Some Aspects of the Biology, Population Dynamics, and Functional Morphology of Musculista senhausia Benson (, ) 1

BRIAN MORTON 2

THE MYTILACEA with the Dreissenacea are In Asia Museulisla senhausia Benson is perhaps the most specialized and most suc­ also a fouling organism (Kawahara 1961) cessful heteromyarian bivalves. Their simi­ and has been introduced into the United larity is probably not phylogenetic, as sug­ States (Smith 1944, Hanna 1966). In China gested by Purchon and Brown (1969), but is the species serves as a source of food and the result of convergence and the adoption attempts have been made to culture them of similar habits (Yonge and Campbell artificially (Cheung et al. 1962). Little in­ 1968). Thus, the European dreissenid formation, however, is available in the pub­ Dreissena po/ymorpha and the Asian lished literature on the biology of this ani­ mytilid Limnoperna forlunei have both mal. Accordingly, a study has been under­ adopted a mode of life involving the coloni­ taken of the functional morphology of the zation of hard surfaces in fresh waters (Mor­ and the biology and population ton 1969a in press). dynamics of a colony occurring in Tai Tam The evolution of the heteromyarian con­ Bay, Hong Kong. The results of this inves­ dition in these bivalve lines probably pro­ tigation are reported here. ceeded from different isomyarian ancestors, with the neotenous retention of the larval byssus by the adult (Yonge 1962). This pro­ DISTRIBUTION AND HABITS cess, occurring in shallow coastal waters, must have enabled the ancestors of Museu/iSla senhausia forms large col­ modern-day species initially to colonize the onies in intertidal mud flats in many parts of intertidal zone. Here the Mytilacea have the Far East. The type locality is Chusan, been extremely successful and inhabit rocky China. Cheung et al. (1962) reported it as shores the world over. Other mytilids may being of very wide distribution in the west­ be found sublittorally, e.g., Crenella ern Pacific and recorded it from the South (Soot-Ryen 1955); in estuaries, e.g., China Sea, the East China Sea, the Yellow Xenoslrobus (Wilson 1967); in fresh waters, Sea, and the Sea of Japan. It has been re­ e.g., Limnoperna (Morton, in press); and ported from Japan and Singapore by Kira even as highly specialized commensals, e.g., (1961) and Chuang (1961), respectively. Fungiaeava (Goreau et al. 1969). The Dreis­ In Tai Tam Bay, Hong Kong, the animal senacea by contrast have not undergone this was found in a dense colony at around mid­ 2 extensive adaptive radiation and are re­ tide level in numbers of up to 2,500/m • The stricted to estuaries, e.g., Congeria (Wolff animal lies buried vertically in the mud, an­ 1969) and fresh waters, e.g., Dreissena chored in position by a well-developed bys­ (Morton 1969a). Within their spheres of in­ sus. The byssus is also woven into a nest in fluence, however, both of these bivalve which the animal is almost completely en­ lines cause problems as fouling organisms, closed (Fig. 1). Such a habit is unusual in the e.g., Dreissena (Morton 196ge) and Mylilus Bivalvia, although it occurs in a few other (Haderlie 1968). mytilid genera such as Modiolus and Amygdalum (Soot-Ryen 1955). The process of nest building in and Lima has been reported upon by Merrill and Turner I Manuscript received 15 May 1973. 2Department of Zoology, The University of Hong (1963). The similarity of the nest of Kong, Pokfulam Road, Hong Kong. M useulisla to that ofMusculus suggests that

19 20 PACIFIC SCIENCE, Volume 28, January 1974

serves as a matrix stabilizing the particles. In Hong Kong the same species has col­ onized wooden test panels suspended 3 to 4 meters in the sea. Such did not build a nest as do their littoral counterparts. Sig­ nificantly, Hanna (1966) found specimens with no nests living attached to pilings in San Francisco Bay. Furthermore, the related M uscullls discors has been reported to be an intertidal species by Tebble (1966), whereas Merrill and Turner (1963) have reported it as living sublittorally.

FUNCTIONAL MORPHOLOGY

Shell and Ligament The shell ofM IIsculista senhausia (Fig. 2) is equivalve and heteromyarian. It is a dull olive green in color but above the umbonal keel is delicately patterned with 15 to 16 radiating brown stripes, originating at the umbo. One ofthe central stripes is typically thicker than the others. Irregular vertical bands of brown pigment also pattern the FIG. I. Mllsclliis/{/ sen!l{/lIsi{/. A diagrammatic rep­ shell. Internally the same patterning can be resentation of the animal in its nest in the mud. The distinguished. The blue-white nacre of the positions of the inhalant and exhalant currents are also interior is uniformly distributed. indicated. The outer periostracallayer of the shell is smooth, shiny, and thin. The umbones are they are constructed in a similar manner. subterminal and the dorsal ligamental mar­ The byssal threads are not attached to the gin is straight or at most only slightly shell but initially to sand grains, thereby curved. The ventral margin of the shell is forming an anchor. Thereafter, further slightly concave. The anterior region of the byssal threads are wrapped around the shell shell is somewhat inflated, rounded, and dis­ and attached to sand grains, thereby forming tinctly crenulate. There are no hinge teeth the nest itself. Unlike the nest of Musculus and no byssal notch. (Merrill and Turner 1963), that ofMusculista The internal opisthodetic ligament (Fig. has a permanent posterior aperture. 2B, L) commences anterior to a number of The shores of Tai Tam are characteristi­ weak crenulations reminiscent of the much cally composed of coarse sand. A few cen­ more pronounced crenulations of Septifer timeters below the colony a similar coarse (Yonge and Campbell 1968). The ligament is sand is found. Only the surface material is composed oftwo layers with similar staining composed of fine mud. There was no evi­ reactions to that ofMytilus edlllis (Trueman dence of empty shells of past generations of 1950, Beedham 1958). The outer layer stains M usculista, either bound up in the colony or red and the inner layer blue with both in the underlying sand. The colony was Mallory's triple stain and Masson's tri­ probably a newly formed one and mucus­ chrome. Other mytilids-for example, bound feces and pseudofeces produced by Modiolus, Lithophaga (Yonge 1955), the colony were likely responsible for the Sept(fer (Yonge and Campbell 1968), and creation of the mud flat. The byssal nest Limnoperna (Morton, in press)- also pos- Museu/ista senhallsia Benson-MoRTON 2\

3mm~

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 typhlosolel ofstyle sac; BG, byssal gland; BS, branchial septum; C, C cell layer ofstyle 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 the stomach; 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 ofstyle 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, posterior adductor muscle; PBR (I) (2), posterior byssal retractor muscles; PL, pallial line; PPR, posterior pedal retractor muscle; 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 is of three layers. The outer layer achieves a significant that in all of these genera and in thickness of 7.5 I.t and stains pink in Museulista senhausia the periostracum ex­ Mallory's triple stain and Masson's tri­ tends over the ligament. Such an ar­ chrome. The middle layer is only 5 I.t in rangement must, therefore, be typical ofthe thickness and is composed of a yellowish Mytilacea in general. substance that is unaffected by the routine The overall dimensions of the shell are stains used in this study. An inner laminated regular for the population of M. senhausia layer ultimately achieves a thickness of25 I.t sampled from Tai Tam Bay, a fact which is and stains blue with Masson's and most clearly demonstrated by the ratio of Mallory'S stains. The structure of the width: height: length, which is: 1 : 1.28 ± periostracum and of the epithelium that se­ 0.15 : 2.65 ± 0.35. The ratios of shell width: cretes the component layers bears a close length, shell height: length and shell width: similarity to those possessed by Mytilus height have been calculated as being 0.38 ± (Beedham 1958) and Limnoperna (Morton, 0.04, 0.49 ± 0.04, and 0.78 ± 0.08, respec­ in press). tively. The dorsal region of each mantle lobe The shell ofM. Senhausia is thin as com­ contains, as in other mytilids, much of the pared with a number of other Hong Kong gonadial tissue. The sexes are separate, and mytilids from a variety ofhabitats (Table 1). spawning in the population inhabiting Tai In relative terms the shell is only one-half Tam Bay occurs from January to March or the thickness of Limnoperna lortunei, an April. Spat were first observed in the popu­ inhabitant of fresh waters, and only one­ lation in mid-January (Fig. 3). In northern quarter of the thickness of Septiler China the species breeds in July and August biloeularis, an inhabitant of exposed rocky (Cheung et al. 1962). shores. Siphons Mantle Only the siphons protrude through the Mantle fusions are of the inner folds only mud to the water above (Fig. 1). The exhal­ and, thus, are oftype A (Yonge 1957). Man­ ant siphon (Fig. 4, ES) is formed by tissue tle fusions occur dorsally above the exhalant fusion between the inner mantle folds only, siphon and between the exhalant siphon and this being type A (ii) (Yonge 1957). The in­ the inhalant aperture. The mantle also fuses halent aperture (IA) is not separated from anteroventrally and here an elongate adduc­ the pedal/byssal aperture by mantle fusions tor muscle (AA) links the two valves. and thus cannot be regarded as a siphon. The outer mantle fold is small and the The exhalant siphon is devoid of tentacles, periostracum that is secreted by the inner though the inhalant aperture bears on each surface ofthe outer mantle fold is composed lobe 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 MAXIMUMSHELL RATIO OF SHELL SHELL LENGTH THICKNESS THICKNESS: SHELL (MM) (MM) LENGTH(%)

MIISClllista senlwlIsi(/ Benson 28 0.25 0.97 Limnopern(/ forlllnei (Dunker) 37 0.65 1.70 Brachidonles (/Ir(/Ills Lischke 16 0.35 2.27 Seplifer biloclliaris Linnaeus 58 2.05 3.53 Muscu/ista senhausia Benson-MoRTON 23

::1'''''"''' '" SAMPLE SIZE: 533 SAMPLE SIZE=790 20 15 10 5 SAMPLE SIZE=851

DECEMBER 1971 SAMPLE SIZE: 1012 ~1~~l\--,.-----,---,

SAMPLE SIZE:7Bl 1972 SAMPLE SIZE:821 ~,

!\ 20 AUGUST 1972 SAMPLE SIZE:466 :n~~T'_Y_19_7T2--,=J,-~-,,--,=S~AM_,PL_E_S_IZ,E_:_9_7-,1 ::L----.------r"~=------.----I ----,------, __

SAMPLE SIZE:643

::100'0"" '''' ...~"" ~,,<.." SAMPLE SIZE=691

::L, -,--,--..ALr II 10 15 20 25 5 10 15 20 25 30 35 40

FIG. 3. Length-frequency histograms showing the composition of monthly samples of the population of Musculisla 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 size expressed as a percentage of the total sample. 24 PACIFIC SCIENCE, Volume 28, January 1974

ES lae (SP). Each mantle lobe is cream colored and patterned by radiating brown bands with small patches of white pigment. This is particularly noticeable around the inhalant aperture. A large branchial septum (BS) re­ stricts the size of the inhalant aperture and (Fig. 5, BS) connects the ctenidia (ID, aD) to the mantle at the point of fusion separat­ ing the exhalant siphon from the inhalant aperture and, thus, the suprabranchial from BS SP the infrabranchial chambers.

Musculature The anterior adductor muscle (Fig. 5, AA) is relatively large and elongate and is located on the anteroventral floor of the shell valves. It is thus in a similar position to that of Limnoperna (Morton, in press),. X enostrobus (Wilson 1967), and Mytilus IA (White 1937). The anterior byssal retractor muscles (ABR) are very small and originate FIG.4. MllsclI/isla senhallsia. A posterior view of on the anterodorsal roof of the shell valve the animal when actively filtering clean seawater. (See just underneath the umbo (U). The posterior legend for Fig. 2 for abbreviations.) adductor muscle (PA) is approximately

PBR(2) 5S 5mm R

ES

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

----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 25 twice the size of the anterior adductor mus­ the ventral marginal food grooves of both cle and is located posterodorsally. The demibranchs, the ctenidial axis, and at the posterior byssal retractor muscle is large junctions of the dorsal edges of the ascend­ and is divided into two component units ing lamellae of the inner and outer demi­ (PBR[I], PBR[2]) as in Limnoperna branchs. (Morton, in press) and X enostrobus ineon­ The ctenidialllabial palp junction is of stans (Wilson 1967). There is a small pos­ type I (Stasek 1963), and the mechanism by terior pedal retractor (PPR). which material arriving at the ctenidial ter­ minii of the food grooves is sorted is essen­ Ciliary Currents ofthe Mantle, tially the same as that described by Morton Visceral Mass, and Foot (in press) for Limnoperna. In Limnoperna, however, the anterior filaments of the inner The ciliary currents of the mantle, vis­ demibranch are shorter than are those ofthe ceral mass, and foot are all rejectory in na­ outer demibranch. In Museu/ista the fila­ ture. Those of the mantle pass unwanted ments ofthe outer demibranch are the short­ material posteriorly to be ejected via the er. However, this modification fulfills the inhalant aperture (Fig. 5, IA). Such material same function in both species. Material ar­ is not ejected by the rapid phasic adduction riving at the labial palps on the crests ofboth ofthe adductor muscles as in many eulamel­ ventral marginal food grooves is thus pre­ libranchs but by cilia passing it dorsally to sented to the sorting surfaces of both labial be finally ejected by the outward flow of palps. Such a modification thereby dramati­ water from the exhalant siphon (ES). In this cally increases the sorting potential of the respect Musculista senhausia is very similar labial palps. to Limnoperna (Morton, in press) andAdu/a As noted by Fankboner (1971) for Adu/a, (Fankboner 1971). the outer demibranch of Muscu/ista The ciliary currents of the visceral mass senhausia is some 4 to 5 filaments shorter similarly pass unwanted material poste­ anteriorly than is the inner demibranch. riorly, where it accumulates at a point im­ This adaptation, apparently characteristic mediately posterior to the byssal gland of all mytilids, further enhances the sorting (BG). From this point it falls on to the man­ mechanism described above. tle for rejection by the mantle cilia. The labial palps of M. senhausia are The foot (F) is long, lanceolate, and very comparatively large. Other burrowing active. The ciliary currents on the surface of species living in soft mud, such as members the foot pass material dorsally. The foot ofthe Tellinacea (Yonge 1949), also possess constructs the nest. large labial palps. The ciliary currents ofthe labial palps bear a close resemblance to Ctenidia and Labial Palps those of Adula (Fankboner 1971) and thus can be considered to be ofthe typical mytilid The ctenidia comprise two somewhat type. subequal demibranchs of which the outer The lips ofthe mouth are large and fleshy; (Fig. 5, aD) is the longer. They are not as they possess ciliary currents similar to those long as those of Limnoperna (Morton, in of Dreissena polymorpha (Morton 1969a) press). The ctenidia are flat, homorhabdic, and serve a rejectory function. They can be and filibranchiate; and at their dorsal edges classified as "simple" (Bernard 1972). the ascending lamellae ofboth the inner and outer demibranchs are attached to the vis­ ceral mass and to thejunction ofthe visceral mass and mantle, respectively, by ciliary Alimentary Canal fusions. Filamentary cohesion is achieved, The stomach is located under the an­ as in all mytilids, by ciliary discs. The ciliary terodorsal margin of the shell and is sur­ currents of the ctenidia are oftype B(I) (At­ rounded by the dark digestive diverticula kins 1937), in which acceptance tracts lie in (Fig. 5, DD). 26 PACIFIC SCIENCE, Volume 28, January 1974

The oesophagus enters at the anterior end Galloprol'incialis (Giusti 1971). In Mytilus of the stomach, whilst from the posterior the style sac and midgut are conjoined but in end arises the midgut (MG) and a separate Musculista senhausia the style sac is sepa­ style sac (SS). The style sac passes back­ rated by a fusion of the minor typhlosole ward between the posterior byssal retractor with the epithelium ofthe midgut. The major muscles (PBR [1] [2]) and terminates dorsal typhlosole of the stomach passes directly to the posterior adductor muscle (PA). The into the midgut. Such an arrangement re­ midgut does not, as it does in other mytilids, sults in a style sac with a structure that is e.g., Mytilus (White 1937) and Limnoperna similar to, but convergent with, the separate (Morton, in press), pass between the byssal style sac of many of the Eulamellibranchia, retractors conjoined to the style sac. Before e.g., Dreissena polymorpha (Morton reaching them the midgut turns upon itself, I969a ). Kato and Kubomura (1954) have de­ loops on the right side of the body, passes scribed the structure ofvarious bivalve style under the posterior edge ofthe stomach, and sacs and recognize that the epithelium con­ the.n penetrates the ventricle (V) of the stituting the sac is divisible into a number of heart, extending posteriorly as the rectum zones which they have termed A, B, and C. (R) and terminating in an anus posterior to A further zone, 0, was recognized by Mor­ the posterior adductor muscle. ton (1969a) and regarded as the secretory The style sac when seen in transverse sec­ region of the major typhlosole. In tion (Fig. 6) is very different from that ofthe Muscltlista senhausia the same zones can be typical mytilid as exemplified by Mytilus recognized, although because the typh­ losole is the minor typhlosole the term B1 has been used. The cells of the A cell layer are 25 J.L tall and possess a dense ciliary border oflength 15 J.L. The cells ofthe B1 cell layer are 70 J.L tall with a somewhat less dense and shorter ciliary border between 12 to 14 J.L tall. The cells of the C cell layer are 20 J.L tall with short (5 J.L) cilia arranged in distinct groups. Internally the ciliary root­ lets are discernible. The cells of the 0 cell layer are 12 J.L tall and possess cilia 10 J.L long. The stomach of M. senhausia (Fig. 7) is elongate and bears a close resemblance to the stomachs of other mytilids, e.g., Lithophaga (Purchon 1957, Dinamani 1967), Mytilus (Graham 1949, Reid 1965), Perna (Dinamani 1967),Adula (Frankboner 1971), and Limnoperna (Morton, in press) and thus belongs to type 111 (the Gastrotri­ teia) and section I of the stomach types elucidated by Purchon (1957) and Dinamani (1967), respectively. The nomenclatural systems of Purchon (1957) and Reid (1965) are adopted here. The structure of the stomach of various members of the Mytilacea seems to be re­ B, 0 markably constant and in this description only those points in which MlIsclilista FIG.6. Musculis/a sell!lausia. A transverse section through the style sac with crystalline style showing the senhausia differs from the others will be distribution of the different epithelia. (See legend for commented upon. The stomach of M. sen­ Fig. 2 for abbreviations.) hallsia possesses a distinct appendix, as Museulista senhausia Benson-MoRTON 27

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

does Mytilus (Reid 1965). In other mytilids food-sorting cecum. In Museulista this structure is not so well developed (Pur­ senhausia the food-sorting cecum (Fe) is chon 1957) and may be vestigial or absent. small and terminates under the left pouch. Lying next to the appendix are a group of In other mytilids it is long and in such gen­ ducts which communicate with the digestive era, e.g., Limnoperna (Morton, in press), it diverticula (DOD 2) located at the termina­ is thought that a long cecum gives greater tion ofwhat Reid (1965) has termed the right efficiency to the processes ofcollection and duct tract (RT). On the left side of the sorting offood material. The ciliary tracts of stomach the left duct tract (LT) terminates the food-sorting cecum are similar to those in the ducts of the digestive diverticula described for Mytilus (Reid 1965) and (DOD 3, DOD 4) constituting the left Limnoperna (Morton, in press). pouch (LP) into which a spur of the gastric shield (GS) is located. It would seem reasonable to call the ducts on the right side POPULATION DYNAMICS of the body, the right pouch (RP). As­ It has been shown earlier that the shell sociated with the right duct tract are other dimensions of Museu/ista senhausia are re­ ducts of the digestive diverticula (DOD 1, latively constant. It was, therefore, decided DOD 5) which are also present in other to attempt to establish the number of age mytilids, e.g., Lithophaga (Purchon 1957) groupings within the population by means of and Myti/lls (Reid 1965), although in Adll/a a length-frequency histogram. Such histo­ (Fankboner 1971) and Limnoperna grams have been used successfully in the (Morton, in press) some of these ducts past for the analysis of populations of other (DOD 5) are to be found just inside the molluscs, e.g., Monodonta lineata (Desai 28 PACIFIC SCIENCE, Volume 28, January 1974

1966), Monacha cantiana (Chatfield 1968), 30 and Dreissena polymorpha (Morton I969b). Accordingly, a large sample of animals was collected from Tai Tam Bay in early 25 • 0 • November 1971 and the shells were mea­ 0 sured along their greatest length to the 0 0 000 0 0 a a nearest I mm (Fig. 3). In November the E 20 0 population comprised a single age grouping e:; I of mean length 22 mm. Such a result finds >- I (9 I accord with an earlier conclusion that the 0 colony was a new one, this conclusion hav­ ing been reached because of an absence of 0 empty shells within the population. Similar n(f) 10 a samples of 500 to 1,000 animals collected in a a a the first weeks of December 1971 and 0 January 1972 showed a similar population structure. By mid-January 1972 a spatfall 5 had occurred on the fringes of the existing colony and young individuals had already established themselves in nests. In subse­ N 0 J F M A M JJ A S 0 quent monthly samples the new age group 1971 1972 MONTHS assumed increasing importance. In the FIG. 8. Average length of each age group in the summer of 1972 they grew very rapidly. monthly samples of Muscu/isla senhausia. Open cir­ Their parents grew at a slower rate. By Sep­ cles indicate live animals, black circles empty shells. tember 1972 the primaryadult age group had all but died out. This was evidenced by the March. However, in April the animals occurrence of very many empty shells started growing again and from then until within the population. In early October 1972 October 1972 when they had died they grew it was found that the entire population had from 9 mm to 25 mm in length. They died. The shell of Musculista senhausia is achieved in 9 months, i.e., from spatfall to extremely thin, so that even after such a death, a size which it had taken their short period oftime most ofthe empty shells parents-if one assumes that the time ~f had been broken up. However, a small sam­ spatfall for this generation was approxI­ ple of intact valves was collected and when mately the same as that of their offspring, measured revealed that the young animals i.e., January-20 months to achieve. The had died when 25 mm in mean length. adult population had bred after approxi­ Perhaps significantly the primary adult mately 1 year of life to produce the younger population had also died when approxi­ generation; the young generation, however, mately this size earlier in August to Sep­ died before becoming sexually mature and tember. this, together with the death of the primary By separately plotting the mean length of generation, resulted in the death of the en­ the age groups within the population (Fig. 8) tire colony. This occurred in October 1972. length~frequency as revealed by the histo­ By mid-October that area of beach previ­ gram, one can see that the primary adult age ously occupied by the M. senhausia colony grouping did not grow between the months had virtually returned to an ecological con­ of November 1971 and May 1972. They did dition similar to that of other neighboring grow, by approximately 4 mm, between ~he unaffected beaches. months ofJune to August 1972 but then died out. By contrast the young age group achieved a high rate of growth in the early DISCUSSION months of their life-January to March The Mytilacea exhibit a wide degree of 1972-but slowed down somewhat in adaptive radiation and the more successful Musculista senhausia Benson-MoRTON 29

genera such as Mytilus and Modiolus are to variety of both intertidal and sublittoral be found on many of the shores the world habitats would seem to suggest that it is an over. This habit can be related to the evolu­ opportunist bivalve, settling whenever and tion of the heteromyarian condition. Other wherever it can. Once settled, the animal mytilids such as Crenella are sublittoral relies upon the production ofa large number and,judged by their shape, infaunal (Tebble of eggs (Cheung et al. 1962) and a rapid rate 1966). Perhaps bridging the gap between of growth to colonize quickly all available these two extremes are such animals as suitable sites. and Musculista sen­ In 1971 the colony comprised a single age hausia. Musculus discors is found living grouping. A further spatfall, which occurred intertidally amongst algae (Tebble 1966), al­ in January to April 1972, settled on the sea­ though Merrill and Turner (1963) found the ward periphery of the existing colony. Such same species living sublittorally. Similarly a habit is almost certainly the way in which Hanna (1966) found Musculista senhausia such colonies are enlarged. The second age without a nest living attached to pilings and group assumed increasing importance this species has also been found attached to within the population during the course of test blocks hung 3 to 4 meters in the sea in 1972 and, after the adult age group had died Hong Kong, again without a nest. Like out in August, were the only age group left. Musculus discors, however, Musculista By October 1972, however, they too had senhausia also occurs intertidally and forms died. The death ofthe colony is attributable large colonies in estuaries and sheltered to the extraordinarily fast rate of growth bays. The colony inhabiting Tai Tam Bay, exhibited by the young generation in 1972, Hong Kong, formed a mat developed by the because both adults and young died before nest-building activities of the colony mem­ producing a further generation. Cheung et bers. In so do-ing they also bound them­ al. (1962) record the maximum shell length selves to sand grains and, when in large ofanimals they examined as 29 mm. Such a enough numbers, to the nests ofeach other. figure falls within the normal distribution The nest completely encloses the animal ex­ pattern of the age groupings elucidated in cept for the posterior margin of the shell this study as do the maximum figures for where the inhalant aperture and the exhalant shell length of this species recorded by siphon open to the water above. The gre­ Hanna (1966). garious habit of M. senhausia results in the Musculista senhausia shows a number of colony accumulating around it a fine mud adaptations to its peculiar mode oflife. Most derived from the feces and pseudofeces. important of these is the byssus which, as Cheung et al. (1962) have suggested that the well as acting as an anchor as in more con­ formation and expansion of a colony ventional heteromyarians such as the Pin­ dramatically alters the fauna of a sandy nidae (Yonge 1953), is also woven into an shore. This was true in Tai Tam Bay where enclosing nest. the colony (Fig. 3) was judged to be newly Other related mytilids also possess this formed. Typical sandy shore bivalves, e.g., habit: Musculus (Merrill and Turner 1963), Cyclina orientalis, Paphia euglypta, and Modiolus, and Amygdalum (Soot-Ryen more importantly Anomalocardia squa­ 1955), as well as the unrelated Lima hians. mosa, apparently had been unable to com­ In Lima, the nest serves a protective func­ pete with the growing Musculista sen­ tion. In Musculus discors, which has a thick hausia colony. Only empty shells of these shell, Merrill and Turner (1963) have sug­ species were found. Cheung et al. (1962) gested that the nest principally protects the report that the layer of M. senhausia eggs which are laid inside the nest. effectively prevents other bivalves from Musculista senhausia does not lay eggs projecting their siphons through to the within its nest; they are planktonic (Cheung water above. et al. 1962). Compared with such species as The very wide distribution of this species Septzfer bilocularis and Brachidontes at­ (Cheung et al. 1962) and its occurrence in a ratus, Musculista senhausia has a very thin 30 PACIFIC SCIENCE, Volume 28, January 1974 shell (Table 1). The shell is also relatively Museu/ista senhausia it is the minor typh­ much thinner than that of Limnoperna for­ losole. In other respects the style sac is simi­ tunei, an inhabitant of fresh waters where lar to that of Dreissena. The separate style the calcium content is typically much lower sac serves to keep the large amounts of de­ than that ofthe sea. It would thus seem that trital material passing through the gut away the nest thatMuseulista senhausia weaves is from the style and thus prevents it from re­ essentially a protective device for the adult. turning to the stomach. The nest serves a subsidiary function in Museulista senhausia possesses a keeping sediment out of the mantle cavity number of characters that are intermediate and thus has contributed to the successful between primitive and highly specialized exploitation of the soft shore environment mytilids. The anterior border of the shell is by this species. The organs of the mantle inflated and distinctly crenulate. Weak cre­ cavity are concerned with the processing of nulations, as in Sept({er (Yonge and Camp­ large currents of particulate material. As a bell 1968), are also present just posterior to consequence, the rejectory tracts are well the ligament. Such a condition would seem developed. The branchial septum serves as to be intermediate between the crenulated a valve regulating the intake of material, isomyarian shell of Crenella (Tebble 1961) whilst the labial palps and foot are large and and the noncrenulated extreme aniso­ the foot, as well as building the nest, also myarian shell of more typical mytilids. serves to keep the mantle cavity (and The anterior byssal retractor is small and perhaps the nest) clean. The ctenidia are is located almost directly under the umbo. relatively small. Museu/ista is thus adapted Such a position is intermediate between the in a similar manner to other lamellibranchs condition encountered in Museu/us diseors such as the Tellinacea (Yonge 1949) that are (Tebble 1961) where the anterior byssal re­ characteristically found in muddy habitats. tractor is located anteriorly and the condi­ Though the stomach is of the typical my­ tion in more extreme genera such as tilid type, it, too, is modified. The food­ X enostrobus (Wilson 1967) where the point sorting cecum is small. In the Tellinacea, of attachment of the muscle is on the pos­ also, the sorting areas of the stomach are terior border of the shell. The umbo of reduced (Yonge 1949, Purchon 1960). Also Muscu/ista senhausia is subterminal and as in the Tellinacea there is a distinct stom­ thus represents a further example of the in­ ach appendix. It would seem that the stom­ termediate condition exhibited by this ach is adapted to the rapid processing of an species with respect to the extremes seen in abundant food supply rather than with the Crenella (Tebble 1966), Myti/us (White sorting and abstraction of all available food 1937), Xenostrobus (Wilson 1967), and material. Septz{er (Yonge and Campbell 1968). In A major difference between M. senhausia Museu/ista senhausia the posterior byssal and the other mytilids studied (e.g., by Di­ retractor is divided into two blocks. This namani 1967) is that in the former the style situation also exists in Limnoperna (Mor­ sac is separate from the midgut. In the con­ ton, in press) and in X enostrobus ineonstans joined style sac and midgut of the typical (Wilson 1967). Such a development can mytilid such as Myti/us galloprol'ineia/is perhaps be related to the elongation of the (Giusti 1971), both major and minor typh­ posterior border of the shell in the losoles are present. In Museulista sen­ Mytilacea. Significantly, in Myti/us edu/is hausia the major typhlosole passes into (White 1937), which displays extreme the midgut whilst the minor typhlosole heteromyarianism, the posterior byssal re­ penetrates the style sac. The style sac is thus tractor is broken up into three units; whilst similar to, but convergent with, the style in Modio/us the posterior byssal retractor is sac of some eulamellibranchs such as divided into many more units (Yonge 1953). Dreissena po/ymorpha (Morton 1969a). In Though in itself highly specialized this species the typhlosole ofthe style sac is Museu/ista senhausia may recall an inter­ a portion ofthe majortyphlosole, whereas in mediate condition in the evolution of the Museu/ista senhausia Benson-MoRTON 31 heteromyarian condition in the Mytilacea. aperture; (2) the ctenidia are relatively Significantly, the evolutionary steps envis­ short; (3) the labial palps are large; (4) the aged as having occurred in the Dreissenacea food-sorting cecum of the stomach is small; (Morton 1970) find a number of parallels and (5) the style sac is uniquely, for a with the condition exhibited by M. mytilid, separate from the midgut. senhausia. Because of the large pallial sinus Other anatomical characters, particularly to the shell, Morton (1970) has suggested of the shell, suggest thatM. senhausia may that the fossil dreissenid Dreissenomya recall a transitional stage in the evolution of aperta was byssally attached and yet lived the heteromyarian condition in the an infaunal life. The similarities that exist Mytilacea, and that the heteromyarian between Dreissenomya and Museulista condition arose in the Mytilacea before the senhausia are attributable to the indepen­ colonization of hard surfaces was achieved. dent evolution of the heteromyarian condi­ tion inthese two bivalve phyiogenies (Yonge I ACKNOWLEDGMENTS and Campbell 1968). However, the occur­ rence ofM useu/ista senhausia living in inter­ During this investigation technical assis­ tidal mud may attest to the similarity of the tance was obtained from Mr. D. Chi who evolutionary process in the Dreissenacea sectioned and stained the material here re­ and Mytilacea and perhaps points to some of ported upon and from Mrs. D. W. Kwan the changes that have occurred in the evolu­ who arranged for the monthly measurement tion of the Mytilacea, namely, that the of the samples. heteromyarian condition was evolved be­ fore the successful exploitation of rocky shores by this group. LITERATURE CITED ATKINS, D. 1937. On the ciliary SUMMARY mechanisms and interrelationships of The mytilid Museulista senhausia lamellibranchs. 111. Types of lamelli­ Benson forms large colonies in intertidal branch gills and their food currents. mud flats in sheltered bays in the Far East. Quart. J. micro Sci. 79: 375-421. M. senhausia is considered to be an op­ BEEDHAM, G. E. 1958. Observations on the portunist bivalve with a high reproductive non-calcareous component of the shell of capacity, a fast rate ofgrowth, and an ability the Lamellibranchia. Quart. J. micro Sci. to colonize other habitats such as hard sub­ 99: 341-357. littoral surfaces. When occurring interti­ BERNARD, F. R. 1972. Occurrence and dally it dramatically affects the ecology of function of lip hypertrophy in the the shore. The mud flat is created and main­ Anisomyaria (, Bivalvia). tained as a result of (I) the deposition of Canad. J. Zool. 50: 53-57. feces and pseudofeces and (2) the animals' CHATFIELD, J. E. 1968. The life history of habit of building a nest which stabilizes the the helicid snail Monaeha eantiana surface mud. (Montagu), with reference also to M. ear­ The nest is woven from byssal threads tusiana (Muller). Proc. malac. Soc. and serves a number of functions: (I) it pro­ Lond. 38: 233-245. tects the very thin shell; (2) it prevents the CHEUNG, S., C. Y. CHI, AND OTHERS. 1962. entry of terrigenous material into the mantle Economic invertebrates ofChina (marine cavity; and (3) it anchors the animal into the Mollusca) [in Chinese]. Scientific Pub­ mud. lisher of China, Peking. The animal also possesses a number of CHUANG, S. H. 1%1. On Malayan shores. other morphological adaptations that suit it Muwu Shosa, Singapore. for an infaunal life. These are: (I) a large DESAI, B. N. 1966. The biology of branchial septum acts as a valve controlling Monodonta /ineata (Da Costa). Proc. the inflow oflarge particles into the inhalant malac. Soc. Lond. 37: 1-17. 32 PACIFIC SCIENCE, Volume 28, January 1974

DINAMANI, P. 1967. Variation in the ---. 1969c. Studies on the biology of stomach structure of the Bivalva. Dreissena polymorpha Pall. 4. Habits, Malacologia 5: 225-268. habitats, distribution and control. Water FANKBONER, P. V. 1971. The ciliary cur­ Treatment and Examination 18: 233-240. rents associated with feeding, digestion ---. 1970. The evolution of the and sediment removal in Adula (Botula) heteromyarian condition in the Dreis­ falcata Gould 1851. BioI. Bull., Woods senacea (Bivalvia). Paleontology 13: Hole 140: 28-45. 563-572. ---. In press. Some aspects of the GIUSTI, F. 1971. The fine structure of the biology and functional morphology ofthe style sac and intestine in Mytilus gallo­ organs of feeding and digestion on provincialis Lam. Proc. malac. Soc. Limnopernafortunei (Dunker) (Bivalvia: Lond. 39: 95-104. Mytilacea). Malacologia. GOREAU, T. F., N. I. GOREAU, T. PURCHON, R. D. 1957. The stomach in the SOOT-RYEN, and C. M. YONGE. Filibranchia and the Pseudolamellibran­ 1969. On a new commensal mytilid (Mol­ chiao Proc. zool. Soc. Lond. 129: 27-60. lusca: Bivalvia) opening into the ---. 1960. The stomach in the Eulamel­ coelenteron of Fungia scutaria libranchia: stomach types IV and V. (Coelenterata). J. zoot. Res. 158: Proc. zool. Soc. Lond. 135: 431-489. 171-195. PURCHON, R. D., AND D. BROWN. 1969. GRAHAM, A. 1949. The molluscan stomach. Phylogenetic interrelationships among Trans. roy. Soc. Edinb. 61: 737-776. families of bivalve molluscs. Proc. third HADERLlE, E. C. 1968. Fouling organisms Europ. malac. Congr. 9: 163-171. in the harbor at Monterey, California. REID, R. G. B. 1965. The structure and 2nd. International Congress on Marine function of the stomach in bivalved mol­ Corrosion and Fouling, 1968. Athens, luscs. J. zool. Res. 147: 156-184. Greece. SMITH, A. G. 1944. Volsella senhausi HANNA, G. D. 1966. Introduced molluscs Reeve in Bolinas Bay, California. Min­ of western North America. Occ. Pap. utes of the Conchological Club of Calif. Acad. Sci. 48: 1-108. Southern California 39: 18. KATO, K.,and K. KUBOMURA 1954. On the SOOT-RYEN, T. 1955. A report on the family origins of the crystalline style of lamelli­ Mytilidae (Pelecypoda). Allan Hancock branchs. Sci. Rep. Saitama Univ. B3: Pacif. Exped. 20: 1-174. 135-152. STASEK, C. R. 1963. Synopsis and discus­ KAWAHARA, T. 1961. Regional differences sion of the association of ctenidia and in the composition of fouling com­ labial palps in the bivalved Mollusca. munities in Ago Bay. Rep. Fac. Fish. Veliger 6: 91-97. prefect. Univ. Mie 4: 65-80. TEBBLE, N. 1966. British bivalve seashells. KIRA, T. 1961. Coloured illustrations ofthe British Museum (Natural History), Lon­ shells of Japan. Hoikusha, Osaka. don. TRUEMAN, E. R. 1950. Observations on the MERRILL, A. S., and R. D. TURNER 1963. ligament of Mytilus edulis. Quart. J. Nest building in the bivalve genera micr. Sci. 91: 225-235. Musculus and Lima. Veliger 6:55-59. MORTON, B. S. 1969a. Studies on the biol­ WHITE, K. M. 1937. Mytilus. L.M.B.C. ogy of Dreissena polymorpha Pall. I. Mem. typo Br. Mar. PI. Anim. 31: 1-117. General anatomy and morphology. Proc. WILSON, B. R. 1967. A new generic name malac. Soc. Lond. 38: 301-321. for three recent and one fossil species of ---. 1969b. Studies on the biology of Mytilidae (Mollusca - Bivalvia) in South­ Dreissena polymorpha Pall. 3. Popula­ ern Australia with redescriptions of the tion dynamics. Proc. malac. Soc. Lond. species. Proc. malac. Soc. London. 37: 38: 471-482. 279-295. Museulisla senhausia Benson-MoRTON 33

WOLFF, W. J. 1969. The Mollusca of the on the evolution of this habit. Quart. estuarine region of the rivers Rhine, J. micr. Sci. 96: 383-410. Meuse and Scheidt in relation to the hy­ ---. 1957. Mantle fusion in the Lamelli­ drography of the area. II. The Dreis­ branchia. Pubbl. Staz. zool. Napoli senidae. Basteria 33: 93-103. 29: 151-171. YONGE, C. M. 1949. On the structure and --_. 1962. On the primitive significance adaptations of the Tellinacea, deposit of the byssus in the Bivalvia and its ef­ feeding Lamellibranchia. Phil. Trans., fects in evolution. J. Mar. bioI. Ass. B, 234: 29-76. U.K. 42: 113-125. ---. 1953. Form and habit in Pinna YONGE, C. M., ANDJ. I. CAMPBELL. 1968. earnea Gmelin. Phil. Trans., B, 237: On the heteromyarian condition in the 335-374. Bivalvia with special reference to ---. 1955. Adaptation to rock boring in Dreissena polymorpha and certain BOlula and Lilhophaga (Lamelli­ Mytilacea. Trans. roy. Soc. Edinb. 68: branchia, Mytilidae) with a discussion 21-43.