the existing colony. Sucha habit is almost certainly the way in whichsuch colonies are enlarged. The second agegroup assumed increasing importancewithin the population during the course of1972 and, after the adult age group had diedout in August, were the only age group left.By October 1972, however, they too haddied. The death of the colony is attributableto the extraordinarily fast rate of growthexhibited by the young generation in 1972,because both adults and young died beforeproducing a further generation. Cheung etal. (1962) record the maximum shell lengthof animals they examined as 29 mm. Such afigure falls within the normal distributionpattern of the age groupings elucidated inthis study as do the maximum figures forshell length of this species recorded byHanna (1966).

Musculista senhausia shows a number ofadaptations to its peculiar mode oflife. Mostimportant of these is the byssus which, aswell as acting as an anchor as in more con­ventional heteromyarians such as the Pin­nidae (Yonge 1953), is also woven into anenclosing nest.

Other related mytilids also possess thishabit: Musculus (Merrill and Turner 1963),Modiolus, and Amygdalum (Soot-Ryen1955), as well as the unrelated Lima hians.In Lima, the nest serves a protective func­tion. In Musculus discors, which has a thickshell, Merrill and Turner (1963) have sug­gested that the nest principally protects theeggs which are laid inside the nest.Musculista senhausia does not lay eggswithin its nest; they are planktonic (Cheunget al. 1962). Compared with such species asSeptzfer bilocularis and Brachidontes at­ratus, Musculista senhausia has a very thin

30 PACIFIC SCIENCE, Volume 28, January 1974

shell (Table 1). The shell is also relativelymuch thinner than that of Limnoperna for­tunei, an inhabitant of fresh waters wherethe calcium content is typically much lowerthan that of the sea. It would thus seem thatthe nest thatMuseulista senhausia weaves isessentially a protective device for the adult.The nest serves a subsidiary function inkeeping sediment out of the mantle cavityand thus has contributed to the successfulexploitation of the soft shore environmentby this species. The organs of the mantlecavity are concerned with the processing oflarge currents of particulate material. As aconsequence, the rejectory tracts are welldeveloped. The branchial septum serves asa valve regulating the intake of material,whilst the labial palps and foot are large andthe foot, as well as building the nest, alsoserves to keep the mantle cavity (andperhaps the nest) clean. The ctenidia arerelatively small. Museu/ista is thus adaptedin a similar manner to other lamellibranchssuch as the Tellinacea (Yonge 1949) that arecharacteristically found in muddy habitats.

Though the stomach is of the typical my­tilid type, it, too, is modified. The food­sorting cecum is small. In the Tellinacea,also, the sorting areas of the stomach arereduced (Yonge 1949, Purchon 1960). Alsoas in the Tellinacea there is a distinct stom­ach appendix. It would seem that the stom­ach is adapted to the rapid processing of anabundant food supply rather than with thesorting and abstraction of all available foodmaterial.

A major difference between M. senhausiaand the other mytilids studied (e.g., by Di­namani 1967) is that in the former the stylesac is separate from the midgut. In the con­joined style sac and midgut of the typicalmytilid such as Myti/us galloprol'ineia/is(Giusti 1971), both major and minor typh­losoles are present. In Museulista sen­hausia the major typhlosole passes intothe midgut whilst the minor typhlosolepenetrates the style sac. The style sac is thussimilar to, but convergent with, the stylesac of some eulamellibranchs such asDreissena po/ymorpha (Morton 1969a). Inthis species the typhlosole of the style sac isa portion of the majortyphlosole, whereas in

Museu/ista senhausia it is the minor typh­losole. In other respects the style sac is simi­lar to that of Dreissena. The separate stylesac serves to keep the large amounts of de­trital material passing through the gut awayfrom the style and thus prevents it from re­turning to the stomach.

Museulista senhausia possesses anumber of characters that are intermediatebetween primitive and highly specializedmytilids. The anterior border of the shell isinflated and distinctly crenulate. Weak cre­nulations, as in Sept({er (Yonge and Camp­bell 1968), are also present just posterior tothe ligament. Such a condition would seemto be intermediate between the crenulatedisomyarian shell of Crenella (Tebble 1961)and the noncrenulated extreme aniso­myarian shell of more typical mytilids.

The anterior byssal retractor is small andis located almost directly under the umbo.Such a position is intermediate between thecondition encountered in Museu/us diseors(Tebble 1961) where the anterior byssal re­tractor is located anteriorly and the condi­tion in more extreme genera such asX enostrobus (Wilson 1967) where the pointof attachment of the muscle is on the pos­terior border of the shell. The umbo ofMuscu/ista senhausia is subterminal andthus represents a further example of the in­termediate condition exhibited by thisspecies with respect to the extremes seen inCrenella (Tebble 1966), Myti/us (White1937), Xenostrobus (Wilson 1967), andSeptz{er (Yonge and Campbell 1968). InMuseu/ista senhausia the posterior byssalretractor is divided into two blocks. Thissituation also exists in Limnoperna (Mor­ton, in press) and in X enostrobus ineonstans(Wilson 1967). Such a development canperhaps be related to the elongation of theposterior border of the shell in theMytilacea. Significantly, in Myti/us edu/is(White 1937), which displays extremeheteromyarianism, the posterior byssal re­tractor is broken up into three units; whilstin Modio/us the posterior byssal retractor isdivided into many more units (Yonge 1953).

Though in itself highly specializedMuseu/ista senhausia may recall an inter­mediate condition in the evolution of the

Museu/ista senhausia Benson-MoRTON

heteromyarian condition in the Mytilacea.Significantly, the evolutionary steps envis­aged as having occurred in the Dreissenacea(Morton 1970) find a number of parallelswith the condition exhibited by M.senhausia. Because of the large pallial sinusto the shell, Morton (1970) has suggestedthat the fossil dreissenid Dreissenomyaaperta was byssally attached and yet livedan infaunal life. The similarities that existbetween Dreissenomya and Museulistasenhausia are attributable to the indepen­dent evolution of the heteromyarian condi­tion inthese two bivalve phyiogenies (Yongeand Campbell 1968). However, the occur­rence ofM useu/ista senhausia living in inter­tidal mud may attest to the similarity of theevolutionary process in the Dreissenaceaand Mytilacea and perhaps points to some ofthe changes that have occurred in the evolu­tion of the Mytilacea, namely, that theheteromyarian condition was evolved be­fore the successful exploitation of rockyshores by this group.

SUMMARY

The mytilid Museulista senhausiaBenson forms large colonies in intertidalmud flats in sheltered bays in the Far East.

M. senhausia is considered to be an op­portunist bivalve with a high reproductivecapacity, a fast rate ofgrowth, and an abilityto colonize other habitats such as hard sub­littoral surfaces. When occurring interti­dally it dramatically affects the ecology ofthe shore. The mud flat is created and main­tained as a result of (I) the deposition offeces and pseudofeces and (2) the animals'habit of building a nest which stabilizes thesurface mud.

The nest is woven from byssal threadsand serves a number of functions: (I) it pro­tects the very thin shell; (2) it prevents theentry of terrigenous material into the mantlecavity; and (3) it anchors the animal into themud.

The animal also possesses a number ofother morphological adaptations that suit itfor an infaunal life. These are: (I) a largebranchial septum acts as a valve controllingthe inflow oflarge particles into the inhalant

31

apertu re; (2) the ctenidia are relativelyshort; (3) the labial palps are large; (4) thefood-sorting cecum of the stomach is small;and (5) the style sac is uniquely, for amytilid, separate from the midgut.

Other anatomical characters, particularlyof the shell, suggest thatM. senhausia mayrecall a transitional stage in the evolution ofthe heteromyarian condition in theMytilacea, and that the heteromyariancondition arose in the Mytilacea before thecolonization of hard surfaces was achieved.

I ACKNOWLEDGMENTS

During this investigation technical assis­tance was obtained from Mr. D. Chi whosectioned and stained the material here re­ported upon and from Mrs. D. W. Kwanwho arranged for the monthly measurementof the samples.

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Museulisla senhausia Benson-MoRTON

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