SRE poi ogy sos Seva te ieee oe VAD © ge < АЯ поли A 7 RSE tan Reta bre tp QAR eros ии а er w aa nn AR PT e AA AO! a cad à BET рим 4 ии GEE e Baty WI Roe LÉ mi Ey i pa inguin ernst saga AENA CRIA sto ae ns ee PER алии De bé SE NES BIO DD Sa econ M à СКК Фома ал Vora RL N OP ps tie fee. Keinen OD ODDO Oem Re eg sien ee № Et À don ee n.d ES LEERE, NET AN ea ie An de ve de Deke м “a i A A Ч We WW A реф Site С > NS A A re AS “ es no sar ee вынес o ee =. “ I EM da a. Ата 4 Ad EA A ero | аи od AVIAR Ska tn tea ha Au» je ne RER! ++ oi of) т рт e и > ee LA ANAS Halo Pret nn Sw nds = eat Pe Me de LEE md À ar fe = AIDA x we a = . » ds LENE HE BNE нас ME 8 66 AG SE DES EM ааа D Se ee ee ee À, À ee see re ee Sa SpE a aa a IO A ав 2 gh ae вразнос ETE HARVARD UNIVERSITY a ES): LIBRARY OF THE Museum of Comparative Zoology | i i | Ñ e 7 u | : | UC | A А 7 A > . О if u | L à р LA 2 u u LL : u О ER a y O À т . yr в | Le if » OR LL . . ve | Tr > ‘a 7 . i Фе er A u В f ic В y . у Y о = e » = = o = i Г o a | | А | = ТИ р 7 ' AS Y . > =D u» Ay u } | | | | 7 on 4 anh SN Y de din Lei. 173 164 Len a dé > q 1 11 (ui 5 Wie is 5 ui о f = | i и e I, ry ha » | PA ee memes 0 - Na amené is a — al фаре: тои: 1: РС! y rra es € Mirek? sic tay qa у Le Sr A Le ig sey Iwinsther 2 e A TE O Hai“ Mana A A одобрил ya gue VOL. 12 1973 MALACOLOGIA International Journal of Malacology Revista Internacional de Malacologia Journal International de Malacologie Международный Журнал Малакологии Internationale Malakologische Zeitschrift г * ФТ с F Si 4 o y NTC | О on ЕЦ, | ИТУ | Ai e В = vvoloyoloM 15 jenwel Inne GC 1030 Hii ab. lon: Om re отв фо: > Y 35 Joneitianietn! lorrıuok Knionoxono”Ni Anka Ruh: 200 AVANSM HivisetiosS arscicolcdalsM slonotoanictal 3 A « MALACOLOGIA, VOL. 12 CONTENTS М. В. CARRIKER and Н. Н. CHAUNCEY Effect of carbonic anhydrase inhibition оп shell penetration by the murieimd gastropod! Охоза рт сте ns 2) ose M. CASTAGNA and P. CHANLEY Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the westernÍMidatlanticicoastist. о one cote ER CO J. N. CATHER Regulation of apical cilia development by the polar lobe of MyanassolGastropoda: Nassariidae) an a... u. „ae ee P. T. CLAMPITT Substratum as a factor in the distribution of pulmonate Snalls=ın,Douslas’Take,; Michigan... er a see ео ee memes Е. 5. DEMIAN and Е. YOUSIF Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). rGeneraloutlinesiofdevelopmentens Qt ое ее Е. 5. DEMIAN and Е. YOUSIF Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). Ш. Development of the’alimentary System в 2 SO ne Е. S. DEMIAN and Е. YOUSIF Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). Ш. Development of the circulatory and renal systems............ Е. 5. DEMIAN and Е. YOUSIF Embryonic development and organogenesis in the snail Marisa сотпиатей$ (Mesogastropoda: Ampullariidae). IV. Development of the shell gland, mantle and TESMTALO OT ans nr. Mi, о а O ЗО Е. а. DRISCOLL and D. Е. BRANDON Mollusc-sediment relationships in northwestern Buzzards Bay Massachusetts, USHA.) LU A. ee ee ae Thin ae to cc ot E. FISCHER-PIETTE and D. VUKADINOVIC Sur les mollusques fluviatiles de Madagascar. ................. MALACOLOGIA, VOL. 12 CONTENTS (cont.) M. J. IMLAY Effects of potassium on survival and distribution of FPOSDWALOT MUSSCl Gy. co... acc. e's en oies es ee oe оо ое 97 M. L. M. LE PENNEC Morphogenése de la charniere chez 5 especes de Veneriidae........ 225 B. MORTON Some aspects of the biology and functional morphology of the organs of feeding and digestion of Limnoperna fortunei (Dunker) (Bivalvia: Mytilacea). „no... « a aS ER 265 S. K. PIERCE The rectum of “Modiolus” demissus (Dillwyn) (Bivalvia: Mytilidae): А clue to solving a troubled taxonomy ............... 283 R. H. POHLO Feeding and associated functional morphology in Tagelus californianus and Florimetis obesa (Bivalvia: Tellinacea).......... 1 W. F. PONDER The origin and evolution of the Neogastropoda ............... 2.1298 G. WIUM-ANDERSEN Electrophoretic studies on esterases of some African Bromphalaria spp. (Planorbidae) ser сн. un ec ae 115 im, oe Раб, = BOL. 12 мо 1 MUS. COMP. ZOOL, 19723 LIBRARY AUG 10 1913 HARVARD UNIVERSITY, rnational Journal of Malacology в is у . . Revista Internacional de Malacologia + A Journal International de Malacologie В о. 14 a! 3 и» “10e x 12 Международный Журнал Малакологии Internationale Malakologische Zeitschrift Editor-in-Chief J. В. BURCH Associate Editor R. NATARAJAN Secretaries E. PERISHO KAWAMURA J. WHITE-RUDOLPH Editorial Office Museum of Zoology University of Michigan Ann Arbor, Michigan 48104 U.S.A. EDITORIAL BOARD | O) ACOCSY. Budapest, Hungary . E. BINDER, Geneva, Switzerland . В. BOETTGER, Braunschweig, Germany . Н. CLARKE, Ottawa, Canada . 5. DEMIAN, Cairo, Egypt . J. DUNCAN, Liverpool, U.K. A. FILATOVA, Moscow, U.S.S.R. FISCHER-PIETTE, Paris, France FRANC, Paris, France FRETTER, Reading, U.K. . GALTSOFF, Woods Hole, U.S.A. V. GROSSU, Bucharest, Rumania HABE, Tokyo, Japan . D. HARRISON, Waterloo, Canada . HATAI, Sendai, Japan . A. HOLME, Plymouth, U.K. . HUBENDICK, Göteborg, Sweden ‚ Р. KANAKOFF, Los Angeles, U.S.A. . М. KEEN, Stanford, U.S.A. ; M. A. KLAPPENBAC H, Montevideo, Uruguay Y. KONDO, Honolulu, U.S.A. T. KURODA, Kyoto, Japan Н. LEMCHE, Cópenhagen, Denmark AKLILU LEMMA, Addis Ababa, Ethiopia J. LEVER, Amsterdam, The Netherlands A. LUCAS, Brest, France N. MACAROVICI, Iasi, Rumania D. Е. MeMICHAEL, Sydney, Australia i. MEIER- BROOK, Tubingen, Germany 11 ее MALACOLOGIA | А. ZILCH, Frankfurt, Germany _ С: J. BAYNE ANNE GISMANN Managing Editor S. K. WU Subscription Office Department of Mollusks Academy of Natural Sciences Philadelphia, Pennsylvania 19103 ISA: J. Е. MORTON, Auckland, New Zealand W. К. OCKELMANN, Helsinggr, Denmark N. ODHNER, Stockholm, Sweden J. OKLAND, Oslo, Norway W. L. PARAENSE, Brasilia, Brazil J. J. PARODIZ, Pittsburg, US Ar С. M. PATTERSON, Ann Arbor, U.S.A. W. F. PONDER, Sydney, Australia А. W. В. POWELL, Auckland, New Zealand R. D. PURCHON, London, U.K. C. P. RAVEN, Utrecht, The Netherlands O. RAVERA, Ispra, Italy C.F.E, ROPER, M cion Die USA. N. W. RUNHAM, Bangor, U.K. 5. С. SEGERSTRALE, Helsinki, Ein R. V. SESHAIYA, Porto Novo, India ben: F. STARMÜHLNER, Wien, Austria J. STUARDO, Concepcion, Chile Е. TOFFOLETTO, Milano, Italy A W. $. S. VAN BENTHEM JUTTING, к Domburg, The Netherlands — J. A. VAN EEDEN, Potchefstroom, S С. О. VAN REGTEREN ALTENA, | Neth. ae В. В WILSON, Perth, Australia = C. M. YONGE, Edinburgh, U.K. H. ZEISSLER, Leipzig, G. О. В. N 4 1 > LI 3 2 в 5. E E : Ave 101 Mystic International Journal of Malacology Revista Internacional de Malacologia Journal International de Malacologie Международный Журнал Малакологии Internationale Malakologische Zeitschrift UNITAS MALACOLOGICA EUROPAEA RESOLUTION The Unitas Malacologica Europaea, representing malacologists and conchologists in Europe, is much concerned by the rapidly increasing destruction of the natural environment. It therefore supports all measures being taken to avoid and reduce pollution. Unitas Malacologica Europaea urges all who are concerned throughout the world to accept responsibility for ensuring the future existence of Mollusca and their habitats. We, the members of Unitas Malacologica Europaea, realise that this will neces- sitate a curtailment of collecting activities, but we are sure that, as responsible naturalists, all conchologists and malacologists will wish to support appropriate conservation measures. Unitas Malacologica Europaea therefore urges that for all purposes whatsoever only about the minimum number of specimens should be collected. Observations as well as photography of living specimens in their natural habitats may be a much more rewarding activity than mere collecting. This applies equally to the work of the amateur and the professional. Such an approach to field studies would result in the acquisition of much of the information which is so urgently needed to ensure the success of the efforts being made to conserve these animals. The European national malacological societies fully associate with this resolution and will publish it in their periodicals. Dr. Oliver E. PAGET Secretary Erratum, Vol. 11, No. 2, page 378. The legends for Figs. 14 and 15 in the paper by F.R. Bernard were mistakenly transposed. MALACOLOGIA, 1973, 12(1): 1-11 FEEDING AND ASSOCIATED FUNCTIONAL MORPHOLOGY IN TAGELUS CALIFORNIANUS AND FLORIMETIS OBESA (BIVALVIA: TELLINACEA) Ross H. Pohlo Department of Biology California State University at Northridge Northridge, California 91324, U.S.A. ABSTRACT A study was made comparing 2 species, Tagelus californianus (Conrad, 1837) and Florimetis obesa (Deshayes, 1855), with other members of the superfamily Tellinacea. The nature of their feeding was investigated and an attempt was made to relate aspects of their morphology to feeding behavior. Field and laboratory studies, particularly of the behavior of the inhalant siphon, and an analysis of mantle cavity and stomach contents were performed to ascertain the mode of feeding of these species. Although many Tellinacea are deposit feeders, these 2 species feed primarily on suspended particles. Deposits, however, can and do fall into the inhalant siphons. This is more prevalent in Florimetis obesa than in Tagelus califor- nianus. Tagelus californianus resembles suspension feeding bivalves by having large ctenidia which possess well developed marginal grooves, the outer demibranch is not upturned, the dorsal hood is large, incipient straining tentacles exist on the inhalant siphon, the animal is upright in the burrow and a mantle fold is lacking. The only major features common to this species and deposit feeders are separated siphons. Florimetis obesa resembles deposit feeders by having upturned outer demibranchs, the presence of a mantle fold, separate siphons which lack straining tentacles and the organism lies on its side. It resembles suspension feeders by having relatively large ctenidia. INTRODUCTION As has been shown (Pohlo, 1969) there has been some confusion concerning the type of feeding that occurs in the super- family Tellinacea. Yonge (1949) regarded the Tellinacea as fundamentally deposit feeders; later other authors such as Morton (1960) and Jorgensen (1966) repeated this assertion. Meanwhile, several authors (Holme, 1961; Brafield & Newell, 1961; Purchon, 1963; Wade, 1965; Pohlo, 1966, 1967, 1969; Maurer, 1967; and Reid & Reid, 1969) have shown that suspension feeding also occurs in this superfamily. It is of interest, therefore, to examine other species of tellinaceans to ascertain the type of feeding they employ and to note, where possible, which features of anatomy and behavior may be associated with a par- ticular type of feeding. To this end the morphology and feeding behavior of Tagelus californianus (Conrad, 1837) and Florimetis obesa (Deshayes, 1855) were studied and compared with а typical deposit feeding tellinacean such as Macoma nasuta and a suspension feeder such as Donax gouldi. MATERIALS AND METHODS OF STUDY Florimetis obesa and Tagelus califor- nianus were collected at Newport Bay and Mugu Lagoon in Southern California. T. californianus was found in various fine to medium grained substrata and occurs in great abundance in the banks of small tidal channels. As described by Weymouth (1920) and Yonge (1952) the animal occurs upright in a permanent burrow that can reach a depth of 50 cm. Its range is from Humbolt Bay, California to Panama bo В. Н. POHLO lem FIG. 1. Organs of the mantle cavity of Tagelus californianus viewed from the right side. Right valve and mantle lobe removed. Arrows indicate the direction of particle movement. Dotted arrows indicate movement on the underside of the surface. AA—anterior adductor; CM—cruciform muscle; ES—exhalant siphon; F—foot; ID—inner demibranch; IS—inhalant siphon; L—ligament; L P—labial palp; ML—mantle lobe; OD—outer demibranch; PA—posterior adductor; PR—posterior retractor. (McLean, 1969). Florimetis obesa was found intertidally in clean sand as well as in sand that contains some rocks or shell fragments. The adult organisms live about 15-25 cm below the surface where they lie on their left side. They have a geographic range from Point Conception, California to Magdalena Bay, Baja California, Mexico (McLean, 1969). Feeding behavior as reflected by the position and movements of the inhalant siphon was observed in the field, by using an underwater viewer, and on specimens maintained in laboratory aquaria. Move- ment of particles in the mantle cavity was observed by removing the right valve, along with its mantle lobe, and placing fine carborundum or carmine particles on various parts of the anatomy. To study the stomach contents of these organisms, the animals were dug in the field, the mantle cavity was opened, and the body was immediately preserved. The alimentary canal was later dissected out and the anatomy of the stomach and the nature of its contents were then observed. The movement of particles in the stomach of live specimens was noted by opening the stomach from the dorsal aspect and placing carmine or carborundum particles in various areas. FUNCTIONAL MORPHOLOGY External morphology Tagelus californianus (Fig. 1). This species is highly elongated being about 4 times as long as it is high. Large specimens are about 11 cm long and 2.7 cm high. The shell is covered by a brownish yellow periostracum that is often extensively worn in larger specimens. The ligament is exter- nal, thin and elongated, reaching a length of about 1.9 cm on the large specimens. Florimetis obesa (Fig. 2). In this species the shell is somewhat circular in outline, large specimens being about 7 cm long and 6 cm high. The valves are asymmetrical; the left valve has 2 grooves running from the umbo to the posterior edge, a condition that is absent in the right valve. The right valve is indented slightly along the ventral margin while the left valve is correspondingly convex in this region. Both valves are notched in the area of the siphons and both have rather heavy growth rings. The ligament is recessed internally in a deep pit, but can be seen from an external dorsal view. It is ap- proximately 1.1 cm long on the large specimens. Mantle cavity Tagelus californianus (Fig. 1). The FEEDING IN TAGELUS AND FLORIMETIS 3 OD fee № N FIG. 2. Organs of the mantle cavity of Florimetis obesa viewed from the right side. Right valve and mantle lobe removed. Arrows indicate the direction of particle movement. MF—mantle fold. For other abbreviations see Fig. 1. 3 A B С FIG. 3. Transverse section of the gills of A. Tagelus californianus. В. Florimetis obesa, and С. Macoma nasuta. Arrows indicate direction of major currents, solid circles indicate currents toward the mouth. Stippled area is the body and foot. demibranchs are large and _ elongated while the labial palps are small. The relationship of the ctenidia and labial palps is of category Ш, i.e., the anterior filaments of the inner demibranch are not inserted into the distal oral groove (see Stasek, 1963). Well developed marginal grooves are present on both demibranchs (Fig. 3A). As in most other tellinaceans a FIG. 4. Inhalant siphons of A. Tagelus californianus and B. Florimetis obesa. cruciform muscle is present but a mantle fold, present in Florimetis obesa and many others, is lacking. The ciliary feeding and rejection currents are shown in Fig. 1. Particles move in a ventral direction on the outer demibranch. When they reach the ventral edge of this structure, they move in 1 of 3 different directions. Some particles enter 4 R. H. POHLO the marginal groove and move toward the mouth. Others move ventrally onto the inner demibranch. The material may also move under the outer demibranch, then dorsally toward a food tract on the axis and then move toward the mouth (Fig. 3A). Once particles reach the labial palps, they move either in an anterior direction, perpendicular to the long axis of the palp plications, toward the mouth, or in a posterior direction parallel to the plications. Small particles combine these 2 movements, i.e., move a short distance parallel to the plication, then change directions and move perpendicularly to the plication. Rejected material moves to the anterior margins of the labial palps and then moves ventrally towards the foot. Eventually these particles accumulate as pseudofeces below the base of the inhalant siphon. Florimetis obesa (Fig. 2). The demibranchs are quite large while the labial palps vary in size from specimen to specimen. The labial palps are shown approximately at their maximum size in Fig. 2. The gill labial palp association is of type Ш, as described above for Tagelus californianus. The outer demibranch is upturned as shown in Fig. 3B. From this figure it can be seen that although the outer-demibranch is upturned, it is not flattened against the body as in Macoma nasuta (Fig. 3C). The plications are ex- tremely fine on both demibranchs. As in the case of T. californianus a cruciform muscle is present. Ciliary currents are shown in Fig. 2. Material moves from the outer demibranch to the ctenidial axis. Here the particles move either in an anterior direc- tion toward the mouth or they continue ventrally on the inner demibranch to a very small marginal groove and then toward the mouth. Particles are then further sorted on the labial palps. Accepted particles can move either perpendicular (i.e., in a dorsal direction) or parallel (i.e., in a posterior direction) to the long axis of the palp plications. Rejected materials move to the anterior edge of the labial palps and then ventrally on to the foot. From here, these particles move in a posterior-ventral direction and eventually accumulate beneath the mantle fold in what Yonge (1949) terms the waste canal. Siphons Tagelus californianus (Fig. 4A). The siphons are separate as they are in Florimetis obesa. The exhalant siphon contains 6 small blunt lobes, as in many of the Tellinacea. The entrance to the in- halant siphon also has 6 lobes but on these lobes are rudimentary straining tentacles. A similar condition was described but not illustrated for Solecurtus scopula by Yonge (1949). Florimetis obesa (Fig. 4B). The inhalant siphon has 6 lobes that are drawn out into finger-like processes. There are no ten- tacles present on these lobes. The exhalant siphon is devoid of lobes. Stomach In both Tagelus californianus and Florimetis obesa the stomach is characterized by the major typhlosole (T) and its corresponding intestinal groove (IG) entering both the right and left caeca (RC, LC). This feature classifies both of these species as possessing stomach type V (gastropemptan, see Purchon, 1960). Tagelus californianus (Fig. 5). The dor- sal hood (H) is quite large and elongated, being a prominent feature of the left side of the stomach. There is also an extension of the stomach on the right-posterior side, which appears somewhat similar to what Purchon (1963) describes as a depression (D) on the posterior wall of Egeria radiata. It is much less drawn out to the side than the dorsal hood but it has a much greater ventral extent. The function of this embay- ment appears to be for temporary storage of sand grains, for they are often located in this area. Grooves and ridges (G) are located near the entrance to and deep within this structure. There is an appendix (X) resembling a cluster of grapes located posteriorly, which also contains sand grains, The major typhlosole and intestinal groove pass anterio-dorsally from the FEEDING IN TAGELUS AND FLORIMETIS 5 ST RG O ; 4 | He FIG. 5. Stomach of Tagelus californianus. Gastric shield removed. Arrows indicate direction of particle movement. Dotted arrows indicate movement on the underside of the structure. D—depression; G—irregular grooves and lobes; H—dorsal hood; IG—intestinal groove; LC—left caecum; LP—left pouch; MG—mid gut; O—oesophagus; RC—right caecum; RG—rejection groove; SA—sorting area; SS—style sac; ST—shield tract; T—major typhlosole; T—minor typhlosole; X—appendix. RG О Imm FIG. 6. Stomach of Florimetis obesa. Gastric shield removed. Arrows indicate direction of particle movement. Dotted arrows indicate the movement on the underside of a surface. PP—posterior pouch; SG—sorting groove; XO—opening to appendix. For other abbreviations see Fig. 5. 6 В. Н. POHLO midgut (MG) into the stomach and enter the right caecum. They then enter the left caecum dorsally from the right side and go very deeply into this structure. In both caeca the typhlosole is upcurled and sends flares into the caecal ducts to form a type C sorting mechanism (see Reid, 1965). A minor typhlosole (t) originates at the beginning of the midgut and terminates on the posterio-ventral floor of the stomach. The style sac (SS) and midgut are conjoined. The dorsal hood receives a curved por- tion of the gastric shield, as does the left pouch (LP). There is a sorting area, the shield tract (ST), in this structure and particles move out of the dorsal hood via a rejection groove (RG). Particles move from the rejection groove to the intestinal groove and then to the midgut. This condition was also found by Reid & Reid (1969) for 8 species of Macoma. The left pouch is also large and it has a sorting area on its ventral side. It contains about 6 openings to the digestive diverticulum. Florimetis obesa (Fig. 6). The stomach of this species is similar to that of Tagelus californianus. The main difference is that F. obesa has a prominent triangular struc- ture on the posterior margin near the appendix (X). A portion of the gastric shield enters this structure and, like the appendix, contains sand grains. This struc- ture is here referred to as the posterior pouch (PP). This structure seems to be more involved in anchoring the gastric shield than as a temporary storage area for sand grains. Other differences from the stomach of Tagelus californianus are: the appendix has finger-like extensions; the dorsal hood (H) is smaller and contains no sorting area, and the right depression is absent, while a posterior sorting groove is present. FEEDING OBSERVATIONS The behavior of the siphons was quite different in the 2 species. The inhalant siphons of many specimens of Tagelus californianus were observed to be т motion much of the time. The species were observed in a stream-like portion of Mugu Lagoon where the water has a unidirec- tional flow either coming in or going out with the tide. Specimens of T. califor- nianus would thrust the inhalant siphon against the direction of water flow and curl back the tentacles exposing а trumpet- shaped opening to these currents. In this position the siphon would be about 1-3 mm above the level of the substratum. After 30 sec. to 1 min. the siphon would move below the level of the substratum. ‘Subsequently it re-emerges and this behavior is repeated. When withdrawn into the burrow, the siphons are partially closed. At this point the incipient tentacles (Fig. 4A) may help to keep deposits from entering. These tentacles, of course, can perform no straining function while the siphon is open wide, and clumps of algae about 1-2 mm in diameter that were carried along by the current were seen to enter the siphons. At no time did the animal press the inhalant siphon to the substratum and ingest deposits, and only material suspended in the water column was seen to enter. In most specimens of Florimetis obesa the inhalant siphon was oriented just below the level of the substratum. Others held this siphon slightly above the level of the substratum and in a few it was below the substratum in a small pit. The inhalant siphon was not active, remained in one spot and was usually partially closed. The species was never observed actively in- gesting deposits as is commonly seen in Масота пазиа (MacGinitie, 1935), Масота secta (Reid & Reid, 1969), and in species of Tellina, Macoma, Scrobicularia and Abra (Yonge, 1949). The mantle cavity and stomach of Tagelus californianus contained only a few sand grains. The stomach contained many diatoms and a lot of green debris, probably derived from various algae other than diatoms. The feces were compact and contained a few sand grains. Fine sand grains were usually present in the mantle cavity of Florimetis obesa especially in the area of pseudofeces ac- cumulation just below the mantle fold. The gills were usually free of sand but FEEDING IN TAGELUS AND FLORIMETIS ih there was some present at the margins of the labial palps. The stomach often con- tained sand. From visual estimates the amount of sand was less than that in deposit feeders such as Macoma secta or Macoma nasuta, but more than in organisms such as Tagelus californianus or Donax gouldi. The stomach also contained diatoms, flagellates and а considerable amount of green debris. The feces were well compacted and contained a few sand grains. DISCUSSION The study of the behavior of the in- halant siphon and of the contents of the mantle cavity and alimentary tract show that material suspended in the water column rather than deposits is the main source of food in Florimetis obesa and Tagelus californianus. The orientation of the siphons in T. californianus does not permit a large quantity of deposits to drop passively into the inhalent opening. Although the siphons are often wide open they are slightly above the substratum allowing only suspended material to enter. The paucity of sand in the mantle cavity and stomach also supports the view that feeding is on suspended material. In Florimetis obesa the siphons are flush with or just below the substratum and this allows deposits to fall into the inhalant opening, the tentacles being incapable of rejecting this material. An analysis of the mantle cavity and stomach contents is consistent with this view and shows that deposits can and do fall into the inhalant aperture and find their way into the stomach. But the quantity of diatoms and algae in the stomach indicates that most of the food comes from material suspended in the water. Both of these species, therefore, would be classified as non-selective suspension feeders with Tagelus califor- nianus ingesting less and F. obesa in- gesting more deposits. Having established the feeding type of these organisms it is of interest to see which features of morphology and behavior are associated with deposit or suspension feeding. Yonge (1949) has indicated that the following features are associated with deposit feeding (some of these features are illustrated in Fig. 7A, which shows Macoma nasuta, a deposit feeding tellinacean): i) the presence of separate inhalant and exhalant siphons and the absence of true straining tentacles on the inhalant siphon; ii) a mantle fold is present and this allows a powerful flow of water to continue but prevents the pseudofeces from fouling the ctenidia; iii) there appears to be a tendency to keep the gill as small as possible in view of the problems presented by a large influx of material; iv) the outer demibranch is upturned to pre- vent clogging when immense quantities of bottom material are taken in; v) a marginal groove is absent and this is associated with the need to reduce the volume of material carried forward. To this list I would add that where the gills are small in such deposit feeding forms as Macoma secta, M. nasuta, and M. balthica the labial palps are large. Also the deposit feeding Tellinacea lie on their side in the substratum. According to Yonge (1949) suspension feeders have some of the following characteristics (some of the general features are illustrated in Fig. 7B, which depicts Donax gouldi, a suspension feeding tellinacean): straining tentacles present on the inhalant siphon; the lack of a mantle fold, indicating a gentle inflow of water, and a large dorsal hood. Also, from the above mentioned features that are correlated with deposit feeding I reason that the presence of a marginal groove(s), large ctenidia with an outer demibranch that is not reflected, small labial palps and an upright position in the burrow are also features associated with suspension feeding. These features are noted in Donax gouldi (Pohlo, 1967) and other non- tellinacean suspension feeders such as Protothaca, Treses, Chione, ес. This study shows that Tagelus califor- nianus has none of the features that would be directly associated with deposit feeding, with the exception of separate siphons, a condition that is universal in the 8 R..H..POHLO FIG. 7. Generalized diagram showing some features of a deposit feeder (A) and a suspension feeder (B). A. Macoma nasuta. Note the up-turned outer demibranch (OD), mantle fold (MF) and the size relations of the demibranchs (ID and OD) compared with the labial palps (LP). B. Donax gouldi. Note that the outer demibranch (OD) is not upturned, the lack of a mantle fold and the size relations of the demibranchs (ID and OD) compared with the labial palps (LP). For other abbreviations see Fig. 1. Tellinacea. The features it shares with suspension feeders are: large gills, outer demibranch not upturned; relatively small labial palps; the presence of marginal grooves; straining tentacles (although in- cipient); the absence of a mantle fold, and a large dorsal hood. The organism is in an upright position in the burrow. Florimetis obesa resembles a deposit feeder by having the outer demibranch upturned. However, it is not flattened against the body as in Macoma secta or M. nasuta (compare Fig. 3B and 3C). A mantle fold is present while straining tentacles on the inhalant siphon are ab- sent. Also, these species lie on their side. FEEDING IN TAGELUS AND FLORIMETIS 9 This species resembles a suspension feeder by having relatively large ctenidia, and a small marginal groove is present on the inner demibranch. In many specimens the labial palps are large but in others they are small. Therefore, this characteristic cannot be associated solely with deposit or suspension feeding. ACKNOWLEDGEMENTS I wish to thank Dr. Marvin Cantor and Dr. Joseph Moore for reading the manuscript. LITERATURE CITED BRAFIELD, A. W. & NEWELL, G. E., 1961, The behavior of Macoma БаШиса (L.) J. mar. biol. Assoc. U. K., 41: 81-87. HOLME, №. A., 1961, Notes on the mode of life of the Tellinidae (Lamellibranchia). J. mar. biol. Assoc. U.K., 41: 699-703. JORGENSON, C. B., 1966, Biology of Suspen- sion Feeding. Pergamon Press, New York. 357 p. MACGINITIE, G. E., 1935, Ecological aspects of a California marine estuary. Amer. М. Natur., 16: 629-765. MAURER, D., 1967, Mode of feeding and diet, and synthesis of studies on marine pelecy- pods from Tomales Bay, California. Veliger, 10:72-76. McLEAN, J. H., 1969, Marine shells of south- ern California. Los Angeles County Museum of Natural History. Science Series 24, Zoology No. 11 (104 р, 54 text fig). MORTON, J. E., 1960, Mollusca: An Intro- POHLO, R. H., 1966, A note on the feeding behavior in Tagelus californianus (Bivalvia: Tellinacea). Veliger, 8: 225. POHLO, R. H., 1967, Aspects of the biology of Donax gouldii and a note on the evolution in Tellinacea (Bivalvia). Veliger, 9: 330-337. POHLO, R. H., 1969, Confusion concerning deposit feeding in the Tellinacea. Proc. malacol. Soc. London, 38: 361-364. PURCHON, R. D., 1960, The stomach in the Eulamellibranchia: stomach types IV and У. Proc. 001. Soc. London, 35: 431-389. PURCHON, R. D., 1963, A note on the biology of Egeria radiata Lam. (Bivalvia, Don- acidae). Proc. Malacol. Soc. London, 35:251- DL: REID, R. G. B., 1965, The structure and funct- ion of the stomach in bivalve molluscs. J. Zool., 147: 156-184. REID, R. G. B. & REID, A., 1969, Feeding processes of members of the genus Macoma (Mollusca: Bivalvia) Can. J. Zool., 47: 649- 657. STASEK, С. R., 1963, Synopsis and discussion of the association of ctenidia and labial palps in the bivalved Mollusca. Veliger, 6(2): 91-97. WADE, B. A., 1965, Notes on the Ecology of Donax denticulatus (Linné). Proc. Gulf Caribb. Fish. Inst., 17th Annual Session, p 36-41. WEYMOUTH, F. W., 1920, The edible clams, mussels and scallops of California. Fish. Bull., Sacramento, no. 4. YONGE, C. M., 1949, On the Structure and Adaptations of the Tellinacea, Deposit- feeding Eulamellibranchia. Phil Trans. Roy. Soc., B., 234: 29-76. YONGE, C. M., 1952, Studies on Pacific coast mollusks. IV. Observations on Siliqua patula Dixon and on the evolution within the duction to their form and functions. Harper. Solenidae. Univ. Calif. Publs. Zool., 55: 232 p. 421-438. ZUSAMMENFASSUNG NAHRUNGSAUFNAHME UND FUNKTIONALE MORPHOLOGIE DES ERNAHRUNGSTRAKTES BEI TAGELUS CALIFORNIANUS UND FLORIMETIS OBESA (BIVALVIA: TELLINACEA). R. H. Pohlo Eine Untersuchung wurde vorgenommen, Tagelus californianus (Conrad 1837) und Forimentis obesa (Deshayes 1855) mit anderen Arten der Oberfamilie Tellinacea zu vergleichen. Ihre Nahrungsaufnahme wurde beobachtet und versucht, Einzelziige ihrer Morphologie mit ihren Ernahrungsgewohnheiten in Verbindung zu bringen. 10 В. Н. POHLO Gelánde- und Laboratoriumsbeobachtungen, besonders der Funktion des Branchialsiphos, und Untersuchungen der Mantellhöhle und des Mageninhaltes wurden vorgenommen, um die Art Nahrungsaufnahme bei diesen Arten festzustellen. Obwohl viele Tellinaceen Schlammfresser sind, nehmen diese zwei Arten hauptsächlich suspen- dierte Teilchen auf. Allerdings tritt auch Schlamm in den Branchialsipho ein. Dies geschieht bei Florimetis obesa in starkerem Masse als bei Tagelus californianus. Tagelus californianus ähnelt anderen suspendierte Partikel fressenden Muscheln durch seine grossen Kiemen, die gut entwicktelte Marginalrinnen besitzen. Die äussere Kieme ist nicht aufwärts gedreht. Die Rückenkappe ist gross, an dem Branchialsipho stehen Tentakel, die das einströmende Wasser seihen, das Tier steht autrecht in seiner gegrabenen Höhle und eine Mantelfalte fehlt. Das einzige wichtige Merkmal, das Schlammfresser mit dieser Art gemeinsam haben, sind getrennte Siphonen. Florimetis obesa ahnelt den Schlammfressern dadurch, dass sie aufwärts gewendete äussere Kiemen hat, eine Mantelfalte, getrennte Siphonen ohne seihende Tentakel, und dass der Organismus auf der Seite liegt. Den Arten, die suspendierte Partikel aufnechmen, ähnelt sie nur dadurch, dass sie verhaltnismass ig grosse Kiemen hat. Нд. RESUME ALIMENTATION ET MORPHOLOGIE FONCTIONNELLE ASSOCIEE CHEZ TAGELUS CALIFORNIANUS ET FLORIMETIS OBESA (BIVALVIA: TELLINACEA). R. H. Pohlo Une étude comparative a été faite entre 2 espèces, Tagelus californianus (Conrad 1837) et Florimetis obesa (Deshayes, 1855) avec d'autres représentants de la supertamille des Tellinacea. La nature de leur alimentation a été recherchée et on a tenté d'établir une relation entre leur morphologie et leur mode de nutrition. Des études dans la nature et au laboratoire, en particulier sur le comportement du siphon inhalant et l'analyse de la cavité palléale et des contenus stomacaux ont été effectués pour s'assurer du mode alimentaire de ces espèces. Bien que beaucoup de Tellinacea soient des déposivores, ces 2 езрёсез se nourrissent en premier lieu de particules en suspension. Les dépéts, cependant, peuvent tomber dans le siphon inhalant, et effectivement le font. Ceci est plus manifeste chez Florimetis obesa que chez Tagelus californianus. Tagelus californianus ressemble aux bivalves suspensivores par ses grandes cténidies qui possedent des sillons marginaux bien développés, la demibranchie externe поп relevée, le capuchon dorsal développé, l'existence d'une ébauche de tentacules filtrants sur le siphon inhalant, le fait que l'animal est placé verticalement dans son trou et l'absence de bourrelet palléal. Le seul caractère important commun entre cette espèce et les deposivores est la séparation des siphons. Florimetis obesa ressemble aux déposivores par les demibranchies externes relevées, la présence d'un bourrelet palléal, les siphons séparés mais sans tentacules filtreurs et le fait que l'animal est couché sur le côté. Il ressemble aux suspensivores par ses cténidies relativement grandes. А ВЕЗОМЕМ MORFOLOGIA FUNCIONAL ASOCIADA А LA ALIMENTACION EN TAGELUS CALIFORNIANUS Y FLORIMETIS OBESA (BIVALVIA: TELLINACEA) R. H. Pohlo Este estudio compara dos especies, Tagelus californianus (Conrad), 1837 y Florimetis FEEDING IN TAGELUS AND FLORIMETIS obesa (Deshayes), 1855, con otros miembros de la superfamilia Tellinacea, e investiga aspectos de sus morfologías relacionados con el comportamiento alimenticio, en estudios de campo y laboratorio, especialmente el comportamiento del sifón inhalante, análisis de la cavidad paleal y contenido estomacal. Aunque muchos Tellinacea se alimentan de sedimentos, estas especies lo hacen de materiales es suspensión; sin embargo, substan- cias de deposito pueden caer, y también se encuentran, en los sifones inhalantes. Esto cuenta más en Florimetis obesa que en Tagelus californianus. Tagelus californianus se asemaja a otros bivalvos que se alimentan de materias en suspensión, por tener largos ctenidios con surcos marginales bien desarrollados, demibranquia externa no doblada hacia arriba, largo capuchón dorsal, tentaculos filtradores incipientes en el sifón inhalante, sin replieque paleal, y el animal se mantiene vertical en la cavidad del substrato donde se aloja. El único, y principal caracter, común a estos dos especies y los sedimentivoros, es la de poseer sifones separados. Florimetis obesa se asemeja a los sedimentivoros por tener las branquias dobladas hacia arriba, repliegue en el manto, sifones separados con tentaculos filtradores, y el animal descansa de costado en el habitáculo. Pero, como los que se alimentan de materias suspendidas, tienen los ctenidos relativamente grandes. ТЛВ. АБСТРАКТ ПИТАНИЕ И СВЯЗАННАЯ С НИМ МОРФОЛОГИЯ TAGELUS CALIFORNIANUS И FLORIMETIS ОВЕЗА (BIVALVIA: TELLINACEA) Е. Хх. РОЛО Сравнивали 2 вида: Tagelus californianus (Conrad, 1837) и Florimetis obesa (Deshayes, 1855) с другими членами надсемейства Tellinacea. Исследована их природа питания и сделана попытка связать аспекты их морфологии с поведением питания. Проведены полевые и лабораторные исследования для выяснения способа питания этих видов и действия дыхательного сифона, сделан анализ мантийной полости и содержимого желудков. Хотя многие ТеШтасеа питаются. осадком, эти 2 вида первично питаются взвешенными частицами. Осадки, однако, могут попадать и попадают в дыхательные сифоны. Это в большей степени свойственно Florimetis obesa, чем Tagelus californianus. Tagelus californianus напоминает двустворок-сестонофагов наличием крупного ктенидия, снабженного хорошо развитыми маргинальными бороздами, наружным жаберным листком, не повернутым вверх, зачаточными щупальцами на дыхательном сифоне, вертикальным положением животного в ходе и отсутствием мантийной скдадки. Единственный существенный признак, общий для этого вида и для детритоедов, - раздельные сифоны. Florimetis obesa схож с детритоедами тем, что наружный жаберный листок его повернут вверх, имеется мантийная складка, на раздельных сифонах отсутствуют щупальца, а само животное лежит на боку. С сестонофагами его сближают относительно широкие ктенидии. Z.A.F. 11 MALACOLOGIA, 1973, 12(1): 13-46 MOLLUSC-SEDIMENT RELATIONSHIPS IN NORTHWESTERN BUZZARDS BAY, MASSACHUSETTS, U.S.A. Egbert G. Driscoll and Dale E. Brandon! Department of Geology, Wayne State University, Detroit, Michigan 45202 and Departmeni of Meteorology and Oceanography University of Michigan, Ann Arbor, Michigan 48104 ABSTRACT Four facies are defined in the Recent sediments of the north-western part of Buzzards Bay, Massachusetts. These are characterized by differences in mean grain diameter, sor- ting, silt-clay content and fauna. A mean grain diameter of less than 2.5ф(0.18 mm )is characteristic of three of these facies which are found in protected areas. The fourth, developing on current-swept bottoms, typically is composed of coarser sediments. Calcium carbonate content of the sediment is a reflection of dead shell abundance throughout the area. Faunas of the 3 fine-grained facies are characterized respectively by (1) Nucula proxima, (2) Yoldia limatula and Nassarius trivittatus and (3) Macoma tenta, Nucula proxima, Eupleura caudata and Nassarius trivittatus. No more than 8 species compose 1% or more of the molluscan fauna in any of the 3 fine-grained facies. In the coarser sediments of the 4th facies 11 species comprise in excess of 1% of the molluscs. Dom- inant species in this facies are Nassarius trivittatus, Anachis avara similis, Chaeto- pleura apiculata, Anadara transversa and Crepidula fornicata. The distribution of more than 35 molluscan species is discussed. The majority have hard parts which are potentially preservable. Mean grain diameter, abundance of silt and clay, and presence of dead shells are important factors in molluse distribution. Macoma tenta, Yoldia limatula, Nucula proxima and Solemya velum increase in abun- dance with decreasing mean grain diameter and increasing silt-clay content of the sedi- ment. Chaetopleura apiculata, Anadara transversa, Crassinella mactracea and many other species increase in abundance with increasing mean grain diameter and decreasing silt-clay content of the sediment. Greater abundance and diversity of epifaunal species is found on bottoms having higher concentrations of dead shells. Potential faunal-lithic associations, indicate that suspension feeding bivalves and carnivorous gastropods are available for preservation in the coarse-grained facies. Poten- tial fossils of the proto-graywacke, which makes up the 3 fine-grained facies, are mostly deposit feeding bivalves. INTRODUCTION Relationships between benthos distribu- tion and various characteristics of the bottom sediment have been of interest to ecologists for many years. Recent work in this area includes that of Bader, 1954; Craig & Jones, 1966; Gamulin-Brida, 1967; Parker, 1956, 1963; Peres & Picard, 1964; Purdy, 1964; Rhoads & Young, 1970; Sanders, 1958, 1960; Thorson, 1966; and others. The present paper examines certain of these relationships in a shallow bay off the Massachusetts coast. The principal in- vertebrate group with hard parts suitable for preservation in the fossil record in this area is molluscs, despite the much greater numerical abundance of such in- vertebrates as polychaetes, unsegmented worms, and crustaceans. The latter taxa are of considerable ecologic and paleo- ecologic importance, particularly as regards reworking of the sedimentary sub- stratum, but are unlikely to be preserved in the fossil record except as trace fossils. Our efforts are directed toward presenting a picture of the distribution and sediment- 'Present address: Esso Production Research Co., P.O. Box 2189, Houston, Texas 77001 14 DRISCOLL AND BRANDON fauna relations of living forms which might be preserved. Consequently, only molluscs are considered. Furthermore, only large and abundant species are treated in any detail. These are the forms which make up the bulk of the macroinvertebrate assemblage. The present study of a limited shallow water area off the Massachusetts coast was initiated in 1965. The area is located in the north-western part of Buzzards Bay (Fig. 1). Certain characteristics of this area make it particularly interesting. A diver- sified fauna is present, coves and headlands provide numerous protected and open environments for benthic in- vertebrates, and there is a variety of clastic sediment types. The distribution and abundance of molluscan species are considered in rela- tion to the maximum and minimum mean grain diameters of the sediments in or on which they are found, as well as in relation to the maximum and minimum silt-clay contents of the substratum. Scatter diagrams of species abundance versus mean grain diameter and silt-clay content are presented. Potential faunal-lithic associations are discussed. METHODS Fifty-four stations were sampled within the study area. Station locations were determined from a plot of random numbers on a grid overlay of the area (sta. 51-54 are exceptions and are not randomly located). Two sediment samples of ap- proximately 100 g each were collected by divers at each station. Samples were taken approximately 4 m apart, the position of the anchor serving as an arbitrary mid- point between them. Sedimentary parameters presented here (Table 1) are mean values of the 2 samples. Faunal samples were collected by a modified scallop dredge equiped with additional weight on the front part of the towing bar, 8 cm teeth on the cutting edge, and 2 mm mesh netting backed by coarser net and a chain link bottom. Observation of the dredge on various substratum types by SCUBA divers in- dicated that a continuous and even bite was obtained by appropriate variations in the length of the tow line. Samples were sieved on 2 mm mesh screens. Molluscan abundances reported here are the sum of 2 dredge hauls taken at each station. Each dredge haul was for 1.5 min at a slow and constant speed. Diver observation at a number of stations indicated that the 70 cm wide dredge covered a distance of approximately 50 m in this time interval. This sampling procedure is, at best, semi-quantitative. It was utilized because no type of grab sampler, nor any more sophisticated dredge of the epibenthic sled type (Hessler & Sanders, 1967) backed with fine mesh netting or canvas can provide data on the abundance of the large and widely scattered faunal elements for- ming a significant portion of the fauna examined here. Because of the sampling errors inherent in our dredging technique, no data are presented here on animal abundance per unit area. All samples are assumed to be of approximately equal size and only relative abundance of the various species in and on different substrata is discussed. Figs. 10-32, in which numbers of specimens are indicated, were con- structed from the total number of specimens taken in both dredge hauls at each station. They are intended to demonstrate relative abundance only and not absolute abundance per unit area. Mechanical size analysis of the sediments was carried out by standard techniques. U.S. Standard Sieves arranged according to the Wentworth grade scale were utilized in separation of the coarser fractions. Size analysis of the silt and clay fraction was accomplished with an ASTM hydrometer 152H. Calcium carbonate content was determined from aliquots of the sediment samples by dry weight difference before and after digestion in dilute НС]. The phi ($) scale is utilized here in the treatment of sedimentary data and the comparison of such data with benthos distribution patterns. This scale was developed by Krumbein (1934) as a MOLLUSC-SEDIMENT RELATIONSHIPS 15 \ y || | | NN) | /. | Pass ja Nautical mile ads 4 3 44 43 42 e 454 A 404 Nautical mile 44 43 —— 205 00 05 10 “Le 150 25 30 35 MEAN GRAIN DIAMETER - РН! FIG. 1. Index map of the study area. General locations is in the northwestern part of Buzzards Bay, Massachusetts, U.S.A. Station numbers are indicated. FIG. 2. Mean grain size distribution map. Grain size is given in phi units. FIG. 3. Per cent silt-clay distribution. The offshore concentration of silt-clay corresponds with a portion of the Pleistocene drainage pattern. FIG. 4. Relationship between % silt-clay content of the sediment and mean grain diameter in phi units. 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The phi scale has integers for Wentworth scale class limits and increases with decreasing grain size (1 mm = 09; 0.5 mm = 19; 0.25 mm = 2¢; 0.12 mm = 39; etc. ). The sorting or spread of the sediment is described in terms of the Trask sorting coefficient. This measure has been used extensively in classical studies of sediments and may be easily converted to other types of sorting measures by graphical methods (Krumbein & Pettijohn, 1938). GENERAL GEOLOGY The geologic framework of Buzzards Bay has been examined by Hough (1940), Mather, Goldthwait & Thiesmeyer (1942), Moore (1963) and others. Sediments of the bay are derived from glacial moraine. The great majority of rock types, both in Buzzards Bay sediments and in local moraine, consist of granite, gneissic granite and gneiss. The Dedham granodiorite undoubtedly acted as an im- portant glacial source area for much of this material. The petrology and chemistry of Buzzards Bay sediments have been dis- cussed by Moore (1963) who also deter- mined that a dentritic Pleistocene stream pattern is still present on the floor of the bay and is of considerable importance in controlling sediment distribution. SEDIMENT DISTRIBUTION Moore (1963) has demonstrated the importance of tidal currents and bottom topography as factors affecting sediment distribution in Buzzards Bay. He observed a general correspondence between strong tidal currents and coarse detritus. He also suggests that deeper troughs, commonly reflecting the Pleistocene drainage pattern, act as traps for fine sediment. We confirmed a general correspondence between coarser clastics and stronger tidal currents as recorded by Moore. Deviations from this pattern would seem to be due partially to the fact that Moore recorded only surface currents. Using SCUBA, we noted that in some areas the bottom current direction deviated considerably from that of the surface currents, although they were generally in close agreement. We also observed that deeper waters, par- ticularly those in the southeastern portion of the area, act as sediment traps for the finer-grained sediment. We suggest, however, that tidal currents and bottom topography are not sufficient to complete- ly explain sediment distribution in the bay and that wind action, particularly in nearshore areas, is a significant factor. The prevailing wind direction is from the southwest. Waves generated by this wind introduce high energy conditions in shallow water areas which are unprotected by headlands. These higher energy con- ditions are clearly reflected in a correspon- ding coarseness of the sediment in such areas. Mean grain size and the percentage of silt-clay distributions are shown in Figs. 2 and 3 respectively. It is apparent, from an examination of these figures, that a greater amount «of fine sediment ac- cumulates on the southwesterly than on the northeasterly margins of the harbors and coves that comprise the northwestern border of the bay. The headlands project southeastward into the bay and are characterized by rocky points and an abundance of eroded boulders, derived from wave reworked glacial moraine, which act as natural riprap along their southwestern shores. The very coarse detritus occurring near the southwest shore of Sippican Neck, Sta. 41 (Fig. 2), is a result of wave action upon a number of such boulders which occur in this area. The relationship between mean grain diameter and silt-clay content at all stations is shown in Fig. 4. Distribution of sorting is illustrated in Fig. 5. Although the sorting pattern described within the same area by Moore (1963) was based upon only 11 stations, the distribution described here, based upon 54 stations, is not markedly different. Refinements of the sorting distribution pattern have been possible, but our work does not affect the general distribution described by Moore in any significant manner. The areal distribution of calcium car- 20 DRISCOLL AND BRANDON Nautical mile Nautical 404 COEFFICIENT wo wo Le o — SORTING m u = LI 2.07 a oe ae = ai $? un. о Nautical т т r + = > —__—_— =0S 00/07 40,5 0. 1.5 20-25 30155 MEAN GRAIN DIAMETER — PHI FIG. 5. Sediment sorting. Isopleths are drawn in terms of standard deviations. Stippled area has sorting values in excess of one standard deviation. FIG. 6. Distribution of calcium carbonate (% by weight of total sediment) in area of study. Isopleths are drawn with increments of 2%. FIG. 7. Facies distribution within the area of study. Vertical and horizontal cross-hatch pattern indicates the shallow protected facies (1), stippled pattern indicates the nearshore facies (II), diagonal lines indicate the open bay facies (III), and narrow horizontal lines indicate the offshore facies (IV). FIG. 8. Relationship between Trask sorting coefficient and mean grain diameter in the 4 facies recognized within the area. Symbols are: black circles, open bay facies; black squares, nearshore facies; black triangles, offshore facies; open circles, shallow protected facies. MOLLUSC-SEDIMENT RELATIONSHIPS 21 bonate is illustrated in Fig. 6. This dis- tribution pattern corresponds with areas rich in shell material (Driscoll, 1967). FACIES DISTRIBUTION Within the restricted geographic area which has been examined it is possible to recognize 4 distinct facies. Although mix- ing between these facies is occasionally present, each is generally characterized by certain sedimentary parameters and by a characteristic faunal assemblage. The facies are (I) shallow protected; (II) nearshore; (ПТ) open bay; and (IV) offshore (Fig. 7). It should be emphasized that facies boundaries are gradational and are not based on a single characteristic. In order to recognize any given facies it is necessary to examine both the faunal association and the sedimentary parameters. The shallow protected (I), nearshore (11), and offshore (IV) facies are characterized by sediments with a mean TABLE 2. Five species are particularly useful in distinguishing between the 3 facies in which mean grain size is less than 0.18 mm. The normalized % of each of these species which occurs in each of the 3 fine-grained facies is given here. It should be noted that some of these forms also occur, though less commonly, in the open bay facies. In this table the total number of individuals found at the 17 stations representing fine grained facies was taken as 100%. Facies Species Offshore Shallow Protected Nearshore Total (5 Stations) (4 Stations) (8 Stations) Масота tenta leg 4.0 94.3 100.0 Yoldia limatula 50.4 0.0 44.6 100.0 Nucula proxima 0.0 99.4 0.6 100.0 Nassarius trivittatus 78.7 0.7 20.6 100.0 Eupleura caudata 3.3 0.0 96.7 100.0 TABLE 3. Total number of identified species and number of species composing 1% or more of fauna in 4 different facies. Facies No. of No. of Species Species Composing 1% or more of fauna Offshore 16 3 Shallow Protected 19 8 Nearshore 23 m Open Bay 34 1] size of 2.54(0.18 mm) or smaller, and are referrred to here as the “fine-grained” facies. They constitute subdivisions of the Nucula proxima-Nephtys incisa communi- ty defined by Sanders (1958), 1960). These 3 facies are clearly distinct in faunal community and in sedimentary characteristics from the open bay facies (III) which is characterized by sediments with a mean grain diameter larger than 2.59, and is analogous to Sanders (1958, 1960) Ampelisca (amphipod) assemblage. The relationships between the Trask sorting coefficient and the mean grain diameters in phi units for all stations sampled is shown in Fig. 8. The Trask sorting coefficient used here is calculated by determining the square root of the ratio 22 DRISCOLL AND BRANDON of the quartiles (25th and 75th percen- tiles). The larger quartile is taken as the numerator. Sediments from the 3 different “fine-grained facies (I, II, IV) fall into separate areas on this diagram. In all of these, sorting becomes poorer as grain size decreases. Offshore Facies This facies (Stas. 19, 25, 42, 45, 49) is generally characterized by water deeper than 9 m (mean low tide). The sediments are fine sands with a high silt-clay content. Mean grain diameters found at all stations in the offshore facies are smaller than 3.064 (0.125 mm). Sorting of the sediment is better than in the nearshore facies, but is somewhat variable (Trask sorting coefficient 1.40-1.80). The physical conditions producing the offshore facies involve a number of factors. Most impor- tant of these is the presence of a Pleistocene drainage pattern on the floor of Buzzards Bay. This pattern has been documented by Moore (1963) who has also shown that both sediment type and bathymetry are reflections of this sub- merged dendritic stream pattern. Each major inlet to the bay has a trough-like depression extending from the bay to near the mouth of the inlet. Even minor inlets such as those of Wings and Aucoot Coves are reflected by depressions which extend bayward from their mouths (Fig. 9). Moore (1963) has demonstrated that a general correspondence exists between areas of silt-clay deposition and the Pleistocene stream pattern in the deeper portions of Buzzards Bay. The offshore facies corresponds to one of the troughs (stream valleys) indicated by Moore. However, comparison of silt-clay distribu- tion (Fig. 3) and of mean grain size distribution (Fig. 2) with the bathymetry (Fig. 9) in other parts of the study area indicates little correspondence between Pleistocene geomorphology and sediment distribution. In the offshore facies, depth of water is such that the effect of waves on sediment distribution is negligible. Although no bottom current studies have been con- ducted in the bay, Moore (1963) has shown that surface currents have lower velocities in the central portion than in the marginal areas. If a general correspondence between surface and bottom current velocities exists in Buzzards Bay, velocities in the area of the offshore facies are low. The silt and clay-rich sediments of the offshore facies are attributable to 3 factors: (1) the presence of Pleistocene stream valleys which act as sediment traps; (2) the reduced velocity of tidal currents in the central part of the bay; and (3) minimal effects of wave action on the sediments due to water depths. Fauna—Sixteen species were collected from sediments representing the offshore facies. These are listed below. The percen- tage of the offshore molluscan macrofauna attributable to each species is indicated. Nassarius trivittatus 85.3 Yoldia limatula 5.5 Laevicardium mortoni 3.4 — © DOS eee SS Pitar morrhuana Anachis avara similis? Macoma tenta Anadara transversa Ensis directus Lyonsia hyalina Mitrella lunata Pandora gouldiana Anachis avara? Crepidula fornicata Solemya velum Eupleura caudata Retusa obtusa АЛЛА AAN TS IN AN IX FDS, AN Two of these species (Nassarius trivit- tus and Yoldia limatula) make up 90% of the fauna collected. Both are deposit feeders. N. trivittatus is common through- out the area of study but is a more im- portant faunal constituent in the offshore facies than in any other. Examination of Tables 2 and 3 indi- cates that the offshore fauna may be dis- tinguished from that found in the fine sediments of the shallow protected facies by the much larger numbers of Nassarius trivittatus, the abundance of Yoldia lima- tula, and the absence or near absence of MOLLUSC-SEDIMENT RELATIONSHIPS 23 SHE! . IN . Nautical mile и le Nautical mile a le 70° 45' 44 43 42 4 44 43 42 1 1 #(567) (298)8 67)4 RE) D eo! x с I = 20 N o Е < © o o y ES = Е = 54 т | N a 154 n if | < = 9 z < < = 10 = u < о 104 u œ . o ш ao x a = ш > = o z = a 54 в. о 5 | z 5 aes 8 s a a Г . a A . a = . a a a a . s à a | Denn EA u iF Y Y т 10 20 30 40 50 =05) 100 Fos? OMIS (2101 2,577 30 35 PER CENT SILT-CLAY MEAN GRAIN DIAMETER — PHI FIG. 9. Bathymetry. Isobaths are indicated at 1 fathom intervals below mean low sea level. After Coast and Geodetic Survey Chart 251 in part. FIG. 10. Areal distribution of Macoma tenta. Isopleths are drawn at intervals of 100 specimens. Note that this selective deposit feeder is concentrated in the silt and clay rich sediments of the nearshore facies, occurs in sediments of the offshore and shallow protected facies, and is nearly absent from the open bay facies. FIG. 11. Relationship of Macoma tenta to silt-clay content of the sediment. This selective deposit feeder becomes more abundant with increasing abundance of silt-clay. Zero occurrences shown below dashed line. Twenty-five of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens of M. tenta. FIG. 12. Relationship of Macoma tenta to mean grain diameter. The species is uncommon in sediments with a mean grain diameter greater than 0.18 mm (2.5 4). Zero occurrences shown below dashed line. 24 DRISCOLL AND BRANDON Nucula proxima. It may be distinguished from the fauna of the nearshore facies by the somewhat larger numbers of Nas- sarius trivittatus, the absence or near absence of Eupleura caudata and the less abundant occurrence of Macoma tenta. This molluscan fauna is more restricted in number of species than that of either of the other 2 “fine-grained” facies (LIL). Shallow Protected Facies This facies (Stas. 29, 30, 31, 51) is lim- ited to those areas with a water depth of less than 3 m (mean low tide). The sedi- mentary parameters and faunal associa- tions characteristic of the facies are devel- oped in coves and inlets (Fig. 7). The rela- tionship between sorting coefficient and mean grain diameter within this environ- ment is shown in Fig. 8. Sediments are fine grained, not exceeding a mean diameter of 2.59 (0.18 mm). Sediment sorting becomes increasingly poorer with decreasing mean grain diameter but the sorting range is nearly identical to that present in sedi- ments from the offshore facies. Mean diameters of these sediments overlap those found in the offshore facies. However, sediments from the shallow protected facies are consistently somewhat coarser than those with a comparable degree of sorting collected from the offshore facies. Areas in which the shallow protected facies are developed are sheltered from the prevailing southwest wind by headlands. Another factor contributing to low energy conditions is the presence of eel grass throughout major portions of this facies. The eel grass has a net effect of damping wave action on the sediment-water inter- face, thereby insuring a relatively low energy environment. Furthermore, this protection prohibits any substantial addi- tion of coarser sediments from offshore areas during storms. Finer sediments may be moved into this facies from offshore areas via the mechanisms detailed Бу Postma (1967). However, very fine sedi- ment is removed by tidal currents and not replenished from offshore areas. Pre- sumably this is because concentration of the very fine fraction in the shallow pro- tected facies is not accomplished through settling lag and scouring lag (Postma, 1967). Two different sets of physical condi- tions have given rise to similar, though not identical, sediments in the shallow pro- tected ( 3 m in depth) and offshore (9 m in depth) facies. In the shallow protected facies, protection from wave action, and the presence of eel grass are effective in producing low energy conditions which are reflected in a sediment consisting of fine grained, silt and clay-rich sand. Similar sediments of the off-shore facies are accumulated because of the lower energy conditions associated with greater depth, lower current velocities, and the protection afforded by troughs and stream valleys of the Pleistocene drainage system. Fauna—Nineteen species were col- lected from sediments representing the shallow protected facies. These, and the percentage of the shallow protected molluscan macrofauna made up by each species, are listed below: Crepidula fornicata 47.4 Nucula proxima 30.3 Crepidula plana 7.3 Bittium alternatum 4.4 Laevicardium mortoni 3.3 Crepidula convexa 17 Argopecten irradians 1.0 Macoma tenta 10 Nassarius vibex N) Anomia simplex 0 Nassarius trivittatus <0 Solemya velum < 1.0 Mitrella lunata 0 Anachis avara similis? < 10 Lunarca ovalis < 1.0 Busycon canaliculatum < 10 Natica clausa <1:0 Pandora gouldiana <0) Retusa obtusa < 10 Eight of these species comprise more than 96% of the collected fauna. The abundant occurrence of Crepidula (a suspension feeding gastropod) ш this facies is probably the result of the presence of scattered cobbles and boulders through- out the area (particularly at Sta. 31) and MOLLUSC-SEDIMENT RELATIONSHIPS 25 possibly to a profuse growth of eel grass in portions of the environment. These hard surfaces provide points for fixation of Crepidula and other attached epifaunal forms. It has been suggested (Van Straaten & Kuenen, 1958; Rhoads & Young, 1970) that shallow subtidal mud bottoms tend to be stabilized by the binding properties of marsh grass and benthic diatoms. Rhoads € Young (1970) present a convincing argument that stability of the substratum is a controlling factor in the distribution of suspension feeders in Buzzards Bay. It seems probable that the shallow protected facies is less subject to resuspension of sediment than either of the other 2 “fine grained” facies. This appears to be the case despite the fact that Nucula proxima, an active burrowing deposit feeder, is abundant in the shallow protected facies. Examination of Tables 2 and 3 indi- cates that the fauna of the shallow pro- tected facies may be distinguished from that of both the offshore and the near- shore facies by the absence or near absence of Yoldia limatula and by the small numbers of Nassarius trivittatus. Perhaps the single most important faunal criterion for distinguishing this facies from others is the abundance of Nucula proxima. This species makes up approximately 30% of the molluscan fauna of the shallow pro- tected facies but is absent, or nearly ab- sent, from other parts of the study area. Table 2 indicates that over 99% of all Nucula proxima collected were found in the shallow protected facies. It is in- teresting to note that Parker (1956), in his study of the Mississippi delta region, com- ments that Nucula proxima is a form which is characteristic of the deeper con- tinental shelf of the Gulf of Mexico be- tween 24 and 91 meters. Hampson (1971) has distinguished 2 distinct species of Nucula in Buzzards Bay, N. proxima and N. annulata. These appear to be geo- graphically separated in their distribution patterns. It should also be noted that Laevi- cardium mortoni is more common in the shallow protected than in other “fine grained facies and that Macoma tenta and particularly Eupleura caudata are less common than in the nearshore facies. The presence of Bittium alternatum in this fauna is a reflection of the abundance of eel grass in the environment. Nearshore Facies This facies (Fig. 7) is characteristic of harbor mouths which open to the south and are therefore only partially protected from wave action generated by the pre- vailing southwest wind. Stations demonstrating characteristics of the near- shore facies (1, 4, 10, 20, 32, 44, 47, 50) are found in waters of intermediate depths of between 3 and 7.5 m. (Sta. 20, an excep- tion, is discussed below). The relationship between mean grain diameters and sedi- ment sorting in the nearshore facies is shown in Fig. 8. Although these 8 stations have a mean grain size comparable to that of the deep offshore and shallow pro- tected facies (mean grain diameters not larger than 2.54) the sorting is generally poorer than in either of these other “fine grained’ facies. (Trask sorting coefficient from 1.81-2.88. ) Sedimentary parameters of the near- shore facies may be explained by a num- ber of factors. The streams emptying into the harbors in which this facies is de- veloped come from areas of relatively low relief, supplying little or no coarse detritus. Consequently, the area exhibits “fine grained’ sediments. The poorly sorted character of the sediments is due to the ex- posure of this area to variable energy con- ditions. These range from the relative calm of low velocity tidal currents to the violence of storm waves with a wave length of 7 m or more. Moore (1963) indicates that current velocity is reduced near harbor mouths. Consequently, the sorting and washing of sediments which is characteristic of the open bay facies is not found here. In Fig. 7, a band of the nearshore facies is shown on the east side of the study area intermediate between the offshore and open bay facies. This area, which is sug- gested on the basis of a single station (Sta. 20), is the result of gradation between the 26 DRISCOLL AND BRANDON offshore fine grained facies and the coarser sediments characteristic of the open bay facies. The fauna of Sta. 20 is also inter- mediate in nature. Fauna—Twenty-three species were col- lected from sediments of the nearshore facies—more than from either of the other 2 “fine grained” units. These, and the per- centages of the molluscan fauna of the nearshore facies made up by each species, are listed below: Macoma tenta 49.8 Nassarius trivittatus 31.0 Yoldia limatula 6.6 Eupleura caudata 3.4 Laevicardium mortoni 2.8 Bittium alternatum 17 Crepidula plana < 1.0 Anachis avara similis? < 1.0 Solemya velum < 1.0 Crepidula fornicata Nucula proxima Polinices duplicatus Chaetopleura apiculata Lyonsia hyalina Mitrella lunata < 1.0 Pitar morrhuana <1:0 Urosalpinx cinerea LO Lunarca ovalis a1) Pandora gouldiana < 1.0 Mulinia lateralis < 1.0 Anachis avara? =1:0 Argopecten irradians <1.0 Busycon canaliculatum =10 Four species make up over 90% of the fauna. The most important form is Ma- coma tenta. Over 90% (normalized) of all specimens of M. tenta collected were found in the nearshore facies. The fauna may be distinguished from that of both the shallow protected and off- shore facies by the much greater relative abundance of Macoma tenta and Eu- pleura caudata. It further differs from the shallow protected fauna in the near absence of Nucula proxima and from the offshore fauna in the relatively less abun- dant occurrence of Nassarius trivittatus. Open Bay Facies Sands with a mean grain diameter larger than 2.56 comprise the bulk of the sediments in the study area. These sands, found at depths of from 3-9 m, constitute the open bay facies (Fig. 7). With the exception of a few stations having very coarse grained sediments, sorting is better than in the “fine grained” facies (Fig. 8) and further improves as mean grain size decreases. This trend con- trasts with the 3 “fine grained” facies in which sorting becomes poorer as mean grain diameter decreases. These tenden- cies are in agreement with similar observa- tions concerning sedimentation in Buz- zards Bay by Sanders (1958). Inman (1949) suggested that sedi- mentary particles having a diameter of approximately 2.5 ф are more easily trans- ported than coarser or finer sediments. Krumbein & Aberdeen (1937); Hough (1942): Shukri € Higazy (1944) and Sanders (1958) have all described environ- mental situations in which better sorting occurs as transported sediments approach this diameter. Recent experimental work by White (1970) indicates that under certain conditions, sedimentary particles finer than 2.59 become increasingly dif- ficult to transport as grain size decreases. However, it is doubtful that these condi- tions represent a common situation in nature. Postma (1967) and Rhoads & Young (1970) have demonstrated that the energy required for resuspension and transport of silts and clays is correlated with the water content of the sediment. Sediments with a higher water content are more easily trans- ported than those which are more com- pacted. Rhoads & Young (1970) have further shown that reworking of the sub- stratum by deposit feeding organisms is effective in increasing the water content of fine grained sediments. Consequently, the particle size which is most easily trans- ported in any given environment is de- pendent upon a number of variables. In the open bay facies characterized by a near absence of fine grained sediments and a paucity of deposit feeders, it appears that the better sorting of fine sands may be ex- plained on the basis of ease of transport. MOLLUSC-SEDIMENT RELATIONSHIPS 27 The poorest sorting and largest mean grain diameters in the open bay facies are found at Stations 35 and 41. Station 35 is located near the southern entrance to the Cape Cod Canal in an area indicated by Moore (1963) as having high tidal current velocities. It seems probable that the coarse grained, poorly sorted character of sediment at this station is the result of these high velocity currents. Station 41 is located near the southwestern shore of Sip- pican Neck in an area of strong wave action and numerous glacially derived boulders. Sediment in this area is, at least in part, debris accumulated locally from these glacial boulders. These 2 stations are extreme examples of the importance of wave action and tidal current velocity on sedimentary parameters within the study area. At both stations high energy condi- tions prevail. Easily transported detritus approaching 2.56 in diameter is rapidly winnowed out and removed. The coarse and poorly sorted residue at both stations is similar, although it is the result of different physical agents. In general, the sedimentary char- acteristics of the open bay facies are largely attributable to the action of tidal currents. Moore (1963) has indicated that this area is subjected to relatively high cur- rent volocities. Regular fluctuation of these currents results in a washing out of finer sedimentary particles and concentra- tion of coarse grained, well sorted sand. Fauna—Thirty-four species were collected and identified from the open bay facies. These and the percentage of the open bay molluscan macrofauna made up by each species are listed below: Nassarius trivittatus 39.0 Anachis avara similis? 12.6 Chaetopleura apiculata 10.5 Anadara transversa 9.9 Crepidula fornicata 5.1 Eupleura caudata 4.9 Crepidula plana 4.2 Crassinella mactracea 3.6 Laevicardium mortoni 3.4 Anachis avara? 2.5 Yoldia limatula 1.2 Argopecten irradians Mitrella lunata <0 Pandora gouldiana <0 Urosalpinx cinerea < 10 Nucula proxima SLO Anomia simplex < 1.0 Cerastoderma pinnulatum < 10 Lyonsia hyalina < 10 Pitar morrhuana 0 Busycon canaliculatum < 10 Cerithiopsis subulata <1:0 Ensis directus < 1.0 Macoma tenta - 10 Crepidula convexa < 150) Lunarca ovalis SO) Seila adamsi < 1.0 Bittium alternatum то Lunatia triseriata < 0 Mercenaria mercenaria то Modiolus modiolus < 1.0 Natica clausa < 1.0 Spisula solidissima < то Tagelus divisus <1.0 The first 10 of these species make up 91% of the fauna in the open bay facies. These 10 species are suspension feeders, carnivores, herbivores, or non-selective deposit feeders. In contrast to the 3 “fine grained” facies, no selective deposit feeders are important elements of this fauna. The fauna turther differs from those of the 3 “fine grained’ facies in pos- sessing a much higher degree of faunal diversity. This observation is in agreement with Sanders (1968) suggestion that the fauna of stable sand bottoms is probably inherently more diverse than that of mud bottoms. For a more comprehensive treat- ment of faunal diversity of Buzzards Bay see Saunders (1968, 1969). The paleo- ecologic implications of faunal diversity are discussed by Bretsky € Lorenz (1970). DISTRIBUTION OF SPECIES AND SUBSTRATE RELATIONS A faunal list and relevant ecological data are given in Table 4. There are 13 species which individually contribute more than 1% of the total collected molluscan fauna (numbers of specimens) from all of the facies in the study area. These forms are listed below with their respective per- centages. Those species whose feeding 28 DRISCOLL AND BRANDON habits are not fully known are indicated by an asterisk. Bittium alternatum was not included in the percentage calculations, but does occur in enormous numbers in areas of eel grass. Selective Deposit Feeders % Macoma tenta 9.4 Nucula proxima 6.1 Yoldia limatula 2.7 Suspension Feeders Crepidula fornicata 11.5 Anadara transversa 3.0 ° Laevicardium mortoni 2.8 Crepidula plana 3.6 °Crassinella mactracea 2.9 Carnivores and Nonselective Deposit Feeders Nassarius trivittatus 39.5 Anachis avara similis? 6.3 Eupleura caudata 3.0 Anachis avara? ie ° Bittium alternatum - Herbivores and Grazers Chaetopleura apiculata 5.1 The areal distribution of most of these species is illustrated in Figs. 10-32 and is briefly discussed below. Isopleths in the figures refer to the relative density of the animals. Species are grouped according to the similarity of their distribution patterns. The mean grain diameter in which each species is found, the mean silt-clay con- tent associated with each species, the ranges of mean grain diameters, and the ranges of the silt-clay content associated with each species are presented in Figs. 33 and 34. Relationships existing between trophic groups, current velocities, and various sedimentary parameters have been dis- cussed by many writers (Bader, 1954; Sanders, 1958; Purdy, 1964; Craig & Jones, 1966; Jorgesen, 1966; Driscoll, 1969; Rhoads & Young, 1970; Newell, 1971). In Buzzards Bay, infaunal suspen- sion feeders become more abundant in sediments with a mean grain diameter approaching 2.56. Sessile epifaunal suspension feeders are commonly most abundant in sediments with a mean grain diameter coarser than 2.5¢@ and selective deposit feeders in sediments with a mean grain diameter finer than 2.54. Масота tenta. This selective deposit feeder is found in “fine grained” sedi- ments with a relatively high silt-clay con- tent (Fig. 10). Occurrences in the open bay facies, in sediments with a mean grain diameter coarser than 2.59, are unusual. The form reaches maximum abundance in the nearshore facies. Parker (1956) reports M. tenta as being most common in his Upper Sound Division of the Mississippi delta region. Both areas are characterized by sands rich in silt and clay, shallow depths, and salinities somewhat below that of normal sea water. The relationships between increasing silt-clay content of the sediment and in- creasing abundance of М. tenta are il- lustrated in Fig. 11. Inasmuch as the correlation between silt-clay content and mean grain size is high (Fig. 4), it is not unexpected that this species is also found to increase in abundance with decreasing mean grain diameter (Fig. 12). Yoldia limatula. The areal distribution pattern of this selective deposit feeder (Fig. 13) shows a high correlation with the distribution of silt-clay throughout the area (Fig. 3). Maximum occurrences are in areas protected from wave action by headlands (Sta. 50) or in deeper areas removed from the zone of severe wave action (Sta. 19). Presumably this distribu- tion pattern is a reflection of the abun- dance of clay and organic detritus rather than a direct negative response of Y. limatula to moderate wave agitation. Although Hunter € Brown (1964) in- dicate that Y. limatula may occur inter- tidally as well as below the low water mark the species was not found in the shallow protected facies. Depths of only a few feet do not appear to favor abundant develop- ment of the species in the study area. A marked increase in abundance of Y. limatula is found with increasing silt-clay content and with decreasing mean grain diameter (Figs. 14-15). Nucula proxima. Comparison of the areal distribution pattern of the species (Fig. 16) with Fig. 7 and Table 2 indicates 29 MOLLUSC-SEDIMENT RELATIONSHIPS dE cé 8T El GI Ig ST GG OS 6 06 19 L'EL Гб? L OF sre C08 LIT $ 18 886 0'0 99 G VE 2.09 0% $16 US с 66 6 L8 whee) poesind0Q satoads YoryM дв suonelg jo 19qUNN 9dÁ | 3U1p99 SAP +. Peur) oul +A % P>ZIJPULION Te GCL SOL 08SI SIDE ] POUIRIT) duly UT Joaquin М 05 ce 95 0? 34 6F OS СОТ SIG 91% 825 $55 $55 183 OOF 9Lv 96? PSL 006 C606 19QUNN (Aes) vxaquos в] пра) (Avs) ра4аи1э xurd]Dso./) (ARS) wunypusagjpp штчия (Аэ[зигт) рирпулош ри (ABS) DIDUN] 2] 241] (ПА) рирртов Dıopung (PIRE) sunipo.n иаэа4овлу (Au31q1O) ха]4ии$ вииоиу ¿ (ABS) DIDAD SIYIDUY (ABS) pynyvum DIPJOX (релио)) иомош VUNIPADILADD] (A9[SUTT) DIIDAJIDUL 1] ] 2185040) (ABS) DSLIASUDA] DIDPDUY (ABS) pjppnpo panajdny (Avg) рир]А njynpidasy (Aes) pypjnaidn pinajdojany) (Aes) риихолА в]пэпм (JOUSABY) ¿SINUIS DADAD SIYIDUY (ABS) DJu2] DWOIDWN (snaeuur]) ррроимо{ DjNpidaty (ABS) snypymanı) SNUDSSDN sonadg "Н ‘oloarqioy snoseydomew ©) “SOJOATUIBO "СМ 'S19P99F изо4эр элцоз[эзиои “HAS ‘лэрээ} JISOdIP эл123|э$ “HS ‘sdopoo} uorsuadsns todÁy Зитрээ} sjuosoidoi € ишиоо) SSA] 10 © SI speunur Jo 19QUINU 24} Чощл UL satoads 10} payepnoyeo jou эле 5эЯвиэолэ4 ‘Sole Áeq uodo oy} о} рэле од $э1ову pouress эцц $ dy) ur 1495944 э8езиэолэа p>z1feuniou a} SI ф UWINJOD ‘(элоЦ5лвэц pur ‘эдоЧ$}уо ‘popojoid моеЧ$) зэюв} (65 ох) UTeIB auf gay} UL рэзоэЦоо spenprarpur jo зэдшии ou} st © uwnJor) 'SOLOR] ЦР ur suonegs [je Je P9J99][09 $иэииоэа$ jo IIQUINU [30] 94} $1 Z UUIN[OS) “Bose dy} UTM рэцииар! samads urosnyfour jo 351 [PUne fF ATAVL DRISCOLL AND BRANDON 30 ‘o1OY SUONJEINIJED au} ut pepnput you SI pue SSI [92 jo SE9IB UT SIsqQuInu SNOULIOUD UT SINIIO WwNIDUA9}]D штциЯ | (2961 ‘шеЦе15) Y 19914) yorye иво р]пра ал) YoIYM 03 sseı [99 pur $4201 Juepunge Aq pasneo A]qeqoxd st Арешоице $141, (08 ‘65) SUONPIS 5 Aq pasne9 SI PUR зпорешоив SI SOLD] pouress JULY UL $0} 3S9YY JO э8в] 199194 ysty a I, | 0 I (ABS) DIDLLISIA] DYDUNT I ‘AS 0 I (SNIPUUTT) DUDUIIIAU DUDUIDAI д I RES 0 I (SNABUUTT) snjoipow snjoıpoW I ‘A'S I I (ABS) 51]1749102] Daur Nw | ‘AS 0 I (ЧААА) 2415511] 0$ Djnsids | Hs 0 I (19[BuadS) snsiaip snjasn J с D I с (Aqiamog pur du9po1g) DSND]I DIUDN $ $ $ (N3PJUO JA) 257140 DSNJIY $ ©) G G (Avg) snynoydnp зао $ 00 0 9 (t9"]) ISUUDPD pas 6 A'S Ses 4 IT (919m3n1g) sypao роарипт] L 00 0 IT (n8ejuoJ\) pypyngns sısdony149) Ol wo $ Gl (SNIPUUTT) tUNIDINIYDUDI uoohsng с AUS NE 0-001 3l ral (ABS) xaqıa SNUDSSON с 00 0 FI (релаоЭ) wunyppnumd римаро}5т42)) 9 `` $6 0001 LI LT (Avg) wnjaa phwajosg д “USE 0'0S 9 SI (prauon)) snpaup sisuq РТ AS 0'0S L IZ (preiuo)) puyphy pısuohr] PAAUNDIO 5912949 Чо лм Je SUONEIS SIDE A Peur) ouly 59108 +. peur) jo 19qUINN od] BUIP99J UL % POZI[EUHON oul] UL 19QUINN 19QUIN N salads (ponumuor)) ф 3|Че1, MOLLUSC-SEDIMENT RELATIONSHIPS 31 | 254 20 ANIMALS — Yo/dia limotu/a NUMBER OF Y Y Y 10 20 30 40 50 a | Sel Nautical mile Y le . PER CENT SILT —=CLAY: \ N 44 43 42 md Un Nn a NUMBER OF ANIMALS — Yo/día limatu/a [| NE Nautical mile У le 44 43 42 -0.5 0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 MEAN GRAIN DIAMETER — PHI FIG. 13. Areal distribution of Yoldia limatula. Isopleths are drawn at intervals of 10 specimens. Note that this selective deposit feeder is abundant in the nearshore and offshore facies, but is uncommon in both the shallow protected and open bay facies. FIG. 14. Relationship of Yoldia limatula to silt-clay content of the sediment. This selective deposit feeder increases in abundance with increasing silt and clay. Zero occurrences are shown below the dashed line. Twenty- two of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens of Y. limatula. FIG. 15. Relationship of Yoldia limatula to mean grain diameter. This species is uncommon in sediments with a mean grain diameter greater than 0.5 mm (1.04). Zero occurrences shown below dashed line. FIG. 16. Areal distribution of Nuclua proxima. Isopleths are drawn at intervals of 100 specimens. This selective deposit feeder is abundant only in Planting Island Cove and Blankenship Cove. These areas are in the shallow protected facies. 32 DRISCOLL AND BRANDON that this selective deposit feeder is most characteristic of the shallow protected facies. The species was not taken in the offshore facies and was uncommon in the nearshore facies. The distribution of N. proxima relative to silt-clay content and mean grain diameter of the sediment is shown in Figs. 17 and 18. Sanders (1956, 1958) has discussed the species” dis- tribution characteristics in some detail. Rhoads & Young (1970) demonstrate that N. proxima is an important agent in the reworking of fine sediments. . Anadara transversa. This suspension feeding bivalve is most abundant in the open bay facies (Fig. 19). The relationship between species abundance and mean grain diameter of the sediment is illus- trated in Fig. 21. It appears that A. trans- versa is most successful in sediments with a mean grain diameter between 0.56 and 1.54. However, many of the stations with- in this sediment size range possess an abundance of dead shell material. Juveniles, which require a hard surface for fixation, are usually found byssally at- tached to the interior of the umbonal region of dead bivalve shells. Con- sequently, the areal distribution of the species is related to dead shell distribution as well as mean grain diameter of the sediment. Fig. 20 illustrates the relationship between the abundance of A. transversa and the percent silt-clay in the sediment. This species is uncommon in sediments with more than 5% silt-clay. A. transversa appears to require a medium to coarse sand bottom (Fig. 21), a low silt-clay con- tent in the sediment, and the presence of dead shell material for successful juvenile settlement. Chaetopleura apiculata. The only local polyplacophoran occurs primarily in sediments having a low silt-clay content and large amounts of associated dead shell material. It is attached to hard surfaces, commonly the dead shells of bivalves, and is characteristic of the open bay facies in areas of dead shell accumulation (Fig. 22). The low silt-clay content and mean grain diameters ranging between 0.5¢ and 1.59 (Fig. 23), which are associated with the abundant occurrence of C. apiculata, in- dicate that finer sediments, particularly clays, may be detrimental to the animal. Parker (1956) reports that C. apiculata occurs only in inlets and passes in the Mississippi delta area. These areas are also characterized by concentrations of dead shell material. Crassinella mactracea. This small bivalve is reported by Hunter € Brown (1964) from sand and shell bottoms in shal- low water. The species was collected only in the open bay facies and was partic- ularly abundant in areas rich in dead shell material (Fig. 24). All specimens were col- lected from sediments having mean grain diameters ranging between 0.59 and 1.59 (Fig. 25). Laevicardium mortoni. Areal distribu- tion of L. mortoni is illustrated in Fig. 26. An interesting aspect of the distribution pattern is that L. mortoni is most abundant in the shallow protected facies (Planting Island Cove and, to a lesser extent, Wings Cove). However, it also is present in the open bay facies and has been observed in the offshore facies (Sta. 45). No specimens of L. mortoni were collected from any of the 8 stations representing the nearshore environment. In Fig. 26 the areal distribu- tion of the species, extending into the nearshore facies, may be noted, but this extension is inferred rather than observed. Relationships between the distribution of Laevicardium mortoni, the silt-clay content, and the mean grain diameter of the sediment are illustrated in Figs. 27 and 28 respectively. A clear trend cannot be seen in either of these distribution patterns. The species commonly occurs in sediments with a silt-clay content ranging from near 0% to 50%. It shows little sensitivity to changes in mean grain diameter. This exceptional adaptability to varying environmental conditions is dif- ficult to explain. Detailed examination of the feeding habits of L. mortoni may reveal a mechanism which allows the species to thrive in environments suitable to both deposit and suspension feeding organisms. Examples of single species MOLLUSC-SEDIMENT RELATIONSHIPS 33 17 #76) #251) 18 & (1764251) 304 304 o Е © à E 2 x o 254 a 2 &25- S 2 > 3 я S | 20 2 te 204 E . | < = Ф à = ar 2 154 < = u | = |5] о < x u = 104 о = 5 & 104 z . o = 5, ® =) ses г a . . 5 > a Е aaa о | : == в в * à A ; = : 10 20 30 40 50 a a РЕВ “CENT ЭТ — СГАУ o — = a а yes à Ам АЕ A 0 T TS TT —0.5 0.0 0.5 1.0 1:5 2.0 225 3.0 219 MEAN GRAIN DIAMETER — PHI 133) 20° ч о TE nm u 1 nm о = E ANIMALS — Anadara transversa a ak NUMBER OF La 1 . о N: / / sel s в | Nautical mile N o mea У: = = acy i x. — x 70° 45' 44 43 42 ar т hr —— LE a т N 1 10 20 30 40 50 PER CENT SILT = CLAY FIG. 17. Relationship of Nucula proxima to silt-clay content of the sediment. Zero occurrences are shown below dashed line. Twenty-one of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens of N. proxima. FIG. 18. Relationship of Nucula proxima to mean grain diameter. The species is uncommon in sediments with a mean grain diameter greater than 0.5 mm (1.0¢). Zero occurrences are shown below dashed line. FIG. 19. Areal distribution of Anadara transversa. Isopleths are drawn at intervals of 100 specimens. This suspension feeder is most abundant in the open bay facies, particularly in areas rich in dead shell material. FIG. 20. Relationship of Anadara transversa to silt-clay content of the sediment. This suspension feeder is not abundant in sediments with more than 5% silt and clay. Zero occurrences are shown below dashed line. Fourteen of the 51 stations at which faunal samples were taken have less than 5% silt-clay and yielded no specimens of A. transversa. 34 DRISCOLL AND BRANDON 2] м = - | fransversa >» Anadora m n o o i 1 ANIMALS — u 1 o 1 > NUMBER OF u 4 aa 11 = à te 4 4 Е Sal QT a— — — — rum mp gee Nautical mile le r - + 7 r 70* 45 44 43 42 -0.5 0.0 0.5 1.0 15 120255055 | Е — MEAN GRAIN DIAMETER — PHI Choetopleuro apiculata i >» ANIMALS ul » NUMBER OF Ц « N ` D \ 0+ a Tey: ut ik Ey pi Ba x \ | Е 00 05 о 5 20 25 30 38 о ye и MEAN GRAIN DIAMETER — РН! Nautical mile N o 44 43 42 FIG. 21. Relationship of Anadara transversa to mean grain diameter. The species is most common in sediment with a mean grain diameter between 0.54 and 1.5%. Zero occurrences are shown below dashed line. FIG. 22. Areal distribution of Chaetopleura apiculata. Isopleths are drawn at intervals of 50 specimens. This macrophagous herbivore is most abundant in the open bay facies, particularly in areas rich in dead sheil material FIG. 23. Relationship of Chaetopleura apiculata to mean grain diameter. The species is most common in sediment with a mean grain diameter between 0.5 ¢and 1.54. Zero occurrences are shown below dashed line. FIG. 24. Areal distribution of Crassinella mactracea. Isopleths are drawn at intervals of 25 specimens. This form is most abundant in the open bay facies on current-swept sand and shell bottoms. MOLLUSC-SEDIMENT RELATIONSHIPS NUMBER OF ANIMALS — Crassinella mactracea a 446 39) 4 à à A Zum Be вы Mee м dl т т т т = 0.0 0:5 10 15 2.0 2.5 3.0 3.5 MEAN GRAIN DIAMETER — PHI 307 254 Loevicardium mortoni 2078 ANIMALS NUMBER OF 10 20 30 40 50 РЕВ (GE Nit SILT=CLAY 35 41° 42 ‚ 2 D Ju N Lye = 40 Xx \ ea / / x Ro - N 4 // ake (EN 10 El SS Sara \ A ; < 39 aS Nea | It Sabu K \ ON ey 0 | EN 38 Nautical mile u le 70° 45' 44 43 42 ar = | $ 304 a Xj o E Е > S 254 LL o 2 a à | % © | = 20- т atl a = a = 155 A a [re о a 10- a Lu o = >) = a 422 54 a a t a a a a a ~~ a aa a a Ada aa a 1 =n хр ам gai fi à À -05 00 05 Kor us ВИ os MEAN GRAIN DIAMETER — РН! FIG. 25. Relationship of Crassinella mactracea to mean grain diameter. The species is most abundant in sediments with mean grain diameters between 0.54 and 1.54. Zero occurrences are shown below dashed line. FIG. 26. Areal distribution of Laevicardium mortoni. Isopleths are drawn at intervals of 10 specimens. This form is present in all facies within the area, but shows some apparent preference for areas with a substantial silt-clay content. FIG. 27. Relationship of Laevicardium mortoni to silt-clay content of the sediment. The occurrence of this species is exceptional in that there appears to be little correlation with sedimentary parameters. Zero occurrences are shown below dashed line. FIG. 28. Relationship of Laevicardium mortoni to mean grain diameter. The species shows little correlation with this sedimentary parameter. Zero occurrences are shown below dashed line. 36 DRISCOLL AND BRANDON utilizing more than 1 feeding mechanism are not unknown (Stasek, 1965). Alterna- tively, as has been suggested for Mulinia lateralis by Levinton & Bambach (1970), the low bulk density of L. mortoni might enable it to survive in soft substrates which otherwise would be lethal. Anachis translirata and Anachis avara. During the field work and preliminary laboratory phases of this study the writers were aware that 2 easily confused species ot Anachis were present in the study area. These were tentatively designated as “A. avara similis?” and “A. avara?. Since that time Scheltema (1968, 1969) has com- pleted detailed redescriptions and life history studies of both species. Our “А. avara similis?” is equivalent to A. translirata. Our “A. avara? is, in fact, A. avara. We are retaining the tentative designations here to indicate that iden- tification of these forms was imprecise. In this discussion reference is made only to “Anachis avara similis?’ (=Anachis translirata), but cursory examination of the distribution patterns of “ Anachis avara?” (=Anachis avara) indicates that both species are similar in their areal distribu- tion and in relation to silt-clay content and mean grain diameter of the sediment. This is in agreement with Scheltema's (1968) observation that the species commonly occur together. The areal distribution of * Anachis avara similis?” is illustrated in Fig. 29. This carnivore is most plentiful in the open bay environment, but is also present else- where. Although illustrations of the rela- tionships between species distribution, silt- clay content and mean grain diameter are not presented here, such relationships do exist. The stations at which “A. avara similis?’ was most abundant are in areas of low silt-clay content and in sediments having mean grain diameters ranging be- tween 0.5ф and 1.54. Parker (1956) indicates that Anachis avara similis? is characteristic of his Lower Breton Sound and Pro-Delta Slope areas in the Mississippi delta region. This environ- ment, possessing a silty clay to clayey silt bottom, is quite different from the en- vironment in which “A. avara similis?” finds its maximum development in the area of the present study. Eupleura caudata. This boring carni- vorous gastropod is present throughout much of the area, but no specimens were collected in the shallow protected facies and only a single occurrence was found in the offshore facies (Sta. 49). Areal distribu- tion of the form is illustrated in Fig. 30. As is typical of carnivores, no close correla- tion exists between the occurrence of the species and silt-clay content or mean grain diameter of the sediment. The largest numbers of E. caudata were found in the open bay facies (Stas. 12, 15) in relatively coarse sediment, presumably because of predator-prey relationships between this species and the abundant epifaunal com- munity in the open bay facies. Nassarius trivittatus. This prosobrach is the most common large mollusc in the area of study (Table 4). Its occurrence, usually in considerable numbers, was observed at all but one of the stations which were sampled. No clear relationship between the distribution of N. trivittatus and silt- clay content exists within the area (Fig. 31), although the 3 stations yielding N. trivittatus in greatest abundance have mean grain diameters in the fine and very fine sand range. Scheltema € Scheltema (1964) have ob- served that Nassarius trivittatus typically occurs in offshore waters of several meters or more, in contrast to its nearshore counterparts, N. obsoletus and N. vibex. Although commonly present in nearshore regions in the study area, № trivittatus becomes increasingly abundant with in- creasing depth (Fig. 32). ANIMAL RANGES Figs. 33 and 34 illustrate the ranges of important species relative to mean grain diameters and silt-clay content of the sedi- ment. Also presented here is the mean occurrence of each species within its range. It is obvious that the reliability of the indicated ranges depends upon the number of stations examined and the num- ber of animals collected. Thus, the mean MOLLUSC-SEDIMENT RELATIONSHIPS 37 Np VE а | \ IS 41* 424 aN м N NS Na 7 / ? / лы у 395 E N N // N 1) о \ | À 4 Ne N 38+ Nautical mile if le Nautical mile J lo 2 НЕ 42 44 SUN 42 4 32 | @(618) e 3504 о = 2 È 300 = Le] = LL 29250 o o = | ф 200- = a = e z = 1504 e u o x . m 1004 e 7 e E . 5 . 8 z . . 504 N e . e . e . . ots о ae . e H ..? NA] ' (Eee es . © Nautical mile N o 5 10 15 20 25 30 35 40 44 43 42 р ОЕРТН —- MEAN LOW TIDE FIG. 29. Areal distribution of ““Anachis avara similis” (= A. translirata). Isopleths are drawn at intervals of 25 specimens. This carnivore, though present in all facies in the area, shows some preference for the open bay facies. FIG. 30. Areal distribution of Eupleura caudata. Isopleths are drawn at intervals of 25 specimens. This carnivore is most abundant in the open bay facies, plentiful in the nearshore facies and absent, or nearly absent, from the shallow protected and offshore facies. FIG. 31. Areal distribution of Nassarius trivittatus. Isopleths are drawn at intervals of 100 specimens. This non- selective deposit feeder is the most abundant form in the area. FIG. 32. Occurrence of Nassarius trivittatus plotted against depth in feet below mean low tide level. Note that N. trivittatus was not found to be abundant in very shallow waters and that abundance of the species increases as depth increases. 38 DRISCOLL AND BRANDON silt-clay value associated with Nassarius trivittatus (3095 individuals collected from 50 stations) is considerably more meaning- ful than that of Natica clausa (2 individ- uals collected from 2 stations). Reference to Table 4 enables one to evaluate the data in these 2 figures. The sequence of species indicated in Fig. 33 is very nearly identical to the sequence found in Fig. 34. This cor- respondence is due to the close correlation between increasing mean grain diameters and decreasing silt-clay content (Fig. 4). In Fig. 34 a distinct break is evident in the otherwise more or less continuous distribu- tion of mean occurrences of species relative to silt and clay at the 5% silt-clay level. It is interesting to note that the 5% silt-clay level was also found to be signif- icant in the delineation of feeding and habitat types in Cape Cod Bay, Massa- chusetts (Young, et. al., 1971). The distribution of trophic groups in Figs. 33-34 is consistent with the previous discussion. Those species having their mean occurrences in coarse grained sedi- ments with low silt-clay contents are all suspension feeders, herbivores, or car- nivores. All selective deposit feeders have their mean occurrences in fine grained sediments with high silt-clay contents. Rhoads & Young (1970) have presented convincing evidence that the exclusion of suspension feeders from many fine grained bottoms in Buzzards Bay is due to fre- quent resuspension of biogenetically reworked sediments. Species with more generalized feeding habits (e.g. Nassarius trivittatus) have their mean occurrences in sediments with intermediate mean grain diameters and silt-clay contents. This does not indicate that such sediments are more suitable for success of the species, but that the species is adapted for survival on a variety of substratum types. POTENTIAL FAUNAL- LITHIC ASSOCIATIONS Moore (1963) has examined the sediments of Buzzard Bay with respect to their potential rock types. Three of the 4 major rock types which he recognized are represented in the area of study. Certain observations concerning the fossils which may be preserved within these types are possible. The fauna examined here is com- posed entirely of animals possessing hard parts suitable for fossilization. These species must be considered the source for nearly all potential fossil material. The 3 compositional types within the area are proto-graywacke, feldspathic sand, and quartzose sand. As indicated by Moore (1963), silts have a distribution pat- tern similar to that of the proto-graywacke. Moore's proto-graywacke facies includes all of the offshore and shallow protected facies as well as most of the nearshore facies of the present study. It is essentially analogous to Sanders’ (1958, 1960) Nucula proxima - Nephtys incisa community in areal extent. His feldspathic and quart- zose sands are found within the open bay facies of the present study and are analog- our to Sanders (1958, 1960) Ampelisca (amphipod) assemblage. It has been pointed out that clear faunal differences exist between the 3 “fine grained’ facies and the open bay facies. These differences, attributable to a variety of factors, should be reflected by con- trasting fossil faunas in the graywacke and the feldspathic and quartzose sandstones. Species of importance in the area of feldspathic and quartzose sands which are suitable for preservation are largely sus- pension feeding bivalves and carnivorous gastropods. These, or comparable forms, might therefore be expected to constitute the bulk of preserved species in rocks that were formed in similar environments with similar sedimentary parameters in the geologic past. Sandstones demonstrating faunal assemblages that are analogous in some respects to this recent molluscan com- munity are not uncommon even during the Paleozoic. Two fossil assemblages serve as examples. McAlester (1962) has described the bivalve fauna of the Devo- nian Chemung Stage of New York. In this sandstone the majority of the bivalves appear to represent suspension feeding species. Certainly Leptodesma, the most 39 MOLLUSC-SEDIMENT RELATIONSHIPS wn¡o¡nuu/d 0DW48P0/50495 092014120ш OJJ8UISSD17 DPIJIU DUIJ[IWSDIDY D¡0¡n¿29und DI20qiYy DSJ3ASUDI/ DIDPOUY ISWDPD od/1ag D/0/n21d0 bD1n9/d0/820ÿ7 9DUDp a ¿OJDAD Sıy9Duy csıııwıs DIDAD SIy3Duy 02/0/1915 sisdolysisag | D919u/2 xuidjosoun 019111049 0210120121 p¡owonbs sıyoydıydwy 1529140} SDILOSY 240/22 200112 хэ/9ш!$ Dıwouy фио!р/поб DJ0PUDg D/0pnD2 0118/4135 puo¡d D,npıdasy 2$10/2 DIIJON wn¡D¡n9/¡0uD9 1024519 D/DUD] DJJ21/1W DUIJDAY DISUOÁA7 $5и01р014! uayaadınbay $11040 D3/0un7 110] 140ш WNnIP1021A807 $п/221/р SISUJ DuDNYsIOW 10414 SNIJOSSON SOJOJ/A14/ D/D9/U10J D/npıdasy WN/DUJS/J0 2 ds WNIJJIB DX3AUOI D/npıdaJy wni/118 Dw4apoıydo OIP/OA DSnıgo osnjay DwIxoid D/NINN wnjousa{/0 Duıdsıra4q oynyowı] SNIJDSSON XOQIA wnjaa DAw3J0S $14021/0пр $821и1104 Dyus; DWOIDW 3107 0.57 Y3L3NVIO NIVIO urrence of the mean grain diameter at represents the range in mean number of individuals within the species occurring at Station i, and M 51 i= grain diameters in which the organism was found. The solid triangles indicate the mean occ where N FIG. 33. Species relationship to mean grain diameter of sediment. The thin line species within this range. Mean occurrence is calculated as follows: Station i. DRISCOLL AND BRANDON DeI04j20W D//9UISSDID DPIJIU DUIJJIWSOJ1DY wWn¿o¡nuuid OWsapojsosaD 240/пу2ипа DI9D0g4Y 9DUDp 016и0115у DSJBASUDJ{ DIDPDUY D19j1/01d 0100120121 DID/ngns $1/5001441192 D/Djn21dD D1N9/d0/80YI 040/82 010/12 € 22040 SIYIDUY с SIJ/IWIS 02040 SIYIDUY 29/8и!2 xuidsjososn x9o¡duwis oıwouy 1589405 $0118945И DUIJOAY DISUOAT 2$12/2 DION 40 CRE LEE, >. 2 > Oe a Oo = 50 n E ь Я ci а OS AGE Bo = я ЕЕ NE © ES aon ee 2 o SS o Dn © Ф QE D == = о d о os (3) SEE Г] $11040 0210ип7 = 3 Г шп} 0112110402 10245189 d = Bm——— oupıpınodb D40oPUDg = = = $ Г] Duo;d 0/npida17 ss © Г] DIDUN] 02/1/9211 5 E + ~ oe — SUDIPDi1/ useyaadınbay es a ojowonbs sijoydiydwy о x et D/D0pnD2 2119/0913 ен PRE A SN/281IP SISUZ $ = eS НН Dx8AU02 D/npıdasy = £ un AA AAA A A A A SI EI | $140414114 SNIJOSSON ww * L | = и /UO(10W WNIPIDIIABDT ЕН - —_ _ rm 24221и120} D0,npıdasy 5s 5 ——— == 11100194106 wnyyıg | = Я. == | n un .— wnyousJayjo 12 ds TI) se = a 2119511919 OW sapolydoO aos ER nes | = Dsn,go osnjay ao LE zu Se, ЕЕ Xx 9Q/A snis0550N | 258 Г] Г | pwixosd 0/NINN 3-3 . Е 5 Duonyssow 1019 Ss 3 = УЕ EIA D = = Г] | 2/040ш!/ DIP/Ox а 5 A se | wneA DÁWES/OS © Bar Г sn d uijog | 9 © à = 4021/Аптр SOIIUIJOS 9 © à | AE ARR E Dr de e à >= s ив) DWOIJOM a Aa r т т т т т 35 T T = 31 Sl en Е о ra) о 0 о wo о o o o Ys y la] Tv + m m a y = = aa = мы IN3WIQO3S МЕ ° AVI9-1I1S LNID 33а | VER MSIE — = w per cent silt-clay at Station i. number of individuals within the species occurring at Station iand P where N MOLLUSC-SEDIMENT RELATIONSHIPS 4] common genus, seems to have been a suspension feeding, and probably an epifaunal, form. This is suggested by a shape unsuitable for rapid burrowing, the possible presence of a byssal notch, and the general pterioid character of the genus. A second example is represented by the Mississippian Marshall Sandstone of Michigan. The bivalves described from this formation (Driscoll, 1965, 1969; Hutchison & Stumm, 1965) are largely suspension feeders. Both infaunal and epifaunal species are abundant. Suspen- sion feeding brachiopods also comprise a significant portion of the fauna. Gastropods are not common, but the car- nivorous element of the fauna can be recognized in the wide variety of cephalopods described from this formation by Miller & Garner (1953a, 1953b, 1955). Bretsky (1968, 1969a, 1969b, 1970a, 1970b) has presented a well documented case for the areal separation of trophic groups in Paleozoic strata. The writers believe that the suspension feeding and carnivorous fauna reported here from the open bay facies of Buzzards Bay may be generally typical of many feldspathic and quartzose sands. It appears that, with the obvious exception of those rocks subjected to unfavorable diagenetic processes, evidence of comparable faunal associations may be expected in similar lithologies in the geologic past. The proto-graywacke recognized т Buzzards Bay by Moore (1963) is associated with those species common in the 3 fine grained facies (shallow pro- tected, nearshore, and offshore). These are largely infaunal selective deposit feeders such as Macoma, Yoldia, and Nucula. Carnivorous gastropods are of somewhat lesser abundance. Inasmuch as deposit feeding bivalves are important preservable elements in the proto-graywacke it would seem that they should constitute an important fossil fauna in older graywackes. However, many gray- wackes are unfossiliferous. We suggest that the thin shells of typical deposit feeding bivalves are easily destroyed by post-mortem processes and are poorly suited for preservation. These shells are delicate and differ markedly from the thicker, usually more compact, heavily ridged forms characteristic of the suspension feeders examined here. Al- though many graywackes may have sup- ported large populations of deposit feed- ing species during deposition, the shells of these species are not generally preserved as fossils. Moore (1963) points out that leached shell material is present in most of his proto-graywacke samples. Thus, shell destruction is occuring even in this early stage of diagenesis. Driscoll (1970), on the basis of a 3 year field study, suggests that differential burial of shells of varying architectural types in the nearshore facies may result in the selective destruction of thinner and lighter valves by shell-boring organisms active above the sediment- water interface. SUMMARY 1. Four facies are defined within north- western Buzzards Bay. These are the shallow protected, offshore, nearshore, and open bay facies. The shallow рго- tected facies is characterized by depths of less than 3 m, mean grain diameters smaller than 2.5 (0.18 mm), sorting that becomes better with increasing mean grain diameter, high silt-clay percentages, and an abundance of selective deposit feeders of which Nucula proxima is the most common. The offshore facies is character- ized by water depths greater than 9 m, mean sediment diameters smaller than 34 (0.125 mm), Trask sorting coefficients from 1.40-1.81, high silt-clay percentages, and an abundance of deposit feeders, of which Yoldia limatula and Nassarius trivit- tatus are most common. The nearshore facies, found in an area of partially pro- tected harbor mouths, is characterized by a water depth of between 3 and 7.5 m, a mean grain diameter not larger than 2.5@ (0.18 mm), sorting coefficients between 1.81 and 2.88, relatively high silt and clay content, and an abundance of deposit feeders and carnivores, of which the most common are Macoma tenta, Yoldia 42 DRISCOLL AND BRANDON limatula, Eupleura caudata, and Nassar- ius trivittatus. The open bay facies is strikingly different from all others in the area. It is characterized by sediments with a mean grain diameter larger than 2.56, a high degree of sorting, a low silt-clay con- tent, and a more diverse fauna which consists largely of suspension feeders and carnivores. 2. The areal distribution and relation- ship to mean grain diameter, silt-clay con- tent, abundance of dead shell material, and feeding type of 39 molluscan species are discussed. The factors most clearly cor- related with the distribution of these species are feeding type, clay content of the sediment, abundance of dead shell material and substratum stability. In- faunal suspension feeders are most sen- sitive to sediment mean grain diameter (a reflection of current velocity). Attached epifaunal suspension feeders are most sen- sitive to the presence of dead shell material to which they become fixed and to the stability of the surrounding substratum. Selective deposit feeders are most sensi- tive to the abundance of clay sized par- ticles—a reflection of the availability of organic detritus in the sediment. 3. Potential faunal-lithic associations are discussed. The shallow protected, off- shore, and nearshore facies are proto- graywackes. The potential fossil fauna is composed largely of selective deposit feeders. It is suggested that the common absence of representatives of this trophic group in the fossil record is due to the effects of post-mortem processes upon these mostly thin-shelled species. Thick- shelled suspension feeders make up a significant portion of the potential fossil assemblage of the open bay facies. These species are generally comparable to those found in similar lithified sediments in the geologic past. ACKNOWLEDGEMENTS We wish to express our appreciation to the Old Rochester Regional School Board, Rochester, Massachusetts, and to Donald N. Gavin, David S. Hagan, Joseph С. Kunces, and Benjamin R. Tilden for pro- viding laboratory space and equipment throughout the summer of 1965. Alicia M. Crabbe, Maureen C. Duff, Dennys A. Grady, Phyllis C. Hartley, and Johanna Teachman acted as laboratory assistants. Ruth A. Swanson assisted in the labora- tory phases of the work and in final preparation and reading of the manu- script. We are grateful to C. J. Bayne, Oregon State University, and D. C. Rhoads, Yale University, for reading the manuscript and providing many helpful suggestions. This work was partially sup- ported by a Wayne State University Facul- ty Fellowship and was completed at the Marine Biological Laboratory, Woods Hole, Massachusetts. LITERATURE CITED BADER, В G., 1954, The role of organic matter in determining the distribution of pelecypods in marine sediments. J. mar. Res., 13: 32-47. BRETSKY, P. W., 1968, Evolution of Paleo- zoic marine invertebrate communities. Science, 159: 1231-1233. BRETSKY, P. W., 1969a, Central Appalachian late Ordovician communities. Bull. geol. Soc. Amer., 80: 193-212. BRETSKY, P. W., 1969b, Evolution of Paleo- zoic benthic marine invertebrate com- munities. Palaeogeography, Palaeoclimatol., Palaeoecol., 6: 45-59. BRETSKY, P.W., 1970a, Upper Ordovician ecology in the central Appalachians. Bull. Peabody Mus. natur. Hist. (Yale Univ.), 34: 150р. BRETSKY, Р. 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SHUKRI, N. M. & HIGAZY, R. A., 1944, Mechanical analyses of some bottom deposits of the northern Red Sea. J. sediment. Petrol., 14: 43-69. THORSON, G., 1966, Some factors influencing the recruitment and establishment of marine benthic communities. Neth. J. mar. Res., 3: 241-267. VAN STRAATEN, L. М. J. U. & KUENEN, P. H., 1958, Tidal action as a cause of clay sedimentation. J. sediment. Petrol., 28: 406-413. YOUNG, р. К. HOBSON, ЮР». O'CONNOR, J. S., MICHAEL, А. D. € MILLS, M. A., 1971, Quantitative analysis of the Cape Cod Bay ecosystem. Final Rept. to the Office of Naval Res., Contr. Nonr 3070(03), Mod. 1-5, Contr. №00014-70-А- 0269. 71 p. WHITE, 5. J., 1970, Plane bed threshold of fine grained sediments. Nature, 228: 152-154. ZUSAMMENFASSUNG DIE BEZIEHUNGEN ZWISCHEN MOLLUSKEN UND IHREM SUBSTRAT IN DER NORDWESTLICHEN BUZZARDS BAY, MASSACHUSETTS, U.S.A. E. G. Driscoll und D. E. Brandon Viererlei Beschaffenheit findet man bei dem Grund des nordwestlichen Teils der Buzzards Bay, Massachusetts. Diese sind gekennzeichnet durch Unterschiede in der durchschnittlichen Korngrósse, Zusammensetzung, Gehalt an Tonschlamm und Fauna. Eine mittlere Korngrösse unter 2,54(0,18mm) ist charakteristisch für 3 dieser Böden, die an geschutzten Stellen vorkommen. Der vierte, den man an Stellen findet, die der Strömung ausgesetzt sind, ist normalerweise aus groberem Material zusammengesetzt. Der Gehalt an kohlensaurem Kalk ist eine Folge des Reichtums an leeren Schalen im ganzen Gebiet. Die Faunen der 3 feinkörnigen Substrate sind charakterisiert durch (1) Nucula proxima, (2) Yoldia limatula und Nassarius trivittatus, und (3) Macoma tenta, Nucula proxima, Eupleura caudata und Nassarius trivittatus. In den feinkörnigen Böden sind weniger Molluskenarten vorhanden als in den groberen Ablagerungen des vierten. Mehr als 35 Molluskenarten werden besprochen, von denen die Mehrzahl dauerhafte Hartteile hat. Die Beziehung von Korngrösse, Schlamm- und Tongehalt und Vorhanden- sein toter Schalen zu der Verteilung wichtiger Faunenelemente wird untersucht. Macoma tenta, Yoldia limatula, Nucula proxima und Solemya velum werden häufiger bei Abnahme der Korngrösse und Zunahme des Schlamm- und Tongehaltes des Bodens. Chaetopleura apiculata, Anadara transversa, Crassinella mactracea und viele andere Arten werden bei Zunahme der Korngrösse und Abnahme des Schlamm- und Tongehaltes häufiger. Die Menge der toten Schalen auf dem Boden hängt eng mit der Entwicklung der daran gehefteten Epifauna zusammen. MOLLUSC-SEDIMENT RELATIONSHIPS Die vorkommenden Faunengesellschaften zeigen, dass Muscheln, die suspendierte Kleinpartikel fressen, und räuberische Gastropoden sich in dem grobbkörnigen Untergrund aufhalten, und dort fossil werden. Mogliche Fossilien der Proto-Grauwacke, die die 3 feinkörnigen Boden bildet, sind Muscheln, die vorwiegend Schlamm fressen. HZ. RESUME RELATIONS ENTRE MOLLUSQUES ET SEDIMENTS DANS LE NORD-OUEST DE BUZZARDS BAY, MASSACHUSETTS, U.S.A. E. G. Driscoll et D. E. Brandon Quatre facies ont été definis dans les sédiments actuels de la portion Nord-Ouest de Buzzards Bay, Massachusetts. Ceux-ci sont caracterisés par des différences dans le diamétre moyen des grains, le triage, le contenu argilovaseux et la faune. Un diametre moyen de moins de 2,5¢ (0,18 mm) est caracteristique de 3 de ces facies, qui se rencontrent dans des zones protégées. Le 4eme, qui se développe sur des fonds balayés par les courants, est typiquement constitué de sédiments plus grossiers. La quantité de carbonate de calcium dans les sédiments est en relation avec l'abondance de coquilles vides dans l'ensemble de l'aire considérée. Les faunes des 3 facies à granulométrie fine sont caractérisées comme suit: (1) Nucula proxima, (2) Yoldia limatual et Nassarius trivittatus, (3) Macoma tenta, Nucula proxima, Eupleura caudata et Nassarius trivittatus. Пу a moins d'espèces de mollusques dans ces facies & granulometrie fine que dans les sédiments grossiers du 4eme facies. Plus de 35 especes de mollusques ont été analysées, la plupart ayant des parties dures conservables. On a examiné la relation entre le diamètre moyen des grains, l'abondance de vase et d’argile, la présence de coquilles vides et les elements importants de la faune. Macoma tenta, Yoldia limatula, Nucula proxima et Solemya velum augmentent en abondance quand décroit le diamètre moyen des grains et que s accrcit la quantité de vase et d'argile dans le sédiment. Chaetopleura apiculata, Anadara transversa, Crassinella mactracea et bien d'autres especes, augmentent en abondance quand le diamètre moyen des grains augmente et que décroit la quantité de vase et d'argile du sédiment. La quantité de coquilles vides sur le fond est étroitement en relation avec le développement de l'épifaune fixée. Les associations zoo-lithiques latentes montrent que les Bivalves suspensivores et les Gastropodes carnivores sont disponibles pour une conservation dans les facies grossiers. Les fossiles latents des proto-grauwackes, qui sont issus des 3 facies & grain fin, sont en grande partie constitués de Pélécypodes déposivores. Me RESUMEN RELACIONES ENTRE MOLUSCOS Y SEDIMENTOS EN EL NOROESTE DE BUZZARDS BAY, MASSACHUSETTS, U.S.A. E. G. Driscoll y D. E. Brandon En los sedimentos del Reciente del noroeste de Buzzards Bay, Massachusetts, se definen cuatro facies, caracterizadas por diferencias en el término medio del diämetro de los gránulos, el contenido de arcilla о limo, у la fauna. Un promedio de granos con diámetro menor de 2.54 (0.18 mm) es caracteristico de tres de estas facies, la cuales aparecen en áreas protegidas. La 4ta, que se desarrolla en fondos barridos por la corriente, está tipicamente compuesta por sedimentos más gruesos. El contenido de carbonato de calcio en el sedimento refleja la abundancia de conchas muertas en toda el área. Las faunas de las 3 facies de grano fino se caracterizan por: (1) Nucula proxima, (2) Yoldia limatula y Nassarius trivittatus y (3) Macoma tenta, Nucula proxima, Eupleura 45 46 DRISCOLL AND BRANDON caudata y Nassarius trivittatus. Е número de especies de moluscos es memor en estas facies de grano fino que en la del 4to sedimento. Se discuten más de 35 especies, la mayoría con partes duras conservables. La relación del promedio de diámetro granular, abundancia de limo o arcilla, y la presencia de conchas muertas, a la distribución de elementos faunisticos importantes, fueron examinados. Macoma tenta, Yoldia limatula, Nucula proxima y Solemya velum, crecen en abundancia en proporción inversa al aumento del promedio de diámetro granular, y el aumento del contenido limo-arcilla del sedimento. Chaetopleura apiculata, Anadara transversa, Crassinella mactracea y muchas otras especies son mas abundantes cuando el promedio del diámetro de los granos es mayor y el sedimento contiene menos limo- arcilla. La cantidad de conchas muertas en el fondo esta estrechamente relacionada al desarrollo de epifauna adherida. Asociaciones fauno-liticas potenciales indican que los bivalvos que se alimentan de materias en suspención y gastropodos carnivoros son preservados en las facies de grano grueso. Fósiles potenciales de la proto-arenisca gris, la cual compone las tres facies de grano fino, son en su mayor parte pelecipodos que se alimentan de materias en deposición. JJ.P. ABCTPAKT ОТНОШЕНИЕ МОЛЛКСКОВ К ДОННЫМ ОСАЛКАМ (В СЕВЕРО-ВОСТОЧНОЙ ЧАСТИ ЗАЛИВА БУЦЦАРД, МАССАЧУЗЕТС, C.I.A.) Е.ДЖ. ДРИСКОЛЛ И Д.Е. БРЕНДОН В современных осадках северо- восточной части залива Буццард, Масс., было найдено 4 фации. Они характеризовались различиями среднего диаметра гранул осадков, их размерным составом, содержанием силта.и фауны. Средний размер гранул менее 2.508 (0.18 мм), был характерен для 3-х из этих фаций, встречающихся в защищенных районах залива. Четвёртая встречена на дне, омываемом быстрым течением, и, как правило состояла из более грубых осадков. Содержание карбоната кальция указывало на обилие повсюду отмерших раковин моллюсков. Фауна трех тонко-зернистых фаций характеризуется наличием 1) Nucula proxima; 2) Yoldia limatula и Nassarius trivittatus, и 3) Масота tenta, Nucula proxima, Eupleura caudata и Nassarius trivittatus. B этих тонко-зернистых фациях количество видов моллюсков меньше, чем на более ‘грубых осадках 4-ой фации. В работе рассматривается более 35 видов моллюсков, большая часть которых имеет твердые защитные части. Изучалось соотношение среднего гранулометрического состава осадков, обилие силта и глин и наличия отмерших раковин - к распространению главных элементов фауны. Обилие Масота tenta, Yoldia limatula, Nucula proxima и Solemya velum увеличивается по мере уменьшения среднего диаметра гранул осадка и увеличения содержания силта и глин. Обилие Chaetopleura apiculata, Anadara transversa, Crassinella mactracea и пругих видов увеличивается по мере увеличения среднего диаметра гранул осадка и уменьшения содержания в нем силта и глин. Количество отмерших в нем раковин на дне тесно связано с развитием прикрепленной фауны. Потенциальные Ффаунистическо-литологические ассоциации указывают, что фильтраторы Bivalvia и хищные Gastropoda сохраняются на более жестких грунтах. Потенциально-фоссильные моллюски, населяющие 3 тонко-зернистых фации, являются, в основном, двустворчатыми моллюсками, собирающими детрит с поверхности осадков. MALACOLOGIA, 1973, 12(1): 47-96 SALINITY TOLERANCE OF SOME MARINE BIVALVES FROM INSHORE AND ESTUARINE ENVIRONMENTS IN VIRGINIA WATERS ON THE WESTERN MID-ATLANTIC COAST! М. Castagna and P. Chanley? ABSTRACT Many species of estuarine bivalves have a distribution pattern closely cor- related with salinity, indicating the importance of salinity in determining these patterns. The approximate salinity tolerance range for 36 species of bivalves. is described. Tolerance limits for 29 species were determined in laboratory experiments. Most of these species display a remarkable degree of euryhalinity. All survived a minimum salinity of at least 17.5% ап4 25 species survived at 12.5%. Twenty species survived at various lower salinities. Salinity tolerance for a given species is not constant but varies with season, salinity experience, and temperature. Burrowing, feeding and reproduction usually occur at nearly all salinities at which survival is possible. Byssal formation requires a higher salinity than is necessary for other activities. In Virginia about two-thirds of the species of salt-water bivalves discussed can be found over the entire salinity range they are capable of tolerating in the laboratory. Eleven species do not occur over their entire potential salinity range. Eight of the 11 species, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis, are near the geographic limit of their range; their distribution locally may be limited primarily by the tactors that determine their geographic range. The distribution of 5 species, Argopecten irradians, Congeria leucophaeta, Macoma mitchelli, Donax variabilis and Spisula solidissima, may be influenced by predation, competition, or special environmental requirements. Four of the 11 species, Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata, occur in specialized habitats with low species diversity. INTRODUCTION Бу graphically distributional patterns Temperature is usually considered the illustrating a variation in the relative most important ecological factor in- numbers of species found at various fluencing the distribution of animals (Gunter, 1957). Within an estuarine sys- tem, salinity is generally the more ob- vious environmental factor (Pearse & Gunter, 1957). Many species have a dis- tribution pattern closely correlated with salinity, and often are categorized accord- ing to the salinities in which they are found (Wass, 1965; Menzel, 1964; Wells, 1961) or identified with certain as- semblages that characteristically occur in a given salinity range (Ladd, 1951; Parker, 1959). Pennak (1953) summarizes the importance of salinity in determining salinities. Carriker (1967) reviewed the classification and distribution of organ- isms in an estuary. The distribution of most adult bivalve mollusks may be especially influenced by salinity since the relative immobility of these animals usually precludes migration from adverse salinity conditions. The literature abounds with accounts of mass mortalities associated with abnormal salinity conditions (Baughman, 1947). However, because of the variable nature of the environment, it is frequently difficult to ascertain from field ob- ‘Contribution No. 476 from Virginia Institute of Marine Science. “Present address: Shelter Island Oyster Company, Greenport, L.I., New York 11944, U.S.A. 48 CASTAGNA AND CHANLEY servations the precise effect of salinity on natural distribution. The ability of most bivalves to adapt to transient conditions of unfavorable salinities by physical exclusion (closing of shell, retreat into burrows, closing of burrows, etc.) rather than by physiological adaptation further confuses attempts to determine their salinity tolerance limits from distributions (Kinne, 1967). Finally, from observations on natural distribution, it is difficult to differentiate between the influence of salinity and several other physical and biological factors (Kinne, 1967). For exam- ple, the edible mussel (Mytilus edulis L.) is limited to high salinity oceanic waters in Virginia not by salinity but because the low-salinity bay and inshore waters reach lethal temperatures in the summer (Hutchins, 1947; Wells & Gray, 1960; Read, 1967). The distribution of other species (Mya arenaria L. and Crassostrea virginica Gmelin), although overtly associated with low salinities in certain areas, may in reality reflect the influence of predation or biological competition (Nichy & Menzel, 1962; Menzel, Hulings & Hathaway, 1958). Although the bivalve mollusks соп- situte a sizable biomass of the benthic and planktonic (as larvae) communities and are important economically and ecologically, very few data are avail- able on the salinity tolerances of most species. Furthermore, available infor- mation is based primarily on field obser- vations. We have undertaken a study to demon- strate more precisely the salinity toler- ance of many species of bivalves occurring in the study area and with this informa- tion determine the influence of salinity on natural distribution. This includes a review of literature, experimental work and a discussion to correlate and evaluate results. The scope of these studies has been limited to the effects of salinity on bivalves from the inshore marine and estuarine environments of Virginia as listed by Wass (1965). Since it is our purpose to survey the salinity tolerances of many species rather than to treat a few exhaustively, emphasis has been placed on the effects on activity and survival of adults. The influence of salinity on growth and reproduction and its possible effect on the distribution of a species has received only cursory treatment in our experimental work. PROCEDURE, METHODS, AND MATERIALS Collections were made from 24 inshore and estuarine sites (Fig. 1). Spisula solidis- sima collections were supplemented by specimens from a commercial dredge boat working off Point Pleasant, New Jersey, in depths of 50-100 feet. Most collections were made in estuarine areas, such as the James and York Rivers, or in small tidal creeks, such as Occohannock ог Pungoteague Creek. These creeks and rivers drain into the Chesapeake Bay, and are usually sand or sand-mud areas with little or no vegetation. Plants, when pre- sent, were predominantly Zostera or Zostera and Rupia together. Salinities were usually below 22%o. The high salinity species were collected from ocean beaches on the barrier islands east of the Delmarva Peninsula (land mass forming the eastern boundary of Chesapeake Bay) or Нот the small bays, creeks, or lagoons between these barrier islands and the peninsula. These were high salinity areas (27-32%) with very turbid waters, peat or sand sub- strata on the beaches and usually soft mud or sand-mud in the bays and lagoons. Specific information on collection sites is shown in Table 2. Salinity tolerances were determined experimentally for 29 species. A few species were not included because they could not be collected in suitable numbers for experimentation. No experimental work was attempted when salinity tolerances could be determined adequately from published accounts. Except where otherwise noted, geographical ranges are from Abbott (1954). Attempts were made to follow the experimental procedures outlined below, but because of the PACIFIC OCEAN SALINITY TOLERANCE OF MARINE BIVALVES af Le, \ \ MEXICO SOUTH AMERICA FIG. 1. Sites collected for species used in salinity tolerance experiments. 49 50 CASTAGNA AND CHANLEY uniqueness of each species, modifica- tions were often necessary. Experimental salinities ranged from 0-30% at intervals of 2.541%. At the beginning of each experiment, a group of 10 animals was placed directly in each salinity. The control was the group placed in the experimental salinity that most closely approximated the salinity from which the animals were collected. The control was maintained at the same salinity throughout the ex- periment. After animals had adapted to ex- perimental salinities, as determined by survival, filtering?, burrowing or other activity, groups were transferred by steps to different salinities at а rate of 2.5+1% per 48 hours or on occasion per 24 hours in an attempt to further extend the salinity range. When the maximum salinity range was determined in this man- ner, surviving groups were transferred directly to either the opposite extreme salinity at which any had survived or to the control salinity to determine if they could adapt to greater salinity changes in the reverse direction. Observations were made daily and con- sisted of counting survivors, removing and measuring length of dead animals, coun- ting those that had burrowed or attached by byssus, and observing the ability of animals to filter algae. Observations were also made of nest-building by Amygdalum papyria (Conrad) and reproduction by Gemma gemma (Totten). Animals were not considered dead unless they gaped and failed to respond to repeated tactile stimuli or were obviously putrescent. Ability to burrow was assumed if the animal was wholly or partly buried in a natural position. Burrowing animals were dug up weekly to determine continued ability to burrow. Ability to filter was noted by the clearing of algae from the water and by fecal deposition. Experimental animals were collected from many areas throughout the entire year. Collection details are summarized in Table 1. Since smaller individuals were more active and adapted better to labora- tory life, the smallest specimens available were used. Sufficient animals were ob- tained so that 10 could be maintained in each experimental container. Whenever possible, experiments were repeated until at least 40 animals were exposed to each experimental salinity. Although repeat experiments with the same species often included different populations, or were conducted at different seasons of the year, experimental results involving one species have been combined. It was sometimes necessary to hold animals until there was a sufficient number for an experiment. They were held in water of the same salinity as the area in which they were collected. All weak, damaged or dying animals were discarded before starting an experiment. Experimental details are summarized in Table 2. In each experiment, animals were maintained in containers with 400 cc, 3 liters or 6 liters of standing water (depending on the size of the animals). Aeration was provided for those species that displayed poor survival in holding containers or preliminary experiments without it. Experimental salinities were adjusted by diluting salt water from the laboratory sea water system with pond water from the irrigation pond at the Virginia Truck Experiment Station, Eastern Shore Branch, Painter. This source of fresh water was chosen because the volume of water needed precluded the use of distilled water and preliminary experiments indicated that tap water was unsatis- factory. The total salt content of the pond water was 80 ppm. Water temperature was taken daily and the range for each experiment is given in Table 2. No means of controlling temperature were used. Since temperature varied considerably, average range was 7.4°C, no attempt has been made to more precisely present mortality and ‘Throughout this paper, animals are reported as filtering if they cleared the water of suspended phytoplankton, even though at high algal densities most of the algal cells may have been rejected in pseudofaeces. 51 SALINITY TOLERANCE OF MARINE BIVALVES 1991 ©) J9yPWMSPL JBOU 2127140212] 49805) DIDIUNA] DOUADE xo] quis DNUOUV DSAJIASUDA] DA DPDU V sıjDao DADPDUV puhdod tunjppshuy OL puog IPS 208 77 £9 Judy ans yorog | usyoig yeod jo sduinjy Aq рэзо4хэ yeog 95 вэ CO-EG во UIQ рие|$1 лерэЭ cg) Aınf 15 pins yorog 1953044 rad yo заи о) 4q posodxo yeod QZ в CE-EE во ивээо PUBIS] рэ) F9 PO $5 jans yorog uoyoaq rad jo sdumpo 4q posodxo yeod QZ 9 C£-£€ во ивээо puUr]s] Jepay F9 4[n[ 6 рэярэ1а [124$ GI Ro 1g Bo Avg ‘SI 30H £9 [dv pospolqd [PUS GI RO 1g © АвЯ ‘SI 30H F9 Judy p98p91 [194$ 68 1g eo Avg ‘SI 30H FQ UN $810} JOAY YOK juoyed [етодэииио о) pny 0 CLT эврия UEW9[ON) 99 ‘Gey CI DIJUIBAD DIADINY I 0} poyoryye JOATY Soule [ IBP [Joys purs QT BO CZ puno13 э рр! 29 PO 55 $810} jouuryy) yuoyrd [етолэцииоо) pny [1-8 0€ во onsroideyor A cg ÁBIA- 9.1 suo] jpuueyy Juoyed |ето4эцииоо) pny 8-5 18-96% onsroideyor M cg ‘qoy- urf OBPoAP [PHIDUIUOT) pau ‘purs 01-5 © 08 BO Avg yurjesoy pg ‘uRf-90q U99195 pue [paoys 10 pur purs РС с'05 19940) enpueN Р9 АГАТ 199155 pur [PAOUS 10 pur} purs 85 8'05 19945) вприем p9 ounf 01 pou 972415919 ior 915 OS ayep OO) duo) u0nda][09 UOND9][0I 00112905) 1938 М ye 0, [еб soods ‘ззиэцилэахо AJIUIJRS UT PISN SIAJPAIQ 107 EPP UONII[OD “TT ATAV.L IBP9IP [етолэииио”) PAIN ‘АО aT 90€ 19910) Á9UUI F9 ‘IPN 98P91P [еолэциио)) pnu “Aero 9 Ze Avg SI 30H F9 qu DSOLIPuod DYION 199155 Y [PAOUS pues OI 6'9Т 19910 A9O0UUPYODIO 99 “Id y | 1995$ Y [9^04$ pues OI eo CO] 4994) YoouurYyoGO 99 ‘IRIN TZ 199125 Y [PAOUS purs 81 977 ЧовэЯ S 1058 N ©9 ‘PO 05 199155 Y JOAOYS purs c'0Z 0'FZ M9 эт Р9АШ[ OZ SYDAIID] DANI 199195 Y |9^04$ pau ‘purs 61 OLI Jey M SUBAY 99 АВИ OI 19915 9N3*9]03UNJ 199455 Y [9^04$ pau “pues OI GFI “Py MA SURAT 99 en L YPAYOU DOOD ae 199155 Y JOAOYS pny ra ЗСТ 991) A9OUURYODIO 99 sunf 6 = 199195 Y [DAOUS PNIN LI LOL 1991) Yoouuryosg 99 ABW ZI-OI = риш ur Зита pur yy pny GI RO JOATY YAO д cg Judy понра DUOIDIN =< 199455 Y [PAOUS pues I 0'07 yorag suose y cg ‘urf €] punpfiy DISUOÑ] = qe18 40519194 pnw-purg с Ев PURJST ULMpoos) gg urf птиц INU вит] ~ 199125 Y [OAOYS purs SI eo с'05 199.10) A9NJRLUBO) F9 PO a U9919$ Y [OAOYS purs 87 8:03 1994) впри М pg ounf[ шонош 1UMIPADILADO] = 199455 Y |9^04$ purs с 0'07 19910 вприе м eg ‘uel ZI 2 199455 Y |9^04$ purs E Gas 199.10) enpueN F9 991 GI DUI DUI) 7 [PAOUS purs 877 PZE APO ру] sepay 19 anV L © JOAOYS purs ez 0'ZE Yoo PUPIST лерэЭ 19 B3NV Pp SNJIIAIP SISUT = yorog = JoyPM JO OBpo Jr pury АЯ purs €] eo CO-EE во UP990 'S] INDROJOSS Y Р9 149$ 11 © Yorog 19JPA JO OBpo Jr pury Ag purs OF eo CE-GE во UBIIO PUPIS] Iepay Р9АШ[ IG зарыта хрио s339 104] pury Aq snq pues Leo 0Z 89 рэтеэл Алоуело Че] 89 99d 217502 DANI]AOJARY poyjou OPASGNS e 915 oys эуер $91294$ uonoa1[[0) duo) UOND9]]0D (101299) 1029905) LOVE М ye 09, "TVS (penunuoo) | TIEAV.L a SALINITY TOLERANCE OF MARINE BIVALVES 199455 № JOAOYS 199155 Y JOAOYS 199155 Y JOAOYS $518 |99 punoar Surgoad pur H [PAOUS [PAOUS [PAOUS [PAOUS J9JPA JO 93po ye puey Ag a8 poip [PTOS TUU o) [PAOUS $51899 риполе Surqoid pur $51899 punoxe 8и4олА pur 55248 [99 punoar Surqoid pur PH PH 191014 yeod jo дип Чо 193044 jead jo зип Чо 193044 yead jo syuny) purs purs pues purs purs purs purs purs purs purs purs риш y purs our] pnu y purs эш pau y pues out pau © purs pnu y pues jans ul 5рэ4 Pad pins ul Spoq 1894 jans ul Spoq 1еэа poypu 1042995) 917.45 Ч 16 55 0 BO cz во $96 Do dus} 1938 М 8. 6% [85 PES 1914] onBeoideyor м eg oun[ ez Gg LO JoTUT эп8вэлаецов М cg aunf [I 05 to 19910) enpueN cgaunf 11 Pz JIND oMTT £9 ANS 07 51190 ри] 2.1 23N3B9J03UNJ 6 FI JEUM SUBA H JONTEFNPZ onserojosundg 813 Pet Suen G9 228% anserojosung r 05 FRI SUE AGT 9% SATT Ads PURISI лерэЭ cg ‘Bny 9 smoqajd snjasn L PE-ZE Bd JU] aNZR9JODUIL) £9 AON A9S19[ MIN PE-ZE BO ‘\ueseald Id £9 'q94 7159 ру 0$ pynsids 1э[] эп8вэла PEE “BYR M ‘тварие$ cg ounf ez sıpıaa U2]0S A 80$ ‘Arg эпявазоэшщо 19 ‘Bny I BA gog ‘Avg anBeajooury) 19 Ап[ $5 A PPE ‘Avg anBrajooury’y) cg ‘dos 5 шт]аа 12] 08 с в JOATY Saue [ C9 ‘A 61 9°C J9AIY Souue [ £9 Aın[ pz DIDIUNI DIBUDY yorog PE-OE PO ивээо Puejs] ерэЭ £9 Idy OI yorog P£-08 PI URIIO PUPI[S] лерэЭ £9 JEW OI yorog 28-08 во URIIO PUIS] JepaDy Pg uel РТ snuofipnjoyd 0011194 9315 OHS ayep sotoeds UON99[[09 uON99[[07) (09119395) (panuyuos) I ATAVL CASTAGNA AND CHANLEY 54 col SET og 095 8 05 56-5 91 GP Lee LES 097 973 G¢-L 0% As 0€ с 8G 67-81 OST 061 €G-LT 8$ [9$ 89-17 OST [cc 85-65 cr x Ibal 081 907 оо! 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CT-9 095 OST 8 GG-9'CT 59 СФУ 55-66 0€l 361 ya-ST 69 $ 96 rg 081 F 61 Yoav > РИ 60€ ¿Sel 097 DA! ec 6l 58 CsI 6 FI “Ol 097 € GG 66-9 GS 9S S'GT SIT "os 097 IC 35-55 Lv speunur (sAep) ( Uru) (uur) jeyuow (),) dus} (D.) 93ue1 yuow sup] IBUPA -Lodxo JO [eyuouiodxa oinjetodu) -Hadx9 JO UPOIN aus Joquiny UBIIN ¡eyuoutiodx5 paye y Ч] p9 aunf c 0} £9 ıdv pz C9 any 17 0] C9 A[nf 85 r9 “AON 08 0] F9 PO FZ F9 'BNV FZ 0] £9 АПТ Р9 ouNnf $ 0} F9 Idy $1 p9 aunf c 0} F9 Idy 01 F9 АВИ 6 0) F9 JEW OT 99 Ady 81 0) 99 ‘494 LI cg 09d РС 0] C9 PO $5 C9 АВИ 07 01 C9 ‘JPN 61 cg ounf (I 0} C9 “Go CI £9 АВИ fF 0] Р9 ‘G24 ОТ F9 1dS 110} F9 Apnf 21 F9 Ап[ 23 0) F9 ounf 01 soyep JUMUILIOdXY 2120440213] пцэ8ио’) DIDIUNA] DIUM x9] dues пииоиу DS1IASUDA] DA DPDU у s1]D20 DADPDUV puhdpd wunjopshuy soloods ‘зЗиэцилэ4Чхо Ayuıes 01041} вер auopmul JO AIR LUNG © УЛЯУТ 55 SALINITY TOLERANCE OF MARINE BIVALVES but uals O€T UTE $ 3-61 87 e TI cI-6 081 9'81 IST IS c'9 657 081 8 6I с 15-81 РТ д.9 6-? 081 Тб G PCT EI 95 6'€ 8-5 081 0233 93-v"81 86 OFT 05-2 081 pat To-ST eb 8'S 6-93 L6 СЗТ [55-61 ce SS 615% 095 961 85591 BE Tel SI-S'Z 093 9'GG 85-56 87 Ge 070% 097 e'LI T3-8l 06 $5 050% 09 У] [5-51 СТ Г75-61 OT 9'1G EST $5 667881 081 LAG 95-11 ce ZT gell 095 $ 03 с 7с-6`9Т 09 $6 GI-C'9 095 LYVG 65-05 39 66 0"8T-0'S 081 Gel LIE pc speunue (sAep) (vu) (ипи) [е]чэш (Эо) dura} (D.) 93ue1 jua sua] IBUPA -Hodx9 JO [ejuowmodxs эллуелэЧи1э} -Hodxa Jo UBIIN y33u9"] 19QUIN М UBIIN ¡pyuauiodx4 pajelay yi3uo] 99 aunf $ 0) 99 ke ZI 99 dy 65 0) 99 JPW OI 99 эип[ pz 0} 99 ounf 01 99 ounfg 0) 99 AIN El cg ounf , 0} cg “1d Y 0€ C9 IBN I 0] cg ‘uel gl 89 ‘424 6 9 89 ‘uef c £9 “AON 61 0] Р9 PO ZI 29 Ат[$ 03 pg эчп[ 11 gg “Id Y ZI 0) cg uel $1 C9 ıdy ZI 0} F9 99 LI L9 3455$ $ 0} 19 ‘sny 2 19 das $ 0} 19 'Зпу € F9 “AON QT 0) Р9 “idos LT £9 das TZ 0} 119 Yy9NU DUOIDIA DIIYI]DG DWOIDN Durphy visuoh] DIVIUY]NU DULIN] 1UOJ10W WUMIPADIIQ ID] Dulas ии IF) Узи SISUY £9 Aın[ zz sılgpııma хрио 69 “Url TE 0} 89 991 L DIDIS09 DANIJAOJA) sayep JUJUILIOGX YA Soadç (penunuos) $ A'IAV.L SHAN LEY NA AND С ASTAG = sl ( C'8P-08 OST S'TG 601 ST=2 LIT 607 9'8 СТ-9 601 VIG e OT $Т-9 631 & IG G CG LG" LT 097 8 L1 9'8p 09-23 093 677 ce Proc 08 С IG AT 95-06 061 861 &GST 96-2 095 OL GGL 98-86 097 906 с 19 C8-6¢ 095 Sl 601 91-2 061 A CCl 81-6 OST esl TI 92 0€l 681 18 GI-S _ O8 sr speunur (ции) (urur) payuoun (о) dua} yysuo] osu -HodXo JO [ejuounodxo UBIN yiBuo”] 19QUIN N US NA S'GG-LT 8733-81 G'EI-S FI 83-636 La-S'LT с 9C-FI 8 03-31 6216-9 FI OFT EI 12291 "26-91 63-07 (9,) 93ur1 941]2494и19} [9 uo Lo dx (sAep) yuouı -Hadx9 Jo yysuo'] cg ANT 0} cg aunf pz 19 `Зпу GZ 0) 19 BnyZ LQ BNY $5 0} Lg Am( 85 G9 10 9 0] cg 3429$ cg ıdy FI 0) C9 "QUA 87 p9 dag 9 0} £9 Aınf 97 pg aunf c 0} F9 “1d y OI pgoun[ 110} F9 BIN OI 79 EN SEN pg uef cl po ANS 0} 79 ABN € p9 ABIN p 0] £9 A SI 99 “Id Y cz 0} 99 1dV | 99 “1d y 8] 0) 99 ABN PG c9 99( Pz 0) C9 PO SG £9 ‘399$ FI 0] 9 AMI TZ sayep Juoumlodx7] sıpıaa uajosg шт] аа 28 и19]06 DIVIUNI DIBUDY snuuofippjoyd DONNA DSOLIPuod DION $1JD1970] DANA TOS (panunuo)) с AIG VL 57 SALINITY TOLERANCE OF MARINE BIVALVES gg Ат[ 93 0} $8 6I-S OST 8 CG p GG-C'TG $5 cg ounf pz cg 4 f 98 0} гот G'YI-L OST GG 6 SG-6 SI pp cg aunf ZI cg anypo Гб ST-8 OSI 877 S'L3-6'8I ¢ gg eunf 51 F9 ‘ANY 85 0} OTI S'eT-S OST Гб 63-77 68 79 Anf TZ so vuaL 99 EN 06 03 T'8I 85-1 OST VSI 05-8 SI TG 99 ‘IRIN 6 99 ‘SI GI 01 661 5-01 OST GET &'TS-S'FI ce G9 ‘23 85 99 ‘uel pz 0} 0G 63-TI OSI CLI T'13-¢ FI 85 G9 OA 8T GQ dag 65 03 OF 0S-ZE OST 917 23-361 pS cg Bny 1 smaqajd snjadv_L G9 ‘url 65 0} 877 18-81 095 691 S'6T-8l TL 79 ‘AON 06 79 “dy € 0} Sé 89-31 ost 891 08-C'ET LG 79 AL punssıpıjos Dynsids sjeunue (sAep) (vu) (uu) [eyuauu (D.) dura} (D.) эВ ие yusu sul IBUPA -Hodx9 JO [eyuauiadxa оллуелэ@иэ} -l1adxa Jo sayep uro|\ y¿3u9] JoquinN ss uray [eJuswnodxg payeloy yysu07] зиэшиэах 5912э4$ (ponunuoo) $ ATAVL 58 adaptation rates influenced by tempera- ture. Water was changed 3 times weekly, and at each change a heterogeneous mix- ture of phytoplankton was added (except in fresh water) so that observations on the filtering ability of the moilusks could be made. The algal mixture was predominantly Chlorella from a culture obtained by fertilizing sea water with commercial inorganic 5-10-5 fertilizer (Loosanoff & Engle, 1942). After mixing, salinity was checked by hydrometer and, if necessary, corrected to within 1% of the desired salinity. Beach sand, collected from Cedar Island or the Machipongo River, was used as the substratum in all experiments except for those involving species incapable of burrowing. The depth of sand varied with the size of the experimental animals. Polyethylene, fiberglass or glass con- tainers were used in the experiments and for collecting and storing animals, sand and water. SALINITY TOLERANCE BY SPECIES Order Protobranchia Family Solemyidae Solemya velum Say (Tables 1,2,3) The awning clam is found commonly in CASTAGNA AND CHANLEY shallow muddy areas from Nova Scotia to Florida. It is relatively scarce in the collection area and is usually asso- ciated with Zostera marina at salinities above 15% (Wass, 1965). Most Solemya survived direct transfer from either 30.8 or 34.4 %o to experimental salinities as low as 20% (Table 3). One clam out of a group of 30 survived transfer from 30.8% to 17.5%: none to lower salinities. However, clams survived at lower salinities after acclimation to intermediate salinities. A few survived at 12.5% after acclimation, but most of the Solemya were unable to survive below 15 %o . Essentially the same salinity limits were established for burrowing and filtering as for survival. Again, the minimum salinities could be reduced to 12.5% by gradually acclimating clams to intermediate salinities. Frequently, filtering and burrowing were observed at salinities that eventually proved lethal. Family Nuculidae Nucula proxima Say The nut clam is a common subtidal mud dweller found from Nova Scotia to Florida and Texas. Menzel (1964) lists this species as occurring at salinities TABLE 3. Response of Solemya velum Say to different salinities. Salinity at collection sites was 34.4 and 30.8%. % Surviving Highest % burrowing Feeding (0= попе, R= reduced, N=normal) After After After Salinity direct After direct After direct After %o transfer acclimation transfer acclimation transfer acclimation 0 0 0 O O 29 0 0 O O 5.0 0 0 O O ES 0 0 O O 10.0 0 0 0 O O 19:5 0 7.4 0 64.1 O R 15.0 0 84.6 0 100 O N 17.5 3.3 92 26.7 100 R N 20.0 86.3 92.3 100 100 М М 22.5 90.0 100 100 100 М М 25.0 89.7 100 100 100 М М DD 90.0 100 N 30.0 96.7 100 N SALINITY TOLERANCE OF MARINE BIVALVES 59 above 25% in Florida. It occurs in sand to silty sand, at salinities above 20% (Wass, 1965). Family Nuculanidae Yoldia limatula (Say) The file yoldia is found along the East Coast from Maine to New Jersey but rarely in lower Chesapeake Bay (Wass, 1965). Natural distribution is probably limited to areas where salinity is above 20% (Wass, personal communica- tion). Order Prionodontida A major problem encountered with the Arcacea was their sluggish response to experimental conditions. In lower salinities they sometimes seemed narcotized and were often found gaping widely. They did not react to stimuli but, after being removed from the water, eventually closed. Some animals may have been removed as dead from earlier experiments before this trait was discovered. Even- tually, only putrescent individuals were considered dead. Family Arcidae Anadara transversa (Say) (Tables 1, 2, 4) The little blood clam occurs commonly in subtidal mud from Cape Cod to Florida and Texas. It is common in Chesapeake Bay and its tributaries in intermediate salinities (15-25% ) but is scarce at higher salinities (Andrews, 1953). It has been reported as occurring in areas where salinity varies from 3-42% (Parker, 1955) and 16-40% (Ladd, 1951). In Florida it is found at salinities above 25% (Menzel, 1964). Anadara transversa were collected on 2 occasions from salinities of 17.5 and 25%, respectively. All died after direct transfer to salinities of 7.5%) and lower (Table 4). Only 2 clams out of 20 from 17.5% and none out of 20 from 25% survived direct transfer to 10%. Ninety percent of all clams survived direct transfer to salinities from 12.5- 30.0%. After acclimation, all clams sur- vived at 10%, and 85% originally taken from 17.5% survived at 7.5%, although all those from 25% died at 7.5% (Table 4). After acclimation, clams were trans- ferred directly to the opposite extreme of the salinity range. Transfers from 12.5 to 30% and 30 to 12.5% were effected without mortality. Only 2 out of 18 sur- vived transfer from 30 to 10%. When clams were transferred directly to experimental salinities, suspended algae were cleared within the salinity range of 10-30%, but several days elapsed before normal filtration occurred below 17.5%o (Table 4). Filtering at 10 and 12.5 % was always reduced unless clams were first acclimated at 15%. After acclimation, some clams cleared the suspended algae from the water irregularly at 7.5%o. At no time did a majority of blood clams burrow into the substrate. Active clams usually climbed the sides of experimental containers by byssal attach- ment. Consequently, few burrowed after they became acclimated to experimental conditions (Table 4). At salinities close to the minimum for survival, burrowing was more obvious, presumably because clams were not active enough to reach the sides of the containers. Byssal attachment occurred at 7.5-30 %o but clams were slow to attach below 12.5% and then only after acclimation at intermediate salinities (Table 4). Anadara ovalis (Bruguiere) (Tables 12.5) The round blood clam is common and widely distributed from Cape Cod to the West Indies and the Gulf states. It is common subtidally in mud in both Chesapeake Bay and Eastern Shore lagoons. Andrews (1953) reported it as occurring in salinities above 15 %. Menzel (1964) found it at salinities above 25% in Florida. All clams transferred directly from a ‘salinity of about 30% to 12.5% and lower died (Table 5). Only 45% survived direct transfer to 15% while 90-100% survived at all higher salinities. In 1 case HANLEY NA AND C + 3 ASTAC > 24 C 60 N N 001 001 AUS 0 0€ 8 L6 0'06 0'0€ N N 001 001 0 69% 001 0'S6 € LG N N 001 001 c'8 GIP VL6 C'L8 0 SG N N 001 001 0 CLG OOT 0 06 CCS N N 001 001 0 986 001 C6 0-02 N N 001 001 0 8 9€ 001 G'L6 CLI N N 001 G'L6 6 CLE 001 001 0ST N Y 001 788 EL ces OOT 0'06 al Y Y C9 Ts $95 65 OOT O'S 001 Y O 07721 0 0'05 0 8 83 0 GL O O 0 0 0 0 0 0 0'S О O 0 0 0 0 co O 0) 0 0 0 0 лэриец 195094} Joysurd} Jojsuen UONBUNJDDR J99M1p UOgRuIpoor J99.11p цоцецрое Joop uoneumpor PSP 00, IOV IOV IOV IOV IOV IOV IOV IOV АИ 6 ([ецчпоч=мМ ‘рээпрэл = »uou=()) 3UIpa9.] snssAq Aq Buryoryye Y Jsoysry э8влэлу BUIMOLING % Soy sly э8елэлу BUIAIAING % "00, CLI pur CZ SEM SOS UOND9][09 ye Ayrumeg ‘SOTIUTPRS JUSIOJ IP о} (AVG) VSaasudA] DADPDUY JO osuodsoy “+ ЯЛЯУТ 61 SALINITY TOLERANCE OF MARINE BIVALVES Áyurpes 03 opgeynquige you Áppualedde sem AJIJEJION ‘palp Jaurejuos эцо ul speunue [je yolym ит зиэшиыэ4хэ SuIpNypoxy , М М М М CCI N N Sub N N $0 М Y GE Y Y oF Y O co Y O O O O O O 1915084} поЦеиоов yop uonrunpoe 19}JV JV JOY V (ewaou=N ‘poonpel CGP G Тб oor 8 TG 8L og 19]SUB.1] PaAp 19V snssÂq Aq Zuryppene =Y ‘эцоч=0) SuIpoa 6 SOYSIY э8вдэлу C'T6 L'T6 .0'S8 6 16 6 06 00T 0'08 618 с 99 885 80% 966 p98 0 0 0 0 0 0 0 0 19]SUB.1] UOTELUI[008 Jo911p IOV 19}}V BUIMOLING % 35948] э8елэлу 0'001 AU 001 0'S6 001 G'L6 001 G'L6 001 006 Fr 86 0'SP LOL 0 T'Z9 0 0 0 0 0 0 1915484} uoneunpoe J99.11p 19YV 191 V BUIATAING 9% 0'08 SLE 0 SG G'GG 0 0G SET ‘OST A 001 GZ OS SG 0 0%, Ayres ‘0608 JNOGe SEM $95 цоцоэ[оэ JE АичЦе$ ‘зэциие$ зиэлэуур оз (alaInBn1g) зурао DIDPDUY jo asuodsay ‘6 ATAV.L 62 CASTAGNA AND CHANLEY a higher mortality occurred at 27.5 % in 1 container. Clams in replicate containers survived well. Most blood clams survived at 15% if salinity was reduced gradually. Nearly 85% of the blood clams acclimated at 17.5 and 20% survived when moved gradually to 12.5%. Clams surviving direct transfer to 15% were moved to 12.5%: all died. Although acclimated clams survived exposure to 10 and 12.5% for extended periods, it is doubtful they could survive indefinitely at these salinities. Two groups of Anadara ovalis, ac- climated to intermediate salinities and then kept at 10% and 12.5 % for 5 days, were transferred directly to 30%o. Only six out of 17 survived the transfer from 10 to 30% and none of these had burrowed when the experiment was con- cluded 13 days after the transfer. Of the 19 clams moved from 12.5 to 30%o, 18 survived but 11 days elapsed before the number burrowing was normal. After direct transfer to experimental salinities clams were slow to start filtering but did clear the water of algae in salinities down to 20%o during the second day. Eventually, clams at 17.5%o filtered and cleared the water consistently. Although some filtering occurred at 10%, it was never normal when clams were transferred directly to salinities lower than 17.5%. Filtering occurred at 7.5%, after acclim- ation, but it was not consistent or normal below 15%. Anadara ovalis were slow to burrow at all salinities and 5 days elapsed before 80% had burrowed, even at 30%. Seven days were required for a comparable percentage at 22.5-27.5% and even longer for those at 20%. At 17.5 % and 15 % a much lower percentage of clams burrowed. After acclimation, more clams burrowed at 17.5 and 15 % but burrowing activity was still reduced at these salinities. Acclimated clams also burrowed at 12.5%, but activity was irregular. Comparatively few blood clams attached by byssus during the experi- ments. These clams were much less motile than Anadara transversa and, unless they were near the sides of the container, had no substratum for attachment. Byssal attachment occurred at 17.5 %o and higher but was far less common below 22.5%o than at higher salinities. The minimum salinity for byssal attachment could be reduced to 12.5% by acclimating blood clams to intermediate salinities. However, only 1 clam attached by a byssus at 12.5 %o. A few attached at 15 and 17.5% but even after acclimation very few clams attached by byssus below 22.5%o. Noetia ponderosa (Say) (Tables 1,2,6) The large blood clam is common in shallow waters along the Atlantic Coast from Virginia to Key West. It is a common bivalve found on the seaside of the Eastern Shore in channels between Spartina marshes. It is also present in deep river channels and in high-salinity (above 20%) portions of Chesapeake Bay. Parker (1955) lists this species with a group found in an area where salinities ranged from 3-42%. Menzel (1964) records it in Florida in salinities above 25 %o. Some blood clams survived for a lengthy period after direct transfer to all salinities down to 12.5% (Table 6). However, mortality continued at 12.5% and 15%, and eventually all died except 1 clam at 15%. Mortality was heavy at 17.5%, but over 75% of the clams kept at 20-30%o survived. After acclimation to inter- mediate salinities, blood clams survived for long periods at 12.5 and 15% though fewer survived than at 17.5 % and higher. Clams acclimated to 15, 17.5 and 20%0 in the Ist experiment were transferred directly to 30%. АП survived, and except for clams transferred from 15 to 30%, all were burrowing and feeding normally within 4 days. Only 3 out of 11 clams transferred from 15 to 30% burrowed. Blood clams filtered normally im- mediately after transfer to salinities of 25- 30%. Clams also filtered immediately after transfer to 20 and 22.5 %o but did not consistently clear the water by filtering out the algae for almost 3 weeks. After the 3rd week, clams also filtered at 17.5 and 15% SALINITY TOLERANCE OF MARINE BIVALVES 63 but never consistently cleared the water. Filtering was rarely observed at 12.5%o and was never normal. No filtering was observed below 12.5%. These limits were not extended by acclimation to in- termediate salinities. Noetia ponderosa were especially sluggish about burrowing in the sand and required 3-4 days to dig in at 12.5-30.0%o salinity. At 27.5 and 30%, over 50% burrowed by the 10th day. Fewer clams burrowed after direct transfer to 22.5 and 20% but 50% dug in at 22.5% between the 10th and the 20th day. No clams burrowed at 20%o until the llth day, and only 17.8% burrowed at this salinity even after 70 days. The minimum salinity at which any clams burrowed was 17.5%o. More clams burrowed at 20 and 17.5%o after being acclimated to intermediate salinities (Table 6). Even after acclimation, however, animals did not burrow at lower salinities. Byssal attachment was usually observed in clams burrowed into the bottom. One clam was found attached to the poly- ethylene container by byssus at 17.5% and another at 20% after acclimation. Byssal attachment was more common at 22.5% but still considerably less than at 25% and higher. Fewer clams attached by byssus during the 2nd experiment than during the Ist, probably because addi- tional sand left less substratum available for attachment. Byssal attachment was less common near the end of experiments. Order Pteroconchida Family Mytilidae Mytilus edulis Linne Along the eastern coast of North America, the edible mussel is found from the Arctic Ocean to South Carolina. In the collection area, permanent pop- ulations of M. edulis are apparently limited by temperature (Hutchins, 1947; Wells & Gray, 1960; Read, 1967) to the cooler, highly saline areas around the mouth of Chesapeake Bay, and to inlets between the barrier islands along the Eastern Shore. Catastrophic summer mor- talities destroy new colonies periodically established in warmer areas. Andrews (1956) records M. edulis at salinities above 15-18% in Virginia. Dodgson (1928) reports survival from TABLE 6. Response of Noetia ponderosa (Say) to different salinities. Salinity at collection sites was 30.6 and 32%. % Surviving Average highest Feeding(0=none, R= % burrowing reduced, N=normal) Salinity After After After After After After oo direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 29 0 0 O 5.0 0 0 O 1) 0 0 O 10.0 0 0 0 0 O O IIS 0 19.8 0 0 O O 15.0 275 67.8 0 0 O R Wee 22:5 91.2 3.1 18.2 O R 20.0 80.0 97.0 17.8 26.2 O N 22.5 1285 100 BET 41.0 R N 2510 85.0 97.4 65.5 52.6 N N DD 95.0 82.1 N N 30.0 92.5 84.2 64 CASTAGNA AND CHANLEY 8.75-31%o, but notes defective byssus formation below 16% and irregular pumping below 12%. Schlieper (1953) found a reduction of oxygen consumption, ciliary activity and heart rate below 15%. Prosser & Brown (1961), referring to other works of Schlieper, report M. edulis as occurring at 4-6%. Motwani (1955) gives the optimum salinity as 20-40% but says this is influenced by other environmental factors. Bayne (1965) found that larval M. edulis failed to grow below 14% and that ор- timum salinity for growth was 18-26%. Apparently, М. edulis can survive at salinities less than 10%o, but about 15%o is necessary for optimum physiological func- tioning and reproduction. Modiolus demissus Dillwyn The ribbed mussel is widely distributed along the east coast from the Gulf of St. Lawrence to Florida (Menzel, 1964). It is found primarily in the intertidal zone where it occurs at a higher level than other bivalves. It is plentiful in seaside salt marshes with near oceanic salinities and is also found in estuaries where salinities are considerably below 20%. Andrews (1953) reports it at all salinities above 8-10 %o. Wells (1961) experimentally determined a ‘salinity death point for M. demissus between 4 and 6%. Vernberg, Schlieper & Schneider (1963) reported a minimum salinity of 2% for ciliary activity of gill filaments and noted a sharp decrease in activity below 4%. In spite of the ability of this species to survive at low salinities, Nagabhushanam (1961) found a marked reduction in rate of pumping as salinities decreased from 32 to 10%. However, his results may show the effects of change in salinity rather than the effects of salinity per se. Brachidontes recurvus Rafinesque The hooked mussel has been reported as occurring from Cape Cod to the West Indies but is probably not commonly found living north of New Jersey. This mussel is common in subtidal areas of Chesapeake Bay and its tributaries where salinities seldom exceed 20-25%. Pearse & Wharton (1938) found it at 5%, while Parker (1959) records it as belonging in an ‘assemblage’ that occurs from 3-40 % . In the laboratory Chanley (1958) found that B. recurvus were not only alive but had “recognizable” gametes after 50 days exposure to salinities from 2.5-27%. Those kept in fresh water all died within 30 days. Allen (1960), however, reported 95% mortality of all mussels kept at salinities below 4.5% and heavy mortality below 6% in only 19 days. Nagabhushanam (1965) noted a decrease in heart rate from 35-31 beats per min. with a drop in salinity from 18-7.2%. A further decrease to 16 beats per min. occurred between 7.2 and 3.6%. At 1.8% the heart beat was only 3 beats per min. Again, these figures may indicate the effect of salinity change rather than salinity per se. The minimum salinity for survival of this species is probably between 2.5 and 6.0%o. Amygdalum papyria Conrad (Tables 1,2,7) The paper mussel is found from Maryland south to the Gulf of Mexico. It is found in areas of moderate salinity such as the lower York and Rappahannock rivers in Virginia. Although abundant in limited areas, it is not generally distributed and is probably the least known of the mussels. It is apparently euryhaline and has been reported аз occurring in areas where salinity may be as low as 10% (Wass, personal com- munication) or as high as 45°%o (Parker, 1960). All mussels transferred directly from about 20%o to O and 2.5% died (Table 7). In the 1st experiment all mussels trans- ferred to 5%o also died. However, 55% survived this transfer in the 2nd experi- ment. Best survival was observed at salinities from 12.5-20%o. The mortality at higher salinities (22.5-30%0) was not as abrupt as that at 0, 2.5 and 5% and occurred only after mussels had apparently SALINITY TOLERANCE OF MARINE BIVALVES 65 adapted to salinities by filtering normally, burrowing, attaching by byssus and by nest-building. The salinity tolerance limits of Amygda- lum papyria could be extended only slightly by moving them gradually to lower salinities. In the lst experiment 10 mussels surviving at 5% for 31 days died within 4 days after transfer to 2.5%o. In the 2nd experiment, however, 17 out of 23 mussels survived and were main- tained at 2.5 % for 5-15 days before being moved to fresh water or before termina- tion of the experiment. Mussels did not survive when moved from 2.5% to fresh water. After direct transfer to experimental salinities, some mussels burrowed in all salinities from 2.5-30%o though the per cent burrowing was reduced below 12.5%o. After acclimation in intermediate salin- ities, burrowing was apparently normal whenever mussels survived. However, a smaller percentage of mussels burrowed late in the experiment regardless of salinity. Some burrowing occurred at salin- ities which eventually proved lethal. Three mussels burrowed even in fresh water but did not repeat the performance when dug up 2 days later. Filtering was apparently normal at 10% and higher, though in the 2nd experiment it was initially reduced at 10%o. Normal filtering was occasionally observed at 2.5 and 5% after prolonged exposure to these salinities. Byssal attachment and nest-building were possible at any salinity in which animals survived. A. papyria differs from the more familiar Mytilus edulis in this respect, since the latter is capable of surviving in salinities at which byssus formation is defective (Dodgson, 1928). Family Ostreidae Crassostrea virginica Gmelin The American oyster is common inter- tidally and subtidally from the Gulf of St. Lawrence south to the Gulf of Mexico. It is widely distributed in Virginia where salinities are higher than 6-10%o (Andrews, 1953). The oyster has been the subject of much research and no attempt is made here to present a complete review of all pertinent literature. Only a few references are cited to establish the salinity tolerance of this species. Baughman (1947) and, TABLE 7. Response of Amygdalum papyria (Conrad) to different salinities. Salinity at collection sites was about 21%o. % Surviving Average highest Feeding (0= попе, R= % burrowing reduced, N=normal) Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 O 10) 29 0 JON 5.0 50.0 O R 5.0 27.5 60.5 27.9 53.0 R R aS 55.0 86.0 65.0 45.6 В В 10.0 70.0 94.6 TOD) 52.8 N N 125 82.5 9741 97.5 76.0 N N 15.0 95.0 90.0 100 100 N N 7.5 75.0 100 М М 20.0 75.0 100 N N 22.9 40.0 100 N N 25.0 45.0 97.5 N N 27.9 45.0 95.0 N N 30.0 37.0 90.0 N N 66 CASTAGNA AND CHANLEY more recently, Galtsoff (1964) give refer- ences describing the salinity tolerance of oysters. Salinity limits for survival. Oysters can survive over a wide range of salinities. Ingle & Dawson (1951) report commercial production in areas with an annual salinity variation from 0-42.5%. Butler (1952) found self-sustaining populations in areas where salinity ranged from 0.2-3.6%o for 5 consecutive months annually. However, field observations by many investigators set the minimum salinity for indefinite sur- vival at 4-5 % (Ryder, 1885; Arnold, 1868; Belding, 1912; Loosanoff, 1932; and many others). Parker (1960) observed that oyster reef formation occurs only between salinities of 10 and 30%o even though oysters are found outside these limits. The optimum salinity range for survival has been described as 14.1-22.2%o (Moore, 1900). Galtsoff (1964) states, according to the Venice system of classification of saline waters adopted by the International Association of Limnology and the Inter- national Union of Biological Sciences in 1958, that the range of salinity favorable for C. virginica falls within 2 zones, the polyhaline (30-18%) and the mesohaline 18-5 oo ). Laboratory experiments show close agreement with these field observations. Vernberg et al. (1963) found a marked decrease of ciliary activity in excised gill tissue below 4%. This agrees well with Fingerman s (1959) earlier report that ciliary activity occurred between 5 and 35%. According to Loosanoff (1952), some oysters survived when kept con- stantly at 5% although there was а high mortality. Survival was normal at 7.5%o and higher. Chanley (1958) reports similar salinity limits for recently metamorphosed C. virginica. Salinity limits for growth and feeding. In Canadian waters, oysters apparently do not “fatten” or increase proportionally in dry weight when salinity drops below 20 %0 (Medcof & Needler, 1941; Medcof, 1944). According to Nelson (1923), the minimum salinity at which growth and feeding occur is based on the salinity at which the oyster is acclimated. Loosanoff (1952), however, maintains that oysters adapt rapidly to salinity change and resume pumping activities within a few hours. He noted that a salinity of 10% is the minimum for normal growth of adult oysters. He observed feeding at 5% but says no growth occurred below 7.5%. Chanley (1958) reported slight growth of recently metamorphosed oysters at 5%, with optimum growth between 12.5 and 25%. Salinity limits for reproduction. The minimum salinity for gametogenesis has been reported as 6% by Butler (1949), who noted delay of gametogenesis until salinity rose above this level. Loosanoff (1952) reported 7.5 % as the minimum for gametogenesis. Davis (1958) observed egg cleavage from 7.5-35%o with good development from 10-22.5%. Much higher limits were given by Amemiya (1926) who records egg development from 18-40.1%, with an optimum range of 19.3-35.1%o. Larval development has been reported as occurring between 14 and 39% (Amemiya, 1926), with optimum devel- opment between 25 and 29%. Clark (1935) is in general agreement with these ranges. Nelson (1909), however, found larvae in plankton samples when salinity was as low as 11.5%. Furthermore, Davis (1958) reported larval growth at as low as 5%, with the optimum between 17.5 and 22.5%. Under certain lighting conditions, Haskin (1964) found that activity of oyster larvae increased with increasing salinity and that all larvae failed to swim when salinity was less than 4.8%o. Davis (1958) gives a minimum salinity of 10% for metamorphosis of oyster larvae, but Prytherch (1934) watched larvae metamorphose at 5.6%. The highest salinity at which he observed metamorphosis was 32.2 %0. Discussion. There are several explana- tions for the apparent contradictions between these reports. Davis (1958) demonstrated that the salinity range for optimum egg development is depen- dent on the salinity at which game- SALINITY TOLERANCE OF MARINE BIVALVES 67 togenesis occurred. Furthermore, it is likely that the degree and rapidity of change from environmental to experi- mental salinity influenced survival and development more than the actual salin- ities in some experiments. Davis & Calabrese (1964) have shown that the influence of temperature on the salinity tolerance of oyster eggs and larvae is minimal, though temperature tolerances are reduced at low salinities. Oyster eggs and larvae are known to be extremely sensitive to dissolved substances (Davis & Chanley, 1956), and possibly an excess or lack of some particular constituent in experimental salinities may have deter- mined limits rather than the actual salin- ity used. The concept of physiologically different races (Stauber, 1950) may also explain some differences. Although races of oysters have never been defined in terms of salinity, the wide distribution of this species could conceivably permit development of races with different salinity tolerances. Family Pectinidae Argopecten irradians Lamarck The bay scallop is found from Nova Scotia to northern Florida and along the Gulf Coast to Texas. In Virginia this species was abundant in Eastern Shore seaside bays until the disappearance of eel grass in the early 1930's (Wass, 1965). Currently, bay scallops are found only rarely in the Eastern Shore lagoons where salinity is usually about 30%. According to Belding (1910), scallops are found in New England in areas where salinity ranges from 14.1-36.3%. In North Carolina, Gutsell (1930) reported a “distri- butional minimum salinity of 20% but noted that scallops survived exposure to 16.2% after unusually heavy rains. In Florida this species is found in salinities above 25% (Menzel, 1964). In the laboratory, Vernberg et al. (1963) noted a reduction in gill ciliary activity below 18% and a complete cessation of activity below 12%. They further observed that cold-acclimated scallops were more resistant to adverse salinity than were warm-acclimated scallops. The minimum salinity at which bay scallops survive would appear to be about 14 %o. Anomia 1.2.8) simplex Orbigny (Tables The jingle is a common fouling organism found attached to shells, buoys, wharfs and other solid substrata from Cape Cod to Florida and in the Gulf of Mexico. It is found subtidally and is frequently associated with oysters. In Texas it has been reported from areas where salinity ranged from 11-40% (Ladd, 1951). It is found at salinities above 15% in Virginia (Andrews, 1953). Scheltema & Truitt (1954) found recently metamor- phosed individuals on test panels in Chesapeake Bay at salinities from 15.2- 26.3 %o. Most Anomia simplex survived direct transfer from 31%o to salinities as low as 17.5 % but direct transfers to salinities of 15% and lower resulted in complete mortality (Table 8). When salinities were reduced gradually, jingles survived to 12.5 and 10%, though it is doubtful that indefinite survival would have been possible at 10%. All jingles died in 5 days when kept at a salinity of 7.5%o even after acclimation. Half of the acclimated jingles survived a transfer directly from 12.5 to 30%o in 1 experiment, but in a 2nd experiment none survived this treatment. Animals transferred to 30% from salinities of 15% and above suffered по mortality and rapidly readapted to 30%o. Anomia simplex filtered and reacted normally immediately after direct transfer to 22.5% and higher. Two ог 3 days elapsed before both filtering and the closing reaction were normal at 17.5- 22.5%. After acclimation, the minimum salinity at which these activities were nor- mal was 12.5%, though some filtering was observed as low as 7.5%. Order Heterodontida Family Carditidae 68 CASTAGNA AND CHANLEY Venericardia tridentata Say Venericardia tridentata has been reported as common in more shallow water from North Carolina to southern Florida. In Florida this species occurs in salinities above 25% (Menzel, 1964). It is found only rarely in Virginia. Family Corbiculidae Polymesoda caroliniana Bosc Polymesoda caroliniana is common in low-salinity muddy areas from Virginia south. Van der Schalie (1933) found this species where salinity ranged from fresh water (at low tide) to about 19%. He also observed that most clams survived for 2 weeks even when kept at oceanic salinities in the laboratory. Parker (1959) found P. caroliniana where salinity is always less than 10% but never in absolutely fresh water. In Virginia this species has been found only in the James River at salinities from almost fresh water to 15% (Andrews € Cook, 1951). Family Dreissenidae Congeria leucophaeta (Conrad) (Tables 1,2,9) This species is common in brackish and fresh water from New York to Florida. In Virginia it is found at salinities below 10%o. Congeria leucophaeta were collected at a salinity of about 7%. However, they were maintained in the laboratory at about 17.5%o for several weeks prior to these experiments. Most survived direct transfer to all experimental salinities from 0-30%o (Table 9). Byssal attachment and filtering were normal at these salinities. However, nearly 2 weeks elapsed before animals adapted to 0, 27.5 and 30%o. After this 2-week period, 65.3% of those kept in fresh water survived direct transfer to 30%o and adapted to that salinity. Only 11% (2 out of 18 clams) survived the reciprocal direct transfer from 30%o to fresh water, but these 2 clams did eventually show evidence of filtering and attach by byssus in fresh water. No mortality was associated with similar reciprocal transfers between 2.5%o and 27.5%. Within 1 week of this transfer, clams were attached and filtering normally, Family Lucinidae Lucina multilineata Tuomey & Holmes (Tables 1,2,10) Lucina multilineata occurs commonly TABLE 8. Response of Anomia simplex (Orbigny) to different salinities. Salinity at collection site was about 31%o. % Surviving Feeding (0= попе, R= reduced, N=normal) Salinity After After After After %o direct acclimation direct acclimation transfer transfer 0 0 0 2,5 0 0 5.0 0 0 1.9 0 0 0 В 10.0 0 68.9 0 В 1925 0 86.6 0 М 15.0 0 97.3 0 М 17.5 76.7 98.1 М М 20.0 100 96.2 М М 22.5 83.3 94.7 М М 25.0 100 96.4 М М 21.5 94.3 N 30.0 96.3 N SALINITY TOLERANCE OF MARINE BIVALVES 69 TABLE 9. Response of Congeria leucophaeta (Conrad) to different salinities. Salinity at collection site about 7 %o. % Surviving Highest % Feeding (0=noné, R= attaching reduce, N=normal) by byssus Salinity After After After %o direct transfer direct transfer direct transfer 0 85.0 94.1 М Po) 95.0 100 N 5.0 100 100 N 1) 100 100 N 10.0 100 100 N 1949 100 95.0 N 15.0 95.0 84.2 N 1785 90.0 94.4 N 20.0 95.0 100 N 22.5 90.0 94.4 М 25.0 100 95.0 М DO 80.0 94.1 N 30.0 95.0 100 N TABLE 10. Response of Lucina multilineata to different salinities. Salinity at collection site about 22 Vo. % Surviving Average highest Feeding (0=none, R= % burrowing reduced, N=normal) Salinity After After After After After After % direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 O 25 0 0 O 5.0 0 0 0 0 (0 O 1:9 20.0 100 10.0 95.0 R N 10.0 100 94.7 90.0 88.9 N N 12:5 100 100 80.0 100 N N 15.0 100 100 N 17.5 20.0 22.5 90.0 100 25.0 27.5 90.0 100 N 30.0 70.0 100 100 100 R N from the shore to depths of over 700 ft mon in Virginia and is found in Chesa- from North Carolina to both coasts of peake Bay at about 20% (Wass, 1965). Florida. In Florida it is found in salinities Some Lucina multilineata survived above 25% (Menzel, 1964). It is less com- direct transfer from 22% to experimental 70 CASTAGNA AND CHANLEY salinities from 7.5-30% (Table 10). Mortality was heavy after direct transfer to 7.5% but negligible at higher salinities. After acclimation to inter- mediate salinities, survival was normal at 7.5%. Clams did not survive at 5% even though gradually acclimated to that salinity. Burrowing and filtering were generally normal at all salinities in which clams survived. Family Cardiidae (Conrad) Laevicardium mortoni (Tables 1,2,11,12) Morton s cockle is a small, active clam common in shallow, protected sandy areas from Cape Cod to Florida and the Gulf of Mexico. Ladd (1951) found this species in an area where salinity varies from 16- 42%o and Parker (1960) found it in an “assemblage” occurring in а salinity range of 30-45%. In Virginia, L. mortoni is fairly common from 15-25% and is periodically abundant in scattered areas of Chesapeake Bay and its tributaries. Laevicardium топот either quickly adapted to experimental salinities or died. Although some survived direct transfer from about 20% to salinities from 7.5-30°%0, there was appreciable mortality at 7.5 and 10% (Table 11). The salinity limits could not be extended by acclimating clams in inter- mediate salinities, although the percent survival at 7.5, 10 and 30% was improved. There were minor differences between experiments. In the Ist experiment all of the 33 clams moved to 7.5 % were dead within 2 days. In the 2nd experiment clams survived and reacted normally at 7.5%. Almost no mortality occurred at 10% and higher in either experiment and по clams survived at 5%o. At the conclusion of these experiments, clams surviving at low salinities were transferred directly to high salinities and survivors at high salinities were transferred directly to low salinities. Those transferred from 10 and 12.5% to 30% all died within 24 hours (Table 12). Only one clam out of 19 survived transfer from 10 to 27.5 %o. Surprisingly, all clams survived reciprocal transfers from 30% to 10 or 12.5%o. No mortality was associated with changes from salinities above 15 % to 30%. Fewer clams burrowed after direct transfer to 7.5 and 10% than to higher salinities, and none burrowed at lower salinities. After acclimation to intermediate _ salinities, burrowing was normal at 10%o and im- proved at 7.5%. Some burrowing occurred at 5% after acclimation though clams eventually died at this salinity. Filtering rapidly became normal at 10% and higher. Acclimated clams eventually filtered normally after exposure to 7.5% and some filtering occurred at 5.0%o. Family Veneridae Mercenaria mercenaria (L.) The commercially important hard clam or quahog is abundant at moderately high salinities along the east coast from the Gulf of St. Lawrence to Florida. In Virginia this species is found in a variety of substrata intertidally and sub- tidally at salinities above 10% (Wass, 1965). Belding (1931) gives the salinity range of the quahog as 12.8-35%o, but says their survival is possible in salinities up to 46%. He does not believe that salinity influences growth within the normal range. Pratt & Campbell (1956) found hard clams occurring naturally from 21.4-31.9 % and also expressed the opinion that growth was unaffected by salinity within this range. Turner (1953), however, reported no growth of adult clams at 19-21%o and optimum growth between 24 and 28%. Chanley (1958) reported similar levels for optimum growth of juveniles and growth decreasing with salinity to little or none below 17.5%. Minimum salinity for survival is given as 12.5%o. Larvae appear to require a slightly higher salinity than juveniles or adults. Metamorphosis did not occur below 20%o (Turner € George, 1955). Davis (1958) found larval growth improved with SALINITY TOLERANCE OF MARINE BIVALVES rik TABLE 11. Response of Laevicardium mortoni (Conrad) to different salinities. Salinity at collec- tion sites about 21%o. % Surviving Average highest Feeding (0=none, R= % burrowing reduced, N=normal) Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 2.5 0 0 O 5.0 0 0 38.4 R 7.5 20.0 50.0 20.2 62.5 R R 10.0 85.0 98.7 83.5 99.1 N N 12.5 97.5 100 100 100 М М 15.0 97.5 100 100 100 М М 17.5 97.5 100 100 100 М М 20.0 92.5 100 100 100 М М 2230 95.0 100 100 100 N N 25.0 100 97.4 100 100 N N 27.5 97.5 100 100 100 N N 30.0 90.0 97.4 100 100 N N TABLE 12. Survival of Laevicardium mortoni after direct transfer between the extreme experimen- tal salinities to which they had become acclimated. Transferred to (Salinity in % ) Transferred from (Salinity in %o ) Le 30.0 10.0 30.0 10.0 27.5 12.5 30.0 15.0 30.0 17.5 30.0 27.5 17.5 30.0 15.0 30.0 12.5 30.0 10.0 increasing salinity from 15-27.5% and reports no metamorphosis below 17.5%o. He also reports that eggs developed normally from 20-35% with an optimum salinity about 27.5 %o. Dosinia discus Reeve This species is found along the east coast from Virginia to Florida but occurs only rarely in Virginia. Menzel (1964) Number transferred Number surviving 20 0 19 0 19 1 19 0 17 15 18 18 20 19 20 20 18 18 14 13 lists it at salinities above 25% in Florida. D. discus is common in areas of North Carolina where the annual salinity range is from 6-38% but seldom less than 15% (Norton, 1947). In laboratory experiments D. discus survived 12 days in 50% seawater and 15-17 days in 75% seawater (Norton, 1947). Unfortunately, even controls were dead on the 19th day. 72 CASTAGNA AND CHANLEY Gemma gemma Totten (Tables 1,2,13) This small clam is very common along the east coast from Labrador to North Carolina (Sellmer, 1967). In Virginia it is frequently found in abundance in sand where salinity ranges from 5-30%o (Wass, 1965). Gemma gemma responded similarly in both experiments, adapted well to labora- tory conditions, and survived for pro- longed periods even at salinities that eventually proved lethal. Clams survived direct transfer to salinities ranging from 10-30%. When transferred to 7.5%, all survived for several days, but then a slow steady mortality occurred and finally only 22.5% were still alive (Table 13). Salinities lower than 7.5% eventually proved lethal to all clams, although 1 clam did survive 51 days at 5%o. After acclimation to intermediate salinities, survival of Gemma at 7.5°%0 was. normal. However, clams transferred to 5.0 °0 suffered a heavy mortality even after acclimation at 7.5%. All those transferred to 2.5% or fresh water died. When clams were moved from 7.5 to 25%o or from 30 to 10%, none died and filtering and burrowing were normal. Clams were capable of burrowing after direct transfer to all salinities of 5% and higher. However, at least 3 weeks were required for normal numbers to burrow at 10%o and only a few burrowed at 7.5 and 5%o unless first acclimated at intermediate salinities. Burrowing was never observed at 2.5%o or in fresh water. Gemma filtered algae from the water at all salinities from 2.5-30°%o. However, filtering was not normal for 5-10 days at 10%o and was reduced and irregular at 7.5% and lower. Normal filtering occurred at 7.5% if animals were first acclimated at intermediate salinities, but was never normal at lower salinities. When the survivors were discarded at the conclusion of these experiments, juvenile Gemma were found in many con- tainers. Consequently, to determine reproductive ability at varying salinities, another experiment was started 23 April 1965, in which 10 Gemma were placed in salinities ranging from 0-30%o. Оп 20 May, only clams at salinities from 10-30%o were still alive. Juvenile clams were found at all these salinities, indicating the ability to reproduce from at least 10-30%. TABLE 13. Response of Gemma gemma (Totten) to different salinities. Salinity at collection sites 23.2 and 20.0%. % Surviving Salinity After After After %o direct acclimation direct transfer transfer 0 0 0 0 9,5 0 0 0 5.0 0 63.9 10.0 10 22/9 100 52.9 10.0 100 98.5 100 125 97.5 99.0 100 15.0 100 100 100 17.5 97.5 100 100 20.0 100 100 22.9 100 100 25.0 100 100 100 РТО 97.5 100 100 Average highest % burrowing Feeding (0= попе, R= reduced, N=normal) After After After acclimation direct acclimation transfer 0 O 0 O R 53.8 O R 98.7 R N 99.4 N N 100 N N 100 N N 100 N N 100 N N 100 N N 100 N N SALINITY TOLERANCE OF MARINE BIVALVES 73 Family Petricolidae Petricola pholadiformis | Lamarck (Tables 1,2,14) This species is common in peat and clay from the Gulf of St. Lawrence to the Gulf of Mexico. Andrews (1956) found it at salinities from 15-25 % and Wass (1965) reported it from 20-30%. We have also collected it in areas where © salinity exceeds 30 %o. Although all Petricola pholadiformis used in the 3 experiments were collected from the same locality, the salinity toler- ance varied considerably. The combined results of all 3 experiments are sum- marized in Table 14. When clams were transferred directly from a salinity of 30-34 %o to experimental salinities, the minimum salinities at which they survived in the 3 experiments were 10, 12.5 and 17.5%, respectively, but mortality was heavy at 10%. The greatest tolerance range was noted in the experi- ment conducted at the coolest tempera- tures. After acclimation at intermediate salinities, clams could tolerate a lower minimum salinity. However, even after acclimation the minimum salinity at which clams survived was different in each experiment (7.9. 10.0% sand # 1275250: respectively). After acclimation at minimum salinities, clams were trans- ferred directly to 30% with virtually no mortality. Within 1 or 2 days they had readapted to 30% and were burrowing and filtering normally. Apparently, slight- ly greater salinity changes could be tolerated when the change was toward 30 %o rather than away from it. At minimum salinities for survival, comparatively few Petricola burrowed. At higher salinities virtually all surviving animals burrowed into the sand sub- stratum. After acclimation at intermediate salinities, a few clams burrowed at 5%, but this salinity was eventually lethal. Filtering was normal whenever sur- vival and burrowing were normal. Even after acclimation, feeding was reduced at 10%o and lower. TABLE 14. Response of Petricola pholadiformis (Lamarck) to different salinities. Salinity at collec- tion site 30-34%. % Surviving Average highest Feeding (0= попе, R= % burrowing reduced, N=normal) Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 O 25) 0 0 O 5.0 0 0 0 5.9 O O eo 0 67.1 0 51.0 O R 10.0 15) 90.8 10.0 81.8 В В 12.5 67.5 96.2 75.0 95.2 N° N 15.0 75.0 98.5 Го 96.4 № М ee 95.0 97.0 100 98.4 N N 20.0 97.5 97.1 100 100 N N 29.5 90.0 100 100 100 М М 25.0 85.0 93.6 100 95.0 М М 271.9 92.5 100 N 30.0 82.5 100 N °Except in 1 experiment where these salinities proved lethal. Тейта agilis Stimpson (Tables 1,2,- 15) Tellina agilis is found from the Gulf of St. Lawrence to North Carolina. It is com- mon in several areas in Virginia where the salinity is above 18% (Wass, 1965). Tellina were collected from an inter- mediate (20-24%) and а high (33%) salinity area. Two experiments were con- ducted with both groups. The results of all experiments are summarized in Table 15. Most Tellina Нот 33% died when transferred directly to salinities below 20%, although a few survived at 17.5%. Most clams from 20-24% survived direct transfer to salinities from 12.5-30%о with a few surviving at 10%. After acclimation at intermediate salinities, both groups had similar minimum limits for survival. A few clams survived at 7.5%o but mortality was greater at salinities below 12.5%othan at higher salinities. Almost all clams burrowed rapidly at all salinities at which they survived. The apparent reduction in percent burrowing (Table 15) after direct transfer to 12.5- 17.5% reflects the failure of high-salinity CASTAGNA AND CHANLEY Tellina agilis to burrow at salinities that were eventually lethal. Filtering was normal at about 12.5% and higher. This limit was not appreciably lowered even when clams were acclimated to intermediate salinities. Macoma balthica (L.) (Tables 1,2,16, 17) This widely distributed species is com- mon along the eastern coast of North America from the Arctic Sea to Georgia. It is apparently euryhaline and is found in oligohaline as well as oceanic salinities. This species is abundant in soft substrates at low salinities (5-15%0) in Chesapeake Bay and its tributaries (Wass, 1965). Macoma balthica survived direct trans- fer from 13-17% to salinities from 2.5- 30%o (Table 16) except in 1 experiment when the minimum salinity for survival was 5.0%. After acclimation at inter- mediate salinities, virtually all clams survived at 2.5-30%o and did not die until 8-9 days in fresh water. Clams that survived 5-6 days in fresh water before being returned to higher salinities, TABLE 15. Response of Tellina agilis (Stimpson) to different salinities. Salinity at collection sites 20, 24 and 33%o. % Surviving Average highest % burrowing Feeding (O=none, R= reduced, N=normal) Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 10) 25 0 0 O 5.0 0 0 0 0 O О Lo 0 10.7 0 76.6 O R 10.0 15.0 66.2 25.0 97.4 R° R 1235 32.5 86.2 50.0 97.9 Re N 15:0 40.0 96.9 50.0 100 N° N 17.0 57.5 95.4 19.0 98.9 N° N 20.0 92.5 100 97.5 100 N N 220 92.5 100 100 100 М М 25.0 95.0 100 100 93.8 М М 97.5 92.5 100 М 30.0 82.5 100 М “Except for the high salinity groups that died at this salinity. SALINITY TOLERANCE OF MARINE BIVALVES 75 TABLE 16. Response of Macoma Баса (L.) to different salinities. Salinity at collection sites 13, 15.8 and 16.7%. % Surviving Average highest % burrowing Salinity After After After After %.o direct acclimation direct acclimation transfer transfer 0 0 34.9° 0 100 265 60.0 97.0 66.7 100 5.0 96.7 100 100 100 leo 96.7 94.9 96.3 100 10.0 86.7 100 100 100 12.5 96.7 100 100 100 15.0 76.7 96.7 17.9 96.7 100 20.0 86.7 100 100 100 2975 80.0 100 96.7 100 25.0 96.7 100 100 100 27.5 96.7 97.4 100 100 30.0 83.7 95.8 100 100 “These survivors were all from 1 experiment and were exposed to fresh water only 5-6 days. Longer exposure would probably have been fatal. TABLE 17: Survival of Macoma balthica after direct transfer between extreme experimental salinities at which they survived. Transferred from Transferred to Number Number (Salinity in %o) (Salinity in %o ) transferred surviving 2.5 30.0 10 0 2.5 279 9 4 5.0 30.0 8 0 5.0 25.0 10 9 7.5 30.0 10 0 10.0 30.0 9 9 10.0 20.0 7 7 20.0 10.0 6 6 22.5 7.9 5 5 25.0 5.0 9 8 27.5 2.5 9 8 30.0 7.5 10 10 30.0 5.0 10 10 30.0 2.9 9 9 would probably have died if they had quickly killed when transferred from remained in fresh water. salinities of 7.5% and lower to 30%. Clams were not harmed by sudden Reciprocal changes from 30% to 7.5, 5.0 transfer from 10 to 30%, but they were and 2.5% resulted in no mortality and 76 CASTAGNA AND CHANLEY clams adapted quickly to the new salinity (Table 17). Virtually all surviving clams burrowed. Even in fresh water all clams burrowed after acclimation at 2.5%. Within a few days when clams were dug up, they failed to burrow again and died. Масота balthica feeds primarily on detritus rather than suspended matter and accurate observations on its feeding or filtering were not possible. Macoma mitchelli Dall (Tables 1,2, 19.19) This species is abundant in many of the brackish water creeks of Chesapeake Bay at salinities from 2-20%o (Wass, 1965). Some Macoma mitchelli survived direct transfer from field salinities (14.9- 17%) to all salinities from 2.5-30%o. Mortality at 2.5 and 5% was greater after such a transfer than at other salinities (Table 18). Surprisingly, clams taken from a salinity of 14.9%o were killed by transfer to 2.5% and only 4 out of 10 survived at 5%. Over 70% of the clams taken from 17%o survived when transferred to these salinities. After acclimation at inter- mediate salinities, no unusual mortality occurred at 2.5-30%. When clams were TABLE 18. Response of Macoma mitchelli (Dall) to different salinities. Salinity at collection sites 14.9 and 17.0%. % Surviving Average highest % burrowing Salinity After After After After %o direct acclimation direct acclimation transfer transfer 0 0 0 5 1128 225 33:0 95.6 14.3 76.3 5.0 60.0 97.9 72.3 79.3 7.5 90.0 100 72.8 81.4 10.0 100 96.3 85.0 81.7 12.5 90.0 100 1225 88.9 15.0 95.0 90.0 LS 90.0 100 20.0 90.0 100 90.0 100 22.5 100 100 85.0 96.7 25.0 80.0 100 81.6 92.0 С, 95.0 94.5 85.0 94.3 30.0 80.0 90.0 95.0 91.1 TABLE 19. Survival of Macoma тисйей after direct transfer between extreme experimental salinities to which they had become acclimated. Transferred to (Salinity in %o ) Transferred from (Salinity in %o ) Number transferred Number surviving 2.5 30.0 5.0 30.0 7.5 30.0 10.0 30.0 30.0 12.5 30.0 10.0 30.0 7.5 30.0 5.0 30.0 2.5 18 0 10 0 1. 0 9 1 6 5 10 10 17 14 10 3 18 0 SALINITY TOLERANCE OF MARINE BIVALVES moved to fresh water, they eventually died though some survived for nearly 3 weeks. Rapid salinity increases of 20%o and more killed most clams (Table 19). Rapid salinity decreases of 25% resulted in little mortality and a few clams survived a rapid salinity decrease of 27.5 % . Macoma mitchelli burrowed at all experimental salinities including fresh water. However, a lower percentage of clams burrowed after direct transfer to O and 2.5%. After acclimation there was little difference in burrowing ability of clams from 0-30% although clams in fresh water eventually weakened and died. Macoma mitchelli did not clear the water of algae satisfactorily throughout the experiments. Possibly they are primarily detritus rather than filter feeders. Some filtering did occur at 2.5-30%o. Macoma tenta Say Macoma tenta is found from Cape Cod to Florida in a sandy substratum in shallow water. In Florida it occurs in sandy mud at salinities above 25% (Menzel, 1964). In Virginia it is found in silt-clay substrata at —] AN salinities from 20-30% (Wass, 1965). Family Semelidae Abra aequalis Say Abra aequalis is abundant from North Carolina to Texas. It is found at salinities above 25%o in Florida (Menzel, 1964). In Virginia it is rarely encountered (Wass, 1965). Family Donacidae Donax variabilis Say (Tables 1,2,20) Donax variabilis, the colorful toquina of southern beaches, is common from Virginia to Florida and Texas. Because of its unique habitat in the surf zone of sandy beaches, it is seldom found at salinities below 30%. In Virginia, D. variabilis is found on ocean beaches during the summer and autumn at salinities above 30%o. Although the 2 experiments involving this species were conducted under different temperature regimes and with clams of different sizes, the results were TABLE 20. Response of Donax variabilis Say to different salinities. Salinity at collection sites 33- 35%. % Surviving Average highest Feeding (0=none, r= % burrowing reduced, N=normal Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 O 25 0 0 O 5.0 0 0 O AD 0 0 0 71.9 O R 10.0 0 38.5° 0 94.8 O R PA) 0 94.6 0 100 O N 15.0 0 100 120 99.3 O N 1725 20.0 99.2 100 100 R N 20.0 60.0 100 100 100 N N DS 85.0 98.7 100 100 N N 25.0 92.5 100 100 100 N N PAT) 97.5 100 N N 30.0 92.5 100 N N “This salinity would probably have eventually killed all. 78 CASTAGNA AND CHANLEY remarkably similar. Donax variabilis survived direct trans- fer to salinities from 17.5-30%, but heavy mortality was associated with trans- fers below 22.5% and only 20% survived direct transfer to 17.5% (Table 20). The relatively narrow salinity limits indicated in the first phase of these experiments were extended appreciably by acclimating coquinas to intermediate salinities. After acclimation, clams sur- vived well and reacted normally at salinities as low as 12.5 %o. At the conclusion of the acclimation phase of the experiments, surviving Donax variabilis were transferred directly to 30%. Only 1 out of 36 clams died when transferred from 12.5% (the minimum salinity at which clams lived) to 30%. None died when transferred from 15 to 30%o. Donax variabilis burrowed and filtered immediately at all salinities at which they survived. In fact, several dug in and fed at either 15%o after direct transfer, or 7.5 and 10%o after acclimation even though these salinities eventually proved lethal. Family Sanguinolariidae Tagelus plebeius Solander (Tables 12.41.22) This species is listed as common from Cape Cod to Florida and in the Gulf of Mexico. It is 1 of the more common bivalves of Virginia. Andrews (1956) reports it as euryhaline and common above 10%o. Tagelus plebeius were collected from intermediate salinity areas (about 20%o) for 3 experiments. These clams survived direct transfer to salinities from 2.5-30%o, though only about 1/3 survived at 2.5%. In the 4th experiment clams were obtained from nearly oceanic salinities. None of these clams survived direct transfer to either 2.5 or 5% and only 10% survived at 7.5%. Survival from 10-30% was normal. After acclimation at inter- mediate salinities, clams from both areas survived well at 2.5% and higher. None survived when transferred to fresh water. The combined results are shown in Table 21. After clams from the intermediate salinity area were acclimated to a salinity of 30%, they were transferred directly to TABLE 21. Response of Tagelus plebeius Solander to different salinities. Salinity at collection sites 14.9, 20.4, 21.8 and 32.4%. % Surviving Salinity After After After %o direct acclimation direct transfer transfer 0 0 0 0 25 27:5 86.9 19.2 5.0 12.5 81.2 46.4 10 12:0 95.8 56.1 10.0 97.5 95.4 78.9 12.5 97.5 98.8 87.2 15.0 100 91.1 87.5 125 100 83.9 82.5 20.0 97.5 94.] 79.4 22.5 100 89.5 Wed 25.0 97.5 100 91.9 Fico 97.5 100 80.0 30.0 100 95.6 90.0 Average highest % burrowing Feeding (0= попе, R= reduced, N=normal) After After After acclimation direct acclimation transfer 0 O O 81.1 O R out R N 79.6 R N 85.9 N N 85.2 N N 85.7 N N 81.3 М М 87.6 М М 81.8 М М 78.9 М М 90.0 М М 86.0 М М SALINITY TOLERANCE OF MARINE BIVALVES 79 TABLE 22. Survival of Tagelus plebeius after direct transfer between the extreme experimental salinities to which they had become acclimated. Transferred to (Salinity in %o) Transferred from (Salinity in %o) 2.5 30.0 2.5 27.5 2.5 25.0 5.0 30.0 7.5 30.0 10.0 30.0 12.5 30.0 15.0 30.0 30.0 7.5 30.0 5.0 30.0 2.5 salinities of 7.5 and 5.0% without appreciable mortality (Table 22). Almost 2/3 survived direct transfer to 2.5%, whereas clams from the high salinity area were killed by comparable _ salinity changes. When clams from both groups were acclimated to 2.5 and 5% and then transferred directly to 30%, all died. Transfer from 7.5 to 30%, 2.5 to 27.5%, and 2.5 to 25% also resulted in heavy mortality (Table 22). Clams burrowed and filtered after direct transfer to salinities of 2.5-30%o. However, activity was reduced below 10%o (Table 21). After acclimation, burrowing and filtering were not appreciably increased at salinities from 2.5-30%o. Tagelus divisus Spengler This species also is found from Cape Cod to Florida and in the Gulf of Mexico. Fraser (1967) studied a Florida population living in an area where salinity ranged from 29.1-39.3 %. In Virginia it has been found only subtidally in moderately high salinity water. Family Solenidae Ensis directus Conrad (Tables 1,2,23) The common razor clam is found from Labrador to South Carolina and probably Florida. In Virginia, Wass (1965) lists it as an intertidal and subtidal form found Number transferred Number surviving 20 0 20 4 9 5 34 0 24 11 15 12 15 14 Y 6 29 29 19 18 38 25 above 20%. In some areas of Chesapeake Bay it is common at much lower salinities (Pfitzenmeyer, personal communication). Under experimental conditions Chanley (1958) found that E. directus could be acclimated to survive at 7.5-28%. How- ever, a rapid salinity change of 15% within this range was lethal. Ensis, from nearly oceanic salinities, sur- vived direct transfer to experimental salinities of 17.5 and 12.5% in the 2 experiments conducted with this species. However, mortality was heavy below 20 TABLE 23. Response of Ensis directus Conrad to different salinities. Salinity at collection site 32%o. % Surviving Salinity After After %o direct transfer acclimation 0 0 2.5 0 0 5.0 0 80.9 7.5 0 95.3 10.0 0 98.4 12:5 5.0 100 15.0 20.0 100 178 50.0 100 20.0 95.0 98.2 22:9 95.0 100 25.0 95.0 100 27.5 90.0 30.0 95.0 80 CASTAGNA AND CHANLEY and 17.5% for the 2 experiments (Table 23). Clams were acclimated to survive, at least for brief periods, at salinities as low as 5%. All clams survived direct transfer from 12.5 to 30% but transfers from 10%o and lower to 30% were lethal. All surviving clams burrowed normally at salinities of 5%o and higher. Some clams burrowed at 2.5% but eventually died. Filtering was slightly reduced below 10% but otherwise was normal wherever clams survived. Solen viridis Say (Tables 1,2) The green razor clam is fairly common in shallow water sand flats from Rhode Island to Florida and in the Gulf states. In Virginia it is found infrequently in sand bars of the barrier islands and therefore only in high-salinity water. Solen viridis are comparatively rare in Virginia and enough were found for only | experiment. Unfortunately, they survived poorly in the laboratory and the experiment had to be terminated after 8 days. At this time it seemed likely that direct transfers from 33-34% to experi- mental salinities of 17.5 to 20%o could be tolerated. Clams were very active and some burrowed immediately after transfer to all salinities, including fresh water. Family Mactridae Spisula solidissima (Dillwyn) (Tables 1,2,24) The surf clam, or skimmer, is abundant from Nova Scotia to Florida and from Florida to Texas. Under natural conditions it is not found below 28% but may be able to tolerate much lower salinities. Welch (unpublished manuscript) found the minimum lethal limit between 15 and 20%. He further stated that eggs of this species do not develop at 22% or lower, but larvae survive and grow at 16%. Schechter (1956) places the minimum tolerance of both eggs and sperm of Spisula solidissima at “40% sea water” or about 15%. Eggs in the “polar-body stage, however, disintegrated at this salinity. Some surf clams survived direct transfer to all salinities from 15-30% (Table 24). Mortality was heavy at 15%, however, and in the 2nd experiment clams failed to survive when transferred to this salinity. TABLE 24. Response of Spisula solidissima (Dillwyn) to different salinities. Salinity at collection sites 32-34 %o. % Surviving Average highest % burrowing Feeding (0= попе, R= reduced, N=normal) Salinity After After After After After After % direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 О 2.5 0 0 O 5.0 0 0 O 1.0 0 0 0 60.0 O O 10.0 0 80.3 0 100 О В 12:5 0 96.0 0 100 В М 15.0 25.0 98.4 100 100 К М 5 76.8 100 100 100 N N 20.0 68.9 98.9 100 100 N N 22.0 86.4 100 100 100 N N 25.0 95.0 100 100 100 N N 225 97.5 98.2 N N 30.0 75.0 100 N N SALINITY TOLERANCE OF MARINE BIVALVES 81 Spisula solidissima failed to remain tightly closed at lethally low salinities and, con- sequently, died rapidly. After acclimation to intermediate salinities, the lower limits for survival were extended and 75% of the clams exposed to 10% survived. Over 90% of those exposed to 12.5% and higher survived. All clams transferred to 7.5% died. All surviving clams were transferred directly to 30%. Thirteen of the 16 moved from 10 to 30%o survived the change eventually readapted to that salini- ty. All clams transferred from 12.5%0 and higher survived and adapted to 30%0 within a few days. Burrowing was normal at all salinities at which clams survived, though at lower salinities there was often a period of adjustment before normal burrowing occurred. Some clams burrowed at 7.5%o before they died. Clams filtered in all containers in which they survived. Some limited filtering occurred at lethal salinities before clams died (12.5% after direct transfer and 7.5 %o after acclimation). Mulinia lateralis (Say) (Tables 1.2 95.96) This small clam is a common to abundant inhabitant of sandy substrata in shallow water from Maine to Texas. Parker (1960) lists it as occurring where salinity ranges from 18-80%. Ladd (1951) found few М. lateralis between 4 and 9%o but many from 10-40%. Nagabhushanam (1964) found that visceral ganglia of this species lose their secretory granules at low salinities. In Virginia, fluctuating populations of this species are common above 8% (Wass, 1965), but less common above 25%. Two samples of Mulinia lateralis, collected from an area where the salinity was between 16 and 17%o, survived direct transfer to experimental salinities from 5- 30%. Although mortality was heavy in 1 group at 5%, virtually no mortality oc- curred at higher salinities. When clams were transferred from environmental salinities of 20 and 24.6 %, the minimum TABLE 25. Response of Mulinia lateralis Say to different salinities. Salinity at collection sites 16.5, 16.9, 24.0 and 24.6 “bo. % Surviving Average highest % burrowing Feeding (0= попе, R= reduced, N=normal) Salinity After After After After After After %o direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 5.0 20.0 O O 29 0 65.5 WED 75.3 O R 5.0 30.0 87.8 32.5 100 R N то 60.0 92.0 66.1 100 В М 10.0 97.5 99.1 100 100 М М 119445) 100 98.9 100 100 N N 15.0 100 100 100 100 N N 170) 97.5 100 100 100 N N 20.0 100 100 100 100 N N 22.9 97.5 100 100 100 N N 25.0 100 100 100 100 N N 29 97.5 100 100 100 М М 30.0 100 100 100 100 М М 82 CASTAGNA AND CHANLEY TABLE 26. Survival of Mulinia lateralis after direct transfer between the extreme experimental salinities to which they had become acclimated. Transferred from Transferred to Number transferred Number surviving (Salinity in %o ) (Salinity in %o ) 2.5 30.0 20 0 5.0 30.0 2 0 7.5 30.0 18 9 10.0 30.0 10 6 12.5 30.0 10 1 30.0 12.5 10 10 30.0 10.0 18 18 30.0 7.5 40 37 30.0 5.0 19 7 30.0 2.5 20 0 salinities at which they survived were 7.5 and 10%, respectively. After acclimation at intermediate salinities, most clams survived at 5%. Clams from low-salinity areas survived at 2.5%, a salinity lethal to Mulinia lateralis from the 2 high-salinity areas even after acclimation at intermediate salinities (Table 25). No clams survived in fresh water. Clams © surviving at 2.5 and 5.0% were killed when trans- ferred directly to 30% (Table 26). Although all clams died in a reciprocal transfer from 30 to 2.5%0, over 1/3 sur- vived transfer from 30 to 5%. Fifty per- cent survived transfer from 7.5 to 30%o but over 90% survived the reciprocal transfer. Appreciable mortality occurred even when clams were transferred from 10 and 12.5%0 to 30%o, but no clams died when transfers were made from 30 to either 10 ог 12.5%o. Some clams burrowed after direct trans- fer to all salinities including fresh water. The number burrowing was not normal, however, at salinities that were eventually lethal. Clams filtered algae from the water at all salinities at which they survived. Rangia cuneata (Gray) (Tables 1,227) Rangia cuneata is a common species in fresh to brackish water along the coast from Maryland to Texas (Pfitzenmeyer & Drobeck, 1964). In Virginia it is common in low-salinity areas of Back Bay and the James River (Wass, 1965). Parker (1960) found R. cuneata in fresh water and in areas where salinity did not exceed 10%. Ladd (1951) noted it as abundant where salinity ranged from 4-9 % but scarce from 13-25%. Parker (1965) observed that Rangia were found in Texas only where the average annual salinity was less than 18%. Well-established populations were studied in Lake Pontchartrain where salinity varied from 1.5-9.8% annually (Fairbanks, 1963). Godwin (1967) reported finding Rangia in Georgia at salinities from 2.5-11.5%o, with commerical concen- trations at 3.5-4.5%o. Gunter (1961) noted that larger Rangia seemed to be found in areas where salinity was lower. Pfitzenmeyer & Drobeck (1964) observed the same phenomenon in Potomac River populations where they found Rangia at salinities from 5.7-11.8%o. In the laboratory, Allen (1961) was able to keep Rangia alive at several salinities from fresh water to 25%. He noted that the concentrations of amino acids in- creased with salinity to 17% but decreased with further salinity increase. Rangia cuneata were collected from salinities of about 5% and transferred directly to experimental salinities. In l experiment mortality was high after direct transfer to 22.5% and higher. In the second experiment only 1 clam sur- vived at salinities of 20% and higher and SALINITY TOLERANCE OF MARINE BIVALVES 83 TABLE 27. Response of Rangia cuneata (Gray) to different salinities. Salinity at collection site about 5%o. % Surviving Salinity After After %o direct acclimation transfer 0 50.0 100 2.5 100 5.0 100 7.5 100 10.0 100 100 1225 100 100 15.0 97.5 100 1723 82.5 100 20.0 47.5 100 2975 15.0 100 25.0 29.5 100 275 2.5 100 30.0 0 100 Highest % burrowing After After direct acclimation transfer 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 100 0 100 several died even at 17.5%. All clams survived direct transfer to fresh water in the lst experiment while a similar transfer was fatal to all clams in the 2nd experi- ment. These results are summarized in Table 27. After acclimation at intermediate salin- ities, Rangia cuneata survived at all experi- mental salinities including fresh water and 30%. At the conclusion of the experiments surviving clams were moved from 30% to 5%0 without mortality. All Rangia cuneata dug in and filtered normally at all experimental salinities at which they survived. Family Myacidae Mya arenaria (L. ) The commerically important soft clam is found from Labrador to North Carolina. It is known to be a euryhaline form and has been found at salinities from 6.3-32.4% (Belding, 1930; Kellogg, 1901). Pfitzenmeyer & Drobeck (1963) found it at salinities as low as 3%. In Virginia, soft clams are abundant above 10% in Chesapeake Bay and its tributaries (Wass, 1965). They are also present but scarce in seaside bays where salinity may reach 35%. In the laboratory, soft clams from several different geographical areas had different minimum salinities at which they survived but all could be acclimated to survive at 2.5%o (Chanley, 1958). Stickney (1964) found that about 1% of Mya eggs developed to normal straight hinge larvae at 8%o. Larvae grew fairly well at 10%o but optimum salinities were higher. Salinity requirements of eggs and larvae were determined by the environment of the adult. Family Pholadidae Barnea truncata (Say) (Tables 1,2,28) This species occurs from Maine to Florida and is common from Massachu- setts south in clay, soft rock or wood (Turner, 1956). In Virginia it is commonly found in peat (Wass, 1965) from 16-35%. Some Barnea survived direct transfer from 30-34% to 12.5% and 15% but mortality was greater than after transfer to salinities above 15% (Table 28). All clams transferred to salinities of 10%o and lower died. After acclimation at inter- 84 CASTAGNA AND CHANLEY TABLE 28. Response of Barnea truncata (Say) to different salinities. Salinity at collection site 33- 35 %o . % Surviving Feeding (0=none, R= reduced, N=normal) Salinits After After After After %o direct acclimation direct acclimation transfer transfer 0) 0) O 2.9 0 0 O R 0 0 42.1 O R То 0 73.8 O R 10.0 () TDA he O R [225 30.0 99.1 В М 15.0 67.5 100 R N 17.5 95.0 98.0 N N 20.0 90.0 94.5 N N 22:5 95.0 93.8 N N 29:0 92.5 97.4 N N 27.9 95.0 N 30.0 95.0 N "When clams that survived the direct transfer to 12.5 were moved to 10%, all died. Almost all 0 clams acclimated at other salinities survived when moved to 10%. mediate salinities, clams survived well at salinities down to 10%. Some clams sur- vived at 7.5 and 5.0% but the higher mortalities at these salinities suggest that they might eventually be lethal. Direct transfers of clams from 5, 7.5, and 10% to 30% killed all clams. Thirteen out of 24 clams survived the transfer from 12.5 to 30%, and 14 out of 19 clams survived transfer from 15 to 30%. Filtering was normal Нот 17.5-30%o after direct transfer. No filtering occurred at 10°%0 and lower and filtering was re- duced at 12.5 and 15%. After acclimation, filtering was only slightly reduced at 10%o and normal at higher salinities. Some filtering was observed at 2.5% but filtering was definitely reduced below 10%o. Barnea truncata are incapable of making new burrows as adults; consequently, observations on the effect of salinity on burrowing were not possible. Diplothyra smithii (Tryon) This species is found boring into shell and, rarely, wood from Massachusetts to Florida. It is common in the south but scarce from Virginia north. Menzel (1964) lists it as occurring at salinities above 25%o. Martesia cuneiformis (Say) Martesia cuneiformis can be found boring in wood from North Carolina southwards. It probably does not normally occur in Virginia (Turner, 1956). Menzel (1964) lists it at salinities above 25%o. Cyrtopleura costata (L.) (Tables 152,29) =, The angel wing is found in sand to soft, sticky mud from Massachusetts to Florida and Texas (Turner, 1956). Ladd (1951) reports it as occurring from 16-40 %. It is a common Virginia species in suitable substrata and is found where salinity is above 10% (Wass, 1965). Cyrtopleura costata survived direct transfer from about 20%o to salinities from 7.5-30 %. After acclimation in inter- mediate salinities, clams survived at SALINITY TOLERANCE OF MARINE BIVALVES 85 TABLE 29. Response of Cyrtopleura costata (L.) to different salinities. Animals were raised in the laboratory at a salinity about 20%. % Surviving Feeding (0= попе, R= reduced, N=normal) Salinity After After After After %o direct acclimation direct acclimation transfer transfer 0 0 0 O 2.5 0 0 O R 5.0 0 100 О В 7.0 100 100 R N 10.0 100 100 R N 12.5 100 100 R N 15.0 100 100 N N 17.5 100 100 N N 20.0 100 100 N N 22:5 100 100 N N 25.0 100 100 N N 27.5 100 100 N N 30.0 100 100 N N 2.5% for lengthy periods but eventually salinities. died and 5% was the minimum salinity Culliney (personal communication) in which clams survived. After direct transfer from 20%, the rate of filtering was reduced at 12.5% and lower. No clams filtered below 7.5%. When animals were acclimated in inter- mediate salinities, feeding was normal from 7.5-30% but reduced or absent at lower salinities. Cyrtopleura costata were incapable of digging new burrows, so no observations on the influence of salinity in burrowing were possible. Family Teredinidae Bankia gouldi (Bartsch) This is a common east coast shipworm found from New Jersey to Florida. This species in plentiful in Chesapeake Bay but is scarce or absent in high- salinity oceanic water. Clark (1954) reports its minimum salinity as 10%. This agrees closely with the observations of Scheltema & Truitt (1954) who found that larval B. gouldi set on test panels at salinities from 9-30%. Within this range, fewer shipworms were found at lower reports that Bankia gouldi larvae survive but are “barely growing” in a constant salinity of 10%o. Teredo navalis L. Teredo navalis has a world wide dis- tribution and is considered euryhaline. It is the common shipworm at oceanic salinities but rare in Chesapeake Bay. The salinity tolerance of this species is fairly constant throughout its range and the minimum salinity for survival has been listed as 5, 6, 7, and 8% (Blum, 1922; Miller, 1926; Clark, 1954; Kudinova- Pasternak, 1960; Soldatova, 1961). These observations were made over a geographic range from San Francisco to the Black Sea and over a period of nearly 40 years, yet they differ by only 3%. These same authors report an optimum salinity of 12- 25 or 28% for survival of T. navalis. Blum (1928) found that activity of T. navalis was reduced when salinity was below 7.5% but that they could survive at 4%o for a month. However, shipworms eventually died when kept at 4%. M'Conigle (1927) found activity reduced 86 CASTAGNA AND CHANLEY at 13% and entirely stopped at 10%. Both he and Soldatova (1961) reported that 40%o is the upper lethal salinity. The minimum salinity for larval devel- opment has been reported as 9% (Miller, 1926) and 12% (Kudinova- Pasternak, 1962). M Conigle (1927) found some development at 7.5% but lists this as an “unfavorable” salinity. Culliney (personal communication) reports that larval T. navalis were reared to the pediveliger stage at a constant salinity of 7.5%. Growth, however, was very slow. Family Lyonsiidae Lyonsia hyalina (Conrad) (Tables 1,2,30) Lyonsia hyalina Conrad is common in shallow water in sandy substrata from Nova Scotia to Florida. In Virginia it is found at salinities above 15% (Wass, 1965) and in Florida above 25 % (Menzel, 1964). Lyonsia hyalina were available for only l experiment. When transferred directly from 20% to experimental salinities, survival was good at salinities from 12.5-30% (Table 30). Four out of 10 sur- vived at 10%. Salinities lower than 10% were lethal. Clams could be acclimated to 7.5% but all died when transferred to 5.0%. Clams began dying from unknown causes before further transfers could be made and the experiment was discon- tinued. Lyonsia hyalina burrowed actively at all salinities at which they survived. A limited amount of filtering was observed at 5%o though these clams eventually died. Filtering was also reduced at 10% after direct transfer and at 7.5% after acclima- tion to intermediate salinities. Clams filtered normally at all other salinities. DISCUSSION During the course of these experiments it became apparent that the minimum salinity tolerated by a species was variable. Acclimation at intermediate salinities usually extended tolerance limits. However, after acclimation, the minimum salinity in which a species survived sometimes varied from 2.5-5% between replicate experiments. Some species collected from the same location at com- TABLE 30. Response of Lyonsia hyalina Conrad to different salinities. Salinity at collection site 20%00. % Surviving Average highest Feeding (0=none, R= % burrowing reduced, N=normal) Salinity After After After After After After %60 direct acclimation direct acclimation direct acclimation transfer transfer transfer 0 0 0 O 20 0 0 O 5.0 0 0 0 0 O R 139 0 100 0 100 O R 10.0 40.0 100 100 100 R N 12:5 90.0 100 100 100 N N 15.0 90.0 100 100 100 N N 17:5 100 100 N 20.0 100 100 N 22.5 100 100 N 25.0 90.0 90.0 100 100 N N DO 100 89.9 100 100 N N 30.0 80.0 100 100 100 N N SALINITY TOLERANCE OF MARINE BIVALVES 87 parable temperatures and salinities but in different months had different minimum tolerance limits, indicating a seasonal variability in salinity tolerance. This difference was not related to reproductive condition or to the appearance of the animals tissues. Occasionally, minor differences could be attributed to the different temperatures at which experiments were conducted. However, in most cases, the temperature primarily affected the rate of response to experimental salinities rather than changing the tolerance limits. For example, burrowing, filtering or mortality usually occurred more rapidly at higher temperatures, but the salinities at which these occurred were about the same regardless of temperature. In some cases, salinity at the time of collection appeared to influence the range of salinity to which bivalves could adapt. Animals collected when salinity was low sometimes had higher tolerances at minimum salinities than those of the same species collected from high salinity waters. This difference persisted even after laboratory acclimation at intermediate salinities. Perhaps longer and more gradual acclimation in the laboratory would have eventually eliminated this difference. Some species such as Solemya velum, Solen viridis and Tagelus plebeius were not adaptable to laboratory conditions and their vital activities were reduced or mortalities increased as experiments Q progressed. These 3 species required a relatively deep substratum for burrowing and apparently a different food (ie., detritus) than the type used. Occasionally, unusually high mortality not associated with salinity appeared in some experi- mental containers but not in others. These mortalities occurred at all salinities and the causative agents apparently did not necessarily exert a synergistic effect at marginal salinities. On the other hand, after exposure to several different experi- mental salinities, some bivalves were capable of surviving more rapid changes in salinity than was possible immediately after collection. In effect, they had become ‘acclimated,’ and hence more resistant to physiological stress from salin- ity changes. Differences in tolerance limits of the same species collected from different localities for this series of experiments most likely reflect seasonal differences in temperature, salinity and other environmental influences and probably are not due to the occurrence of physiolog- ically different races. When bivalves survived in a given salinity, their activities were generally normal, except for some arcids and mytilids which apparently require higher salinities for byssus formation than for other activities. Active species did burrow and filter immediately after being moved to salinities that eventually proved lethal. However, there were no salinities at which animals survived but did not burrow or TABLE 31. Comparison of the minimum salinity necessary for survival of adults and for survival of larvae or reproduction. Approximate minimum salinity in %o Species at which adult survives Bankia gouldi 10 Crassostrea virginica 6 Gemma gemma 10 Mercenaria mercenaria 12.5 Mulinia lateralis 5 Mya arenaria 2.5 Mytilus edulis 8 Spisula solidissima 1255 Teredo navalis 6 Minimum salinity in %o at which larvae survive or reproduction occurs 10 5.6 10 15 Who 8 or lower 14 16 1.9 88 CASTAGNA AND CHANLEY filter. There appears to be little difference in the minimum salinity for survival of adult bivalves and the minimum salinity for reproduction and larval development (Table 31). Data are available for only a few species but in only 1 case did the salinity tolerance limits for survival of adults or larvae and occurrence of reproduction differ by a maximum of 6%. Small bivalves frequently succumbed more rapidly to lethal salinities than did larger individuals of the same species but there was no difference in the minimum salinity at which they would survive. Small bivalves adapted better to experimental conditions within their individual salinity tolerance range than the larger in- dividuals. This could be due to the stress of overcrowding or increased metabolic waste accumulation in the larger specimens. From the preceding discussion, it is evident that the minimum salinity for TABLE 32. Salinity tolerance limits of 36 species of bivalves as determined from natural distribu- tion and laboratory experiments. Species Salinity range Experimentally determined in nature in%o minimum salinity in %o Argopecten irradians Above 15 15 Amygdalum papyria Above 10 7.5 Anadara ovalis Above 15 12:5 Anadara transversa Above 15 10 Anomia simplex Above 15 12.5 Bankia gouldi Above 10 => Barnea truncata Above 15 10 Brachidontes recurvus Above 5 4 Congeria leucophaeta Below 12 0 Crassostrea virginica Above 6 5 Cyrtopleura costata Above 10 5 Donax variabilis Above 30 12.5 Ensis directus Above 10 7.5 Gemma gemma Above 5 7.5 Laevicardium mortoni Above 15 7.5 Lucina multilineata Above 20 7.5 Lyonsia hyalina Above 15 7.5 Macoma balthica Above 5 2.5 Macoma phenax 2-20 2.5 Macoma tenta 20-30 a Mercenaria mercenaria Above 12.5 12.5 Modiolus demissus Above 8 5 Mulinia lateralis Above 10 5 Mya arenaria Above 3 20 Mytilus edulis Above 8 == Noetia ponderosa Above 20 17.5 Nucula proxima Above 20 == Petricola pholadiformis Above 15 10 Polymesoda carolininana Below 15 —— Rangia cuneata Below 15 0 Solemya velum Above 15 15 Spisula solidissima Above 28 12.5 Tagelus plebeius Above 10 2.5 Tellina agilis Above 18 12.5 Teredo navalis Above 6 —— Yoldia limatula Above 20 —— E all | SS: a Il 7 7 7 _ те = = UT 3 so 2555058 Bethe oy Jo нию ме N a CO OS, o. 22-5 E< =. о Te) nd on | oO oe a Wer ce oy tan Le № 7 7 _ _ MWC _ Y _ $3153а$ 30 H38WNN 7 90 CASTAGNA AND CHANLEY oceanic salinities. D. variabilis, though living on ocean beaches, undoubtedly experiences some temporary reductions in salinity after heavy rains. Juvenile S. solidissima are frequently found on ocean beaches and in estuarine waters but are found as adults only in deeper waters. In recent laboratory experiments juvenile Chama congregata, a species normally found only in oceanic water and not normally exposed to salinity reductions, were also discovered to be euryhaline. About 2/3 of the bivalves which occur in Virginia's estuarine and inshore environment occur naturally over the approximate salinity range they tolerated in the laboratory (Table 32). This would indicate ihat salinity is of prime importance in determining their distribu- tion. In Virginian waters, Mytilus edulis, Argopecten irradians, Macoma balthica and Mya arenaria are not commonly found over their entire salinity range though they are in other areas. Virginia is near the southern limit of the geographical range for both Mytilus edulis and Mya arenaria. As mentioned previously, summer water temperatures limit the distribution of Mytilus edulis to oceanic waters. Mya arenaria does not appear to be confined to low-salinity water by temperature. However, the unknown factor or factors which determine the southern range limit of Mya arenaria may serve to limit this species to intermediate and low-salinity areas within the coastal waters of Virginia. The bay scallop, Argopecten irradians is rare, and is restricted in Virginia to high-salinity water. Because this species is abundant both north and south of Virginia in a wider range of salinity, its distribu- tion along the coast of the state must be limited by other factors, for example, absence of suitable setting substratum or protective cover, formerly provided in the area by the extensive eel grass beds. Scallops were much more abundant prior to the disappearance of eel grass (Zostera marina) in the early 1930's. The absence of suitable habitat in the eastern shore bays may prevent scallop populations from recolonizing those areas of Chesapeake Bay where salinity is above 15%o and eel grass, Rupia, or other suitable marine grass is established. In Virginia Macoma balthica is limited to low and intermediate salinity creeks with soft muddy substrata. This clam is found at higher salinities and in different substrata elsewhere. Biological competition for suitable habitats with 3 other tellinids (M. mitchelli, M. tenta, and Tellina agilis) may account for its distribu- tion in Virginia. About 1/3 of the species studied have never been found naturally over the entire salinity range tolerated in the laboratory. Predation could cause this or perhaps this reflects a lack of adequate sampling in the cases of Tagelus plebeius, Laevicar- dium топот, Lyonsia hyalina, Barnea truncata, and Lucina multilineata. In other cases (Congeria leucophaeta, Rangia cuneata, Масота mitchelli, Donax variabilis, Тейта agilis, and Spisula solidissima), there can be no doubt that salinity is, by itself, not a major impor- tance in limiting distribution. In almost every instance, these species live in marginal habitats where species diversity, and therefore interspecific competition, is low. Congeria leucophaeta, Rangia cuneata and Macoma mitchelli are pri- marily brackish water forms that thrive at salinities too low for most marine bivalves and too high for fresh water bivalves. Donax variabilis inhabits the surf zone of ocean beaches where few other species of animals can survive. Tellina agilis and Spisula solidissima, though not living in unique habitats, may not inhabit their potential salinity range because of biological interaction such as predation or competition from other species, or special environmental requirements (i.e., high oxygen, low levels of suspended sediments, bottom type, etc. ). Tellina agilis and Macoma mitchelli are closely related species, virtually indistin- guishable except for their hinge structure. Both exhibited a wide salinity range in the laboratory (2.5-30%0) yet there is very little overlap in their distributions. М. mitchelli is found from 2-20% and T. agilis from 18-34% (Table 32). It again SALINITY TOLERANCE OF MARINE BIVALVES 91 appears that some other environmental requirement determines their distribution. Spisula solidissima is adapted to the relatively stable oceanic environment which supports tremendous beds of this species. However, when larvae colonize inshore areas they rarely develop beyond the juvenile stage because they are subject to intense predation by a variety of crabs, carnivorous gastropods and bottom feeding fish. This predation rather than salinity prevents establish- ment of permanent populations of S. solidissima in estuarine areas. The relationship, if any, between salin- ity tolerance and systematic position is not at all clear. In some taxonomic groups of closely related species, the separate species do not occur over the entire salinity range which the species can tolerate under experimental conditions. This could be due to interspecific competi- tion. Within the Mytilidae and Pholadidae, the species are separated by other environmental factors. For example, in the Mytilidae, Brachidontes recurvus is epibenthic and subtidal, Amygdalum papyria benthic intertidally and in shallow water. Modiolus demissus occurs high in the intertidal zone. 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WASS, M.L., 1965, Checklist of the marine invertebrates of Virginia. Spec. Sci. Rept. No. 24, 3rd rev., Va. Inst. Mar. Sci. 55 р. WELCH, W., The Atlantic coast surf clam. Unpublished manuscript. WELLS, H.W., 1961, The fauna of oyster beds with special reference to the salinity factor. Ecol. Monogr., 31: 239-266. WELLS, H.W. & GRAY, LE., 1960, Seasonal occurrence of Mytilus edulis on the Carolina coast as a result of transport around Cape Hatteras. Biol. Bull., 119: 550-559. ZUSAMMENFASSUNG SALZGEHALT-TOLERANZ EINIGER MEERESMUSCHELN VON LANDNAHEN UND ASTUAR-BIOTOPEN IN DEN GEWASSERN VON VIRGINIA AN DER WESTKUSTE DES MITTELATLANTIK M. Castagna und P. Chanley Viele Arten Brackwasser-Muscheln haben eine Verbreitung, die eng mit dem Salzgehalt zusammenhangt, was die Wichtigkeit des Salzgehaltes fiir die Verbreitung zeigt. Die ungefáhre Amplitude der Salzgehalt-Toleranz fiir 36 Arten wird dargestellt. Die Toleranz-grenzen fiir 29 Arten wurden im Laboratorium experimentell bestimmt. Die meisten davon sind stark euryhalin. Alle blieben noch bei einem Mindest-Salzgehalt von 17.5% am Leben, und 25 Arten noch bei 12.5%. Zwanzig Arten ertrugen noch niedrigeren Salzgehalt. Die Salzgehalt-Toleranz fiir ein und dieselbe Art ist nicht konstant sondern variiert mit der Jahreszeit, der Gewóhnung, der Temperatur. Eingraben, Nahrungsaufnahe und Vermehrung finden bei fast jedem Salzgehalt statt, bei dem die Art am Leben bleibt. Byssusbildung erfordert einen hóheren Salzgehalt, als er ftir andere Tatigkeiten nótig ist. In Virginia kónnen etwa zwei Drittel der besprochenen Salzwasser-muscheln in dem gesamten Salzgehaltis-Bereich gefunden werden, in dem sie im Laboratorium úberlebt haben. Elf Arten kommen nicht in ihrem gesamten móglichen Salzgehalt-Bereich vor. Acht davon, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina mul- tilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis sind nahe der geographischen Grenze ihres Verbreitungsgebietes; ihre Verteilung kann lokal in erster Linie durch die Faktoren bestimmt sein, die ihre geographische Verbreitung bedingen. Die Verbreitung von 5 Arten, Argopecten irradians, Congeria leucophaeta, Macoma mitchelli, Donax variabilis und Spisula solidissima kann durch Feinde, Konkurrenz oder besondere ökologische Ansprüche beeinflusst werden. Vier von den 11 SALINITY TOLERANCE OF MARINE BIVALVES Arten, Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata kommen an besonderen Biotopen mit geringer Arten-Mannigfaltigkeit vor. HZ RÉSUMÉ TOLÉRANCE A LA SALINITÉ DE QUELQUES BIVALVES MARINS DES MILIEUX LITTORAUX ET D'ESTUARIES EN VIRGINIE, CÔTE OUEST MEDIO-ATLANTIQUE M. Castagna et P. Chanley Plusieurs bivalves d estuaires ont un type de distribution en corrélation avec la salinité, ce qui montre l'importance de celle-ci dans le déterminisme de leur distribution. Le niveau approximatif de tolérance saline pour 36 espèces de bivalves est décrit. La plupart de ces espèces montre un remarquable degré d'euryhalinité. Toutes survivent à une salinité minimale de 17,5% et 25 espèces survivent à 12,5 % . Vingt espèces survivent à diverses salinités plus faibles. La tolérance saline pour une espèce donnée n'est pas constante, mais varie en fonction de la saison, du mode expérimental, de la température. Le fouissage, l'alimentation et la reproduction ont généralement lieu à presque toutes les salinités où la survie est possible. La formation du byssus réclame une salinité plus forte que celle nécessaire aux autres activités. En Virginie, environ les 2/3 des espèces de bivalves étudiées peuvent être trouvées dans les limites de salinité qu'elles peuvent tolérer au laboratoire. Onze espèces ne se rencontrent pas jusqu'aux limites qu elles sont capables de supporter au laboratoire. Huit de ces 11 espèces, Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis, sont proches de leurs limites de répartition géographique. Leur distribution localement peut étre d abord limitée par les facteurs qui déterminent leur répartition géographique. La distribution de 5 especes, Argopecten irradians, Congeria leucophaeta, Macoma mitchelli, Donax variabilis, et Spisula solidissima, peut &tre influencée par la prédation, la compétition et des exigences spéciales d'environnement. Quatre de ces 11 espéces, Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata, se rencon- trent dans des habitats spéciaux de faible diversité spécifique. AE RESUMEN TOLERANCIA DE SALINIDAD EN BIVALVOS MARINOS DE AGUAS COSTERAS Y AMBIENTES ESTUARINOS DE VIRGINIA M. Castagna y P. Chanley Muchas especies de bivalvos marinos tienen su distribución correlacionada a la salinidad, indicando la importancia de tal factor en los patrones distribucionales. Se estudiaron los limites de tolerancia en 36 especies; 29 fueron determinadas por experimentos de laboratorio. La mayoría muestran marcada eurihalinidad. Todas sobrevivieron a una salinidad minima de 17.5% y 25 а tan poca como 12.5% ; 20 sobrevivieron a concentraciones varias, menores. La tolerancia de una especie dada no es constante sino que varia con la estación y la temperatura. Excavamiento, nutrición y reproducción ocurren a grado de salinidad en el que puedan sobrevivir, pero para la formación de biso requieren salinidades más altas. En Virginia, dos terceras partes de los bivalvos discutidos se pueden encontrar entre los límites de salinidad que son capaces de resistir en el laboratorio. Once especies no aparecen en todos sus límites potenciales y ocho de las mismas, Yoldia limatula, Mytilus 95 96 CASTAGNA AND CHANLEY edulis, Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis, estan cerca del límite geográfico de tolerancia; sus distribuciones locales peuden ser limitadas, primariamente por los factores que deter- minan sus áreas geográficas. La distribución de cinco especies, Argopecten irradians, Congeria eucophaeta, Macoma mitchelli, Donax variabilis, y Spisula solidissima, pueden estar influenciadas por predación. Cuatro de las once especies, Congeria leucophaeta, Macoma mitchelli, Donax variabilis y Rangia cuneata, aparecen en habitats es- pecializados con diversidad de bajas salinidades. ИТР: АБСТРАКТ ВЫНОСЛИВОСТЬ ПО ОТНОШЕНИК К СОЛЕНОСТИ НЕКОТОРЫХ МОРСКИХ BIVALVIA ИЗ ПРИБРЕЖНОЙ ЗОНЫ И ЭСТУАРИЕВ ВИРГИНИИ (ЗАПАЛНО-АТЛАНТИЧЕСКОЕ ПОБЕРЕЖЬЕ) М. КАСТАНЬЯ И П. ЧЕНЛИ Особенности распределения ряда видов Bivalvia тесно связано € распределением солености и имеет для них большое значение. Описываются пределы выносливости различной солености 36 видов Bivalvia. ina 29 видов эти пределы были определены экспериментально. Большая часть изученных видов оказались очень оэвригалинными. Все моллюски выживали при наименьшей солености в 17.5°/oo, а 25 видов - при 12.507685; 20 видов выживали при различной, HO еще более низкой солености. Выносливость к солености данного вида не постоянна, а изменяется по сезонам, при опытах с соленостью и в зависимости от температуры. Закапывание, питание и размножение моллюсков обычно происходит почти при всякой солености, при которой только они могут выживать. Образование биссуса требует более высокой солености, чем другие виды елеятельности. В районе Виргинии около 2/3 исследованных морских двустворчатых моллюсков могут встречаться и при более высокой солености, чем та, которую они выносили в лаборатории. 11 видов не встречаются при солености, более высокой, чем та, которую они потенциально могут выдерживать. Восемь видов из одиннадцати - Yoldia limatula, Mytilus edulis, Venericardia tridentata, Lucina multilineata, Dosinia discus, Abra aequalis, Mya arenaria, Martesia cuneiformis находятся здесь почти на границе своего. географического распространения. Их местная встречаемость может ограничиваться прежде всего теми факторами, которые определяют их общее географическое распространение. На распространение пяти видов - Aequipecten irradians, Congeria leucophaeta, Масота mitchelli, Donax variabilis, Spisula solidissima могут влиять - хищники, кокуренция или особые потребности моллюсков в условиях обитания. Четыре из одиннадцати видов - Congeria leucophaeta, Macoma mitchelli, Donax variabilis, Rangia cuneata - встречаются в особых условиях обитания и при малом их видовом разнообразии. Z.A.F. MALACOLOGIA, 1973, 12(1): 97-113 EFFECTS OF POTASSIUM ON SURVIVAL AND DISTRIBUTION OF FRESHWATER MUSSELS Marc J. Imlay United States Environmental Protection Agency National Water Quality Laboratory 6201 Congdon Boulevard Duluth, Minnesota 55804, U.S.A. ABSTRACT 1. In the laboratory potassium ions were lethal to 4 species of freshwater mussels. Eleven ppm K was lethal to 90% of Actinonaias carinata, Lampsilis radiata siliquoidea, and Fusconaia flava in 36-52 days of exposure, and 7 ppm K was fatal to the latter 2 species in about 8 months. Amblema plicata was almost as sensitive as the other species. Similar K ion concentrations occur naturally in many North American rivers. 2. On the basis of National Water Quality Network data on potassium concentrations and the concentrations lethal to mussels in the laboratory, it was predicted that certain rivers would not have mussels and others would. Known distribution of mussels was generally correlated with the predicted locations. In 1 study the 6 rivers with more than 7 ppm K were not reported to have mussels. Mussels were reported from 28 of 39 rivers with less than 4 ppm K but from only 2 out of 10 rivers with 4-7 ppm K. 3. On the basis of the laboratory and field data, the predicted maximum safe level for the continued existence of most freshwater mussels is 4-10 ppm potassium. It is recommended that the concentration of potassium not be allowed to increase in mussel producing rivers if the concentration is above 4 ppm. INTRODUCTION This investigation owes its origin to the observation by Koshtoyants & Salanki (1958) that addition of KC1 to produce a dissolved potassium ion concentration of 10-*M (39 ppm) exceedingly altered the “daily activity pattern” of the freshwater mussel, Anodonta cygnea (Linnaeus) (Unionidae: Anodontinae)', and by the knowledge that this concentration was not much greater than that found in some rivers. Although mortality of A. cygnea was not reported, the exposures were for only about 1 week, and thus it was pos- sible that longer exposures at lower con- centrations would be lethal to these mussels. Ellis, Merrick & Ellis (1931) studied the effect of potassium on fresh- water mussels but only at concentrations of 0.1% KCI or more. The purpose of the present investigation was to study the pos- sibility that potassium at concentrations found in some rivers was lethal to North American mussels. These are rapidly dwindling in numbers [according to Stansbery (1970) at least 8 species have recently become extinct because of Man's activities], and have considerable commer- cial importance (Neel & Allen, 1964; Lopinot, 1967; Isom, 1969). MATERIALS AND METHODS A preliminary exposure of mussels to about 30 ppm potassium and a 2nd ex- posure to about 9 ppm potassium were conducted in order to yield a preliminary indication of the toxic concentrations of potassium. Two more experiments fol- lowed each with 4-5 concentrations and a control. Testing apparatus The testing apparatus was effectively the same in all the experiments and will be described only for the Ist experiment. There was a flow of fresh water con- 'The normal active phase lasted 50-100 hours and the rest phase 5-15 hours but after potassium addition both phases were 3-5 hours. 98 M. J. IMLAY == = = SS ST — — — STAINLESS HYPODERMIC NEEDLE FIG. 1. Potassium toxicity testing apparatus. taining a constant concentration of potas- sium into the test chamber. A 20 liter stainless steel chamber contained the test animals and received 1.0 liter of the test water at regular (52.5-56.1 min.) in- tervals. This interrupted flow was ob- tained by first directing water into a liter flask which emptied about hourly upon filling to the level of a siphon tube (Fig. 1). As the water passed down a tygon tube towards the experimental chamber it received a precise aliquot of prepared highly concentrated KCI solution through a capillary tube because of the venturi effect. Daily measurements of the volume of highly concentrated KCI solution re- moved were used to calculate the actual diluted concentration in the testing chamber. The potassium ion concentration ranged between 24.4 ppm and 34.4 ppm (x=30.1 il SNA] — — —THICK WALLED CAPILLARY TUBE — —UNDILUTED KCL SOLUTION — CONSTANT LEVEL KCL SOLUTION CLAM IN TEST CHAMBER ppm). The concentration in the 2nd ex- periment was held at about 9 ppm. This calculated concentration was verified on 2 occasions by the colorimetric method as detailed in Standard Methods for the Ex- amination of Water and Waste Water (cf. Anonymous, 1967: 240-242). The measurements were 9.65 ppm and 8.85 ppm. For the final experiments the cal- culated potassium ion concentration was verified throughout each experiments duration by the flame emission method on 4-5 day composite samples of water from the testing chambers. Table 1 shows the mean flame emission concentrations as well as the range (highest and lowest measured values). The daily calculated concentrations were close to the flame emission composite averages. Note the low potassium concentration in untreated POTASSIUM! TOXICITY TO MUSSELS 99 TABLE 1. Water qualities present in the 3rd and 4th experiments on KCI toxicity. Third experiment (December 19, 1968-January 25, 1969) Potassium flame emission concentration (ppm) Mean: DM 99 Rane: 54.0-60.8 32.5-36.4 Water introduced per hour (liters ) DT 927 Illumination (foot candles) 22 22 Velocity of water current (feet per second) 0.20 0.20 Qt I Qt pH (January 2) l 24 15 11 (control) 223-250 13.8-15.8 9.9-12.4 0.8-1.0 2.4 DM 2.6 1.9 21 22 19 16 0.20 0.14 0.11 0.20 7.5 Te) ia fs) Fourth experiment (July 14, 1969-May 14, 1970) Potassium flame emission concentration (ppm) Mean: 57 Range: 47-70 Water introduced per hour (liters) 6.9 Ilumination (foot candles) 22 (control) test water. Collection and handling of animals Three- to six-inch Amblema plicata (Say), Lampsilis radiata siliquoidea (Barnes), Actinonaias carinata (Barnes), Lampsilis ovata ventricosa (Barnes), and Fusconaia flava (Rafinesque) were chosen as test species for 2 reasons. They belong to the clam harvester s commercial 3 ridge, mucket, pocketbook, and pigtoe forms respectively (Горшо 1967). Secondly, they were collected from local rivers having a calcium content that was analysed and found to be at most 20% greater than that of the laboratory test water (described under “test conditions’) of 13.5-13.7 ppm. This small difference minimized calcium content, a major con- stituent of mollusks, as а difference 37 11 Yi 1 36.3-38.4 9.7-11.9 5.5-8.2 0.5-1.1 4.9 5.6 5.5 4.0 22 22 19 16 between natural and test water. Amblema plicata is known also as Amblema costata Rafinesque or Crenodonta costata (Rafinesque), and Actinonaias carinata as Actinonaias ligamentina (Lamarck). For the Ist experiment, 17 mussels were collected in November 1967 from the Eau Claire and St. Croix Rivers, Wisconsin, and maintained at 10-12° C and 5-5.5 ppm dissolved oxygen until testing which began on January 28, 1968. These included 4 Lampsilis radiata siliquoidea, 4 Lampsilis ovata ventricosa, 8 Fusconaia flava, and 1 Amblema plicata. For the 2nd experiment 8 Lampsilis radiata siliquoidea, 9 Lamp- silis ovata ventricosa, and 6 Fusconaia flava were collected from the Eau Claire River and held at 5% C and saturated dis- solved oxygen until testing began about 2 weeks later, on April 7, 1968. Specimens of these species from the collection sites on 100 M. J. IMLAY the St. Croix and Eau Claire Rivers were identified by Dr. Henry van der Schalie. For the 3rd experiment each of 6 testing chambers received 10 Actinonaias carin- ata on December 11, 1968. Almost all of these animals were from collections of equal numbers made on October 28 and December 6 from Yellow River, Wis- consin, a few miles above the St. Croix River. However another collection of what was believed to be the same species from the Yellow River was identified by Dr. David Stansbery as containing about 33% Lampsilis radiata siliquoidea. He re- marked (pers. comm.) that “The Yellow River material was most interesting since the Lampsilis radiata luteola (Lamarck, 1819) (=siliquoidea Barnes, 1823) are so very similar in shell characters to the Actinonaias ligamentina (Lamarck, 1819) (=carinata Barnes, 1823) from the same site. Both species are members of the unionid subfamily Lampsilinae, but there was no way of knowing which specimens of each had been included in the experi- ment. However, the absence of any bimo- dality in the results makes this experiment usable. Amblema plicata was collected from Moose River, Minnesota, near the city of Sturgeon Lake, on November 25 and 27. The clams were maintained in water saturated with oxygen at about 10° C until testing (potassium was introduced on December 19). There were not enough Amblema plicata for 10 specimens рег testing chamber since ice cover prevented sufficient collecting; each chamber received only 8 or 9 Amblema plicata. Lampsilis radiata siliquoidea and Fusconaia flava were used for the 4th experiment. Ten mussels of each species per test concentration were collected from Ox Creek, Wisconsin (uppermost tributary of St. Croix River) on July 14, 1969, and exposure to potassium began the same day. Conditions at Ox Creek were potassium, 0.4 ppm; temperature, 28.4°C (19°C on July 10); alkalinity, 58 ppm; total hardness, 58 ppm; calcium, 15.6 ppm; and magnesium, 4.3 ppm. The exposure extended for over 300 days and the mussels were fed 1 gram of trout fry commercial feed per test chamber twice daily. No successful report for rearing mussels (other than glochidia) in the laboratory was found in the literature, although Florkin (1938) studied adult mussels of Anodonta cygnea in running tap water without nourishment for 22 months before the mussels succumbed. The mussels in the 3rd and 4th experi- ments were examined daily for mortality, and mussels with gaping valves which re- mained open after an attempt was made to close them by hand were considered dead. For uniformity among the tests at each potassium concentration, each testing chamber received 1 mussel from each of 10 size categories. Testing conditions Laboratory conditions of temperature, pH, etc., similar to those in natural con- ditions, were maintained satisfactorily for the well-being of the animals. Except for the 4th experiment which utilized un- treated water pumped directly to the lab- oratory from Lake Superior, the test water was Lake Superior city water dechlor- inated with carbon filters. In order to provide lighting similar to natural conditions, combined fluorescent (Durotest? optima FS) and incandescent illumination were used; photoperiod was automatically adjusted to the local (Duluth) conditions. Foot candles of illu- mination at the water surface for the final experiments are shown in Table 1. In the Ist experiment (Fig. 1), mixing in the test chamber was adequate because the water entered parallel to the channel of the ellipsoid tank at a high velocity. In the 2nd experiment, rotating paddle wheels provided a continuous current of 1 К/Т sec. Electrical stainless steel stirrers set obli- quely in each ellipsoid chamber in the 3rd and 4th experiments provided the flow Mention of commercial products does not constitute endorsement by the United States Environmental ‚ Protection Agency. POTASSIUM TOXICITY TO MUSSELS 101 571000105 4432111000000000000000000000000 = a a г "IDIOIO99'63/3:3:21 2:2 | O — < a = = uJ о pa O © 2400000976433332221 POTASSIUM 1510IOIOI0I0 9197761616 3 З2 22 111000000000000000000000 IATA A AIROAOFO10 "OOOO IO OOO | 0000000000000 OOOO A IS 7 7 7 7616616515515 515 5542222 | | [010 101010101010 1010101010 10101010 101010101010 10 1010 1010 1010 101010101010 12345678910 12 14 16 18 20 22 24 26 28 30 32 34 36 DAYS OF EXPOSURE FIG. 2. Number of live mussels (Actinonaias carinata) during exposure to potassium. rates shown in Table 1; these rates simu- late stream conditions. Table 1 shows the amount of water entering each test cham- ber per hour in the 3rd and 4th experi- ments. The total volume of a test chamber was 32.5 liters. From this information one can calculate turnover rates, if desired. pH readings taken on January 2 in the 3rd experiment are shown in Table 1. In the 4th experiment, pH was measured weekly in all chambers and varied from 7.0-7.7. Temperature was measured several times a week in all chambers and in the 1st experiment ranged from 11-13°C, in the 2nd experiment from 14-18°C, in the 3rd experiment from 18-19°C and in the 4th experiment from 16-21°C. Dissolved oxygen was measured once weekly in all test chambers with the azide modification of the Winkler method; measurements were also made each time 102 M. J. IMLAY 97/999999999987764333211100000000 000000 = a a = 3§1I99999999998888885544331! 000000000000 = < x E 2 uJ o = O 24|99999998888888886 6664322221111 111100 = >, n YN < E © 151888888888888888888888888877777765544 119:949:/9:9:9:99:9:99/9:9:99:399:9/9/9/99/9/9/99/9/99/9/99/9/9/9/9 11888888888888888888888888888888888888 12345678910 12 14 18 20 22 24 26 28 30 32 34 36 DAYS OF EXPOSURE FIG. 3. Number of live mussels (Amblema plicata) during exposure to potassium. more than one mussel died. Dissolved oxygen, with one exception (1 ppm 2 days in highest concentration of potassium of 3rd experiment), was always much greater than that found to be re- quired for these species of mussels in con- current experiments and ranged from 4.5- 9.6 ppm. In the 4th experiment total hardness, calcium hardness, acidity (as mg/l CaCO’, Anonymous, 1967) and alkalinity were measured in all test chambers and varied from 45-51.5 ppm, 34-40 ppm, 1-2 ppm, and 43.5-45 ppm CaCO’, respec- tively. RESULTS None of the mussels in the Ist experi- ment (about 30 ppm potassium) died in the first 17 days of exposure, but more than half died one by one in the next 15 days. Those which died were 4 Lampsilis POTASSIUM TOXICITY TO MUSSELS 103 A3TIO 1 00 43710 3 00 = a a = o Fr < x E z w о = о о = aitloiog 853100 5 alilioioios 5 3200 a Z ^тююююююююююююююю0ю0ю09э 8 470 10.10 10 10 10 10 10 10 10 10 10 10 1010 10 10 10 10 о a A= LAMPSILIS RADIATA SILIQUOIDEA A = FUSCONAIA FLAVA O 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 10 IO O 10 10 10 1010 101010 10 10 10 10 10 10 10 10 10 1010 lOlo |lOol0o9 39999999 99999999 O 15 30 45 60 75 90 105 120 135 150 165 180 195 210 225 240 255 270 285 300 DAYS OF EXPOSURE FIG. 4 Number of live mussels potassium. out of the initial 8 animals, and 5 Fusconaia flava out of the initial 8. In the 2nd experiment (about 9 ppm potassium), 56 days of exposure brought the death of 6 mussels while 16 mussels died in the next 31 days of exposure. Figs. 2, 3, and 4 show the number of days of exposure required to kill speci- mens of each species at each potassium concentration in the 3rd and 4th experi- ments. Eleven ppm was lethal to 90% of Actinonaias carinata in 36 days (Fig. 2). Amblema plicata was not quite as sensi- tive (Fig. 3). In 36 days 50% had died in 15 ppm K. Lampsilis radiata siliquoidea and Fusconaia flava were tested at lower con- centrations and died in about 8 months at 7 ppm K (Fig. 4). Mortality was much more rapid at 11 ppm. Only 1 of the 40 control animals died while the test animals were undergoing exposure. Further, on March 26, 2 months after the last day of exposure to potassium in the 3rd experi- (Lampsilis radiata siliquoidea and Fusconaia flava) during exposure to ment, only 1 of the 20 control animals had died. Conditions for the 2 months re- mained the same as during exposure (same temperature, oxygen, retention time, etc. ), and consequently it is evident that the control animals had been in healthy condi- tion during exposure. In conclusion 2 species of the amblemid subfamily Ambleminae (Amblema plicata and Fusconaia flava) and 2 species of the unionid subfamily Lampsilinae (Lampsilis radiata siliquoidea and Actinonaias cari- nata) are mortally sensitive to very low levels of potassium. DISCUSSION Toxicity and distribution The laboratory experiments demon- strated that the 4 species tested from 2 of the 3 subfamilies of unionid clams were killed by concentrations of potassium lower than those found in some rivers of the United States (cf. National Water 104 M. J. IMLAY Quality Network, 1962). K* (11 ppm) killed 90% of Lampsilis radiata siliquo- idea and Actinonaias carinata in 36-45 days. Eleven ppm was about as lethal to Fusconaia flava. From the rate of change of minimum lethal concentration with time it can be expected that with longer exposures, lower concentrations would produce mortality. The chronic test at 7 ppm destroyed laboratory populations of Fusconaia flava and Lampsilis radiata siliquoidea in about 8 months. Further- more, most studies of clams and other animals show that reproduction and/or growth are prevented at sublethal con- centrations of various toxicants. Inhibi- tion of spawning in fathead minnows (Mount, 1968) by copper, and reduced growth of clam and oyster larvae (Hidu, 1965) by detergent, are examples. Re- production, survival, and growth are, of course, all necessary for the ultimate exist- ence of a species. There is evidence that glochidial larvae of Anodonta may be more sensitive than adults to KCI. Läbos & Salánki (1963) found the glochidia to re- spond by abnormal activity to concentra- tions as low as 10*M KCI (3.91 ppm К) and sometimes even lower. Thus it is pos- sible that 3.91 or about 4 ppm K* is a maximum safe concentration, and only rivers with less than 4 ppm K* would con- tain mussels. The National Water Quality Network (1962) has measured potassium from many rivers in the U.S.A., and on the basis of the Lábos € Salánki report, the acute results at 11 ppm with rate of change described above, and the chronic results at 7 ppm, I hypothetically predicted that the rivers with less than 4 ppm К* would generally have mussels, and 7 ppm K was postulated as a predictive indicator that a river would have no mussels. In addition, 4-7 ppm was considered marginal. Since the Network data were tabulated for 3- month composites of weekly samples it FIG. 5. Prediction of presence of unionid clams (C) (0-4 ppm K), marginal (M) (4-7 ppm K), and no clams (NC) (7 or more ppm K) based upon National Water Quality Network data of potassium measurements. POTASSIUM TOXICITY TO MUSSELS 105 CT RS SN N NAS SYS ES Was SS SS N N SS AS N NN N NN N SY ROSY | i was felt that any high 3-month value would be the effective one regardless of the concentration at another season, and accordingly the higher value was chosen where more than one value was pre- sented. After making these predictions, I plotted the Network data as shown in Fig. 5. The symbols C (less than 4 ppm), M (4-7 ppm), and NC (greater than 7 ppm) are predictions of clams, marginal, and no clams. The symbols are plotted at the Jame Mail i um ppi or “Interior Basin” I NS y Y ARS р N > Y N < < N SS N N \ Ÿ S DIN S y A 2, LY) 4 Wh LLL ee LE CAES SS IN Wh В fauna as compared to other distinctive mussel assemblages. N NS The relatively large area in the United States inhabited by the Mississi FIG. 6. Reproduction of map published by H. & A. van der Schalie (1950) showing regions of U.S.A. containing S : N YI WEST FLORIDA ог APPALACHICOLAN unionid clams. y comeentano or CUMBERLANDIAN Y г ñ Е I MISSISSIPPI or INTERIOR BASIN в I ATLANTIC | М OZARK @® a Northern TD b.Southern 8 П PACIFIC specific sites on the river specified in the Network data. Comparison of Fig. 5 with a map published by H. & A. van der Schalie (1950), Fig. 6, shows a partial correspond- ence of high potassium concentrations with the regions of the U.S.A. that are known to essentially not contain mussels. The only discrepancy between Figs. 5 and 6 is the North Dakota to Texas zone of the U.S.A. But the occurrence of Fusconaia flava, Amblema plicata, Ac- M. J. IMLAY 106 ‘POHAUY YYWON UL safoadsqns sty} jo uonnqinsip эзеиихола4е smoys dew 31954] 'sesuey ur vapronbyis DIDIPDA Sid] JO uoynquysiq 6561 some 0 биз) Krim Ion j0 wann O ss < ЕЕ a NAN : = SE > an an LEON Lyf Sens ee ROUE eh mamma nn ERS, ‘ROWDY UJION UL Saldads -qns Ч304 107 uonnqınsıp ajeurxoidde smoys dew 19$] jo defi940 Aq poyesıpur 91 UOHPEPEIBIOQUI JO SPOIY ‘4 ‘о pue (ор) рирютыа@ duniansad pjuopouasg Jo uonnqinsi( ‘sjop pur saul] 'sesury Ul (594) 2124509 a ms EN] we воцэшу YYWON UL Sardads $43 jo uoNqysIp ajeunxoidde smoys deur pasuy ‘sesuey Ul DIDULIDO DIDULIDI SDIDUOUIY Jo поцичизяа IAS A um 1 | | Ц | | ‘зопэцгу YHON UL Satoads $143 JO цоциизятр ayeuı -Ixo1dde smoys deu 31950] 'sesuey ul рару pipuoosny JO чоци Ча 6561 CORTE ON) 4201914 ONION JO wnesnm hed by Murray and Leonard (1962) showing essential absence of unionid 15 . Reproduction of maps publ clams from North Dakota to Texas. F the reader is advised to see ( IG. 7 F in, or a more up-to-date survey of distributions within the Canadian Bas larke (1972). = 4 POTASSIUM TOXICITY TO MUSSELS 107 tinonaias carinata, and Lampsilis radiata siliquoidea (cf. Murray & Leonard, 1962; 41, 48-49, 110 and 151, respectively), species tested in the present studies in the laboratory, as well as the occurrence of the numerous other species of the Midwest is limited in significant numbers to only the eastern fringe of the North Dakota to Texas zone (Fig. 7). Van der Schalie (pers. comm.) also notes? that the mussels found in this zone are few in number; they were presented on his map (Fig. 6) to show that the relatively few mussels which are found here belong to the Mississippi basin assemblage. A 2nd method of testing the hypothesis was to compare the Network data with in- formation on the presence or absence of mussels in the Network rivers, some of which have been sampled for mussels by the Ohio State Museum (Stansbery, pers. comm., 1969). None of the 6 streams con- taining more than 7 ppm K (Colorado at Yuma, Bear, Big Sioux, North Platte, Platte, and South Platte) was recognized by Dr. Stansbery to be reported in the lit- erature as having mussels. Personnel from the Ohio State Museum have sampled one of these rivers (the Colorado River at the Network Yuma site) and found no mus- sels. Of the streams with less than 4 ppm K, Dr. Stansbery was unsure of 2 rivers but for the others, 28 of 39 were known to have mussels from reports in the literature or from Ohio State Museum sampling. In the marginal category (4-7 ppm K), only 2 of the 10 rivers were known to have mussels. For the sake of unbiased interpretation it should be noted that these 2 rivers were the only 2 sampled by Ohio State Museum. The 10 rivers had no known lit- erature report of mussels. It should be noted that 28 of 39 is significantly dif- ferent from 0 of 6, p <0.001, or 2 of 10, p <0.003 (Croxton & Cowden, 1955: 679- 680). An interesting case of mussel distribu- tion was described by Cvancara (1966) for the Red River of the North and its tribu- taries. Information on potassium levels in many of these tributaries appears in Water Resources Data for North Dakota (1966, 1968, and as yet unpublished data kindly supplied by the Geological Survey at Bis- marck, North Dakota and Lincoln, Nebraska) and in Water Resources Data for Minnesota (1965, 1966, 1967, and 1968). Potassium was measured in each tributary close to one of the sites indicated by Cvancara as having mussels. Average values were provided or were otherwise calculated by the author. Several species of mussels were found by Cvancara in the following tributaries in Minnesota: South Branch Two Rivers (4 ppm), Middle River (4), Red Lake River (4), Wild Rice River, Minnesota (5), Buffalo River (7), Pelican River (5-6), Ottertail River (3). In North Dakota the Pembina River had 8 ppm potassium but was similarly rich in mus- sels. This will have to be tolerated as a slight infringement on the hypothesis that rivers over 7 ppm will not have mussels. The Tongue River (4) in North Dakota had 4 species of mussels. The Forest River, North Dakota, was rich in mussels in the upper reaches near Fordville (4). At Minto (6) mussels were also found. Below this point mussels were not found, but Cvan- cara (1966) reports that the chloride level became very high. Suggestive evidence that potassium was also high will be men- tioned shortly. Finally, the Sheyenne River, North Da- kota, was rich in mussels throughout the sampled region (lower part). At the lowest points, West Fargo and Harwood, potas- sium was 8 ppm. Samples taken slightly The correlation here is striking and interesting. The basic and widespread “Mississippi” mussel assemblage usually becomes sparse in such western regions as extend from the Dakotas to Texas, particularly because the streams are often too intermittent, or, as in the case of the Missouri drainage, the rivers are often too silted to permit mussel faunas to survive. It should also be emphasized that the mussel distribution patterns as depicted partially reflect the fish distribution because of the host-parasite relations between larval mussels and their fish hosts. In any case the correlation as shown is a remarkable one and indicates biological relationships that warrant further study. Few animals are better suited for studying salt content or mineral relationships than mussels which often remain active for 25 years and monitor the materials taken into the shell in the growth process. 108 M. J. IMLAY upstream from mussel sites were found to have potassium values of 10 ppm. Thus this river also slightly erodes the pre- dictive hypothesis. The following rivers were high in potas- sium and had few or no mussels. The Wild Rice River, North Dakota (15 ppm), had only 1 species and only 1 out of many sampling stations yielded any mussels at all The Goose River, North Dakota, at Portland (8-14) and at Hillsboro (10-12), was well sampled for both potassium and mussels but had only 1 species. Cvancara (1966) found that the upper reaches of the Park, Turtle, and Forest Rivers were rich in mussels and had a low chloride content. The lower reaches were devoid of mussels and high in chlorides. He concluded that a correlation “of eco- logical significance’ appeared to exist be- tween high chlorides and absence of mus- sels. Pollution and physical conditions (bottom type, turbidity, river discharge rate, or industrial and municipal effluent) were believed not to be probable causes. The high chloride content was reported by Cvancara as being brought in by seepage from the Dakota group of cretaceous rocks. Observing that these rocks do contain potassium (Dole & Wesbrook, 1907), it ap- peared to me that potassium might be high where the chloride was high and be the direct cause of the absence of mussels. The following data on the Park River sub- stantiates this explanation. The South Branch of Park River below Homme Dam (7 ppm) had mussels. Further down- stream at Grafton, the Park River proper had no mussels and the potassium had in- creased (survey the same day) to 12 ppm. Finally, another measurement on that day at Oakwood (still further downstream) showed 40 ppm and there were no mussels. The correlation of potassium con- centration with mussel distribution is not necessarily a direct cause-and-effect cor- relation, but could conceivably be created by a common variable (carbonate, Mg, silting, etc.) that causes both the potas- sium and distribution variation. This is not considered likely, however, because of the laboratory demonstration of direct toxicity. Potassium may enter a stream naturally or artificially as a pollutant. Potash (K?CO*) production has been listed as a significant and steady component of the minerals industry (Krieger, 1968). KCI occurs in brines from oil wells and other industrial wastes (McKee & Wolf, 1963). It is con- sidered to be a significant component of paper wastes (Powers, Sacks & Holdaway, 1967: Table 1) and occurs in runoff from irrigation diversions or excessively fer- tilized crops. The Green River, Kentucky, lost most of its former mussel abundance from brine waste in 1958 with the opening of the Greensburg, Kentucky oil field (Williams, 1971). Other organisms Low concentrations of potassium may be toxic to other animals but only rela- tively short-term studies of potassium ex- posure ( 1 week) have come to my atten- tion (McKee & Wolf, 1963). Fig. 3 indi- cates less than 50% mortality for Amb- lema plicata for the first 2 weeks of ex- posure at any concentration tested. Extra- polation of Fig. 3 indicates the probability of such a delay in toxicitity of potassium for concentrations much higher than those used in the present studies. Thus studies of only 1 week, while abounding in the litera- ture, give little evidence of the chronic effects of potassium. There is scant evidence that potassium may be highly toxic to other animals. Galun € Kindler (1966) found that the medicinal leech, Hirudo medicinalis (Linnaeus), would no longer imbibe an NaCl: glucose solution across a mem- brance if 7.5 X 102M КС were added, but this was a rather high K* concen- tration. Coler, Gunner, & Zuckerman (1967) substituted sodium for potassium in the growth medium used with tubificid oligochaetes because of reports of an effect of potassium on tubificids, but again con- centrations were high. There are indications that high sensi- tivity to potassium may be unique to unionaceans or at least certain mollusks. In a comparison of numerous phyla, (Prosser POTASSIUM TOXICITY TO MUSSELS 109 & Brown, 1961: 58-63), Anodonta was dis- tinguished by the lowest blood potassium along with the other common cations, ex- cept for calcium. During narcosis, Anodonta (Bivalvia) and Lymnaea (Gastropoda: Pulmonata) increase т weight, and the principal ions become diluted in the blood, except for potassium which is released by cells at an even faster rate than it is diluted (Robertson, 1964: 296). Further studies are necessary to show whether chronic sensitivity to potassium is unique or general among aquatic life. Such studies are underway in this laboratory and the results to date show that a freshwater fish, leech, and snail are at least an order of magnitude less sensi- tive to chronic potassium exposure than the mussel. Effects of other ions Salanki (1962) found the common cations K+, Nat, Mgt, Cat to affect seriously the normal activity of glochidial and adult Anodonta cygnea, at concentra- tions which, relative to the actual con- centrations in streams, would be im- portant only for the case of potassium in real river conditions. Although, it is well known that these other cations may ameliorate the toxic effects of potassium, [sodium for Artemia (Stahl, 1967), and calcium for Tubifex (Ringer, 1899), to cite representative ex- amples] the potassium was highly con- centrated in such studies. There is little reason to conclude that their addition would protect organisms from potassium at the low levels found to be chronically lethal for mussels. Since KCl was the vehicle used to introduce K+ in the pre- sent studies, it is advisable to examine the possibility that Cl~ contributed to the ob- served toxicity. The report by Ellis (1937: Table 7) suggests that C17 is not the toxic ion in KCl because goldfish show по apparent injury after 25 days exposure to the very high concentration of 5,000 ppm NaCl. Evidence from data related to mussels, that C17 is not the toxic ion in KC1, is in the Water Quality Network data (1962) which show chlorides to be much higher in mussel producing streams than in KCl solutions which killed mussels in the lab- oratory. Examples are the Allegheny (10- 46 ppm), Escambia (8-100 ppm), Illinois (9-32, 14-40), Little Miami (9-30), Missis- sippi (Cape Giradeau, Missouri) (9-21), Ouachita (14-355), Potomac (8-18), St. Lawrence (17-36), Wabash (22-132), and Tombigbee (4-58) Rivers. These are all rivers specifically stated by Dr. Stansbery (pers. comm., 1969) as having mussels. Another line of evidence is the finding that the threshold of NaCl effect on the activity of Anodonta cygnea glochidia was at 100 times greater concentrations than the KC1 threshold. Further, the effect of NaCl was short lived (Lábos € Salánki, 1963).* The order of threshold concentra- tion. (based ion’ molarity was K GENE — mar — р Bere | — oe LS 22 Res и A : De Е - я «application a ( 2 ms — 2 mt | ee еее pfeifferi alexandrina alex. camerunensis alex. s udanica Ismailiya wansoni tang- FIG N Tr ( I SEE + = AA ES A asf) IN IT LA LE J > 4 Biomphalaria pfeifferi sudanica tang. EE. YOR] —— < alex. wansoni camerunensis alexandrina FIG. 2. Sampling species identical laboratory conditions and fed on scalded oven-dried lettuce. Preparation Hepato-pancreas is removed from the live snail and placed in a micro test tube with a drop of distilled water. After homo- genization with a rotating glassrod the specimens are centrifuged at a tempera- ture of 5°C and 12000 g for 2 minutes. 1. The esterase bands found in African Biomphalaria species by electrophoresis of hepato-pancreas. localities for the African Biomphalariae examined and the geographic distribution of the Each specimen contains hepato-pancreas from only one animal, so that the esterase pattern is determined for individual snails. Electrophoretic procedure The horizontal starch-gel electro- phoresis is carried out in a rectangular plexiglass frame (0.6 x 15 x 28 cm) using a gel composed of 12.5% starch dissolved in a 1:14 dilution of a 0.341 M boric acid ESTERASES OF BIOMPHALARIA buffer with a value of pH 9.0 (21.1 g boric acid and 5.32 g NaOH in 1 litre H,O). Concentrated buffer is placed in the buffer containers. Four pieces of filter-paper Whatmann No. 1 serve as a bridge be- tween the gel and the buffer. The super- natant from each centrifugated hepato- pancreas is sucked up in a piece of What- mann No. 4 filterpaper 6 x 3 mm and placed in a slit 3 - 4 cm from the edge of the gel at a distance of about 2 mm from each other. This arrangement makes space for approximately 20 specimens. During electrophoresis the gel is placed between 2 cooling plates of the same size as the gel. Plastic-foil is placed between the gel and the cooling plates, which maintain a tem- perature of 0°C to 2°C. Best results are ob- tained with a voltage of 290 У сог- responding to 70 mA in 2 hours. Methods of staining To obtain the clearest staining of the bands, the gel is split lengthwise. For the specific staining of esterases 50 mg fast blue salt RR (Michrome) was used, dis- solved in 100 ml buffer, to which was added 2 ml 1% 1-naphthyl acetate in ace- tone and water in the ratio of 1:1. The es- terases are stained for approximately half an hour. RESULTS Biomphalaria pfeifferi In this species I found 6 esterase bands (see Fig. 1), out of which 2 move towards the cathode and the remaining to the anode. The bands are called a', a?, b', b?, с! 117 and &@. The number of animals examined from each locality and the bands occuring are shown in Table 1. The individuals from Sendafa, Lubum- bashi and Pakwach were identical, and all the bands appeared with a frequency of 100%. The Gwebi individuals were similar to the 3 populations mentioned except that band a! was lacking. Unfortunately only 2 specimens from this population were avail- able. Biomphalaria alexandrina The maximum number of esterase bands found in this species was 11, desig- nated: Al A2 А BiB В. С EICHE: and С° (see Fig. 1). However, with the technique used, Biomphalaria alexandrina from Ismailiya did not show bands Nos. В', В? and В? but instead 2 more powerful ones with a quite thin band in between (see Fig. 1) moving a little faster towards the anode. These 3 bands almost merge. In all the other B. alexandrina populations bands B', В? and B® were always present. The fre- quency of the bands А', A’, Аз, C!, C?, C?, C* and С? is given in Table 2. It can be seen that the variation in the esterase pat- tern in B. alexandrina is very great from one population to another. The only bands always found in the A and С series are A! and C? Apart from the B-series, the Ismailiya population can always be dis- tinguished from the others by the pres- ence of С'. The Suez population is rec- ognizable by the presence of С? and С? and the lack of C'. The Abu Rawaash popula- tion showed the greatest variation. The TABLE 1. Total number and frequency of esterase bands in 4 populations of Biomphalaria pfeifferi. Localities No. Esterase bands a! а? b! b? c! с? a! а? b! b? c! с? Sendafa 10 10 10 10 10 10 10 100 100 100 100 100 100 Lubumbashi 14 14 14 14 14 14 14 100 100 100 100 100 100 Gwebi 2 0 2 2 2 2 2 O 100 100 100 100 100 Pakwach 8 8 8 8 8 8 8 100 100 100 100 100 100 ¿N 4 RSE = 4 E WIUM-AND a] 3. C 118 001 001 001 001 001 001 &) 001 001 001 001 001 001 0, От 001 001 001 001 001 001 00T OOT 001 00T 001 001 001 001 От 001 001 iD ¿el ¿el (2) Aduonboa y e > | DIN Y] AH tO spu Bq 9581915 0810) ‘opuogey WOLF IUOSUDN SISUIUNAIUUDI © 19 Y YH to © 5 Ow TH] AH tO O 10 tt tO DIN Y] YH tO (se) 7 $ IIUIIINIIG) Mm On + + + © < Oin + + + © < хючччо 9 opuogry + I¡UBBUBSIN + oyoseg P IJO]IALIA с ezodur N 9 ipnqn' pasn speunue jo ‘ON Sa1}1[P00"] puppy dwoirg jo pue 03u0/) ay} UL $91 Цеэо| © шоц язиаиплаиио pupjpydwoirg UL зрие4 э549}59 jo Aduanbaay pue aaquınu [eJ0L “€ ATAVL 001 0 001 0 001 0 98 001 GT 0 ST O0T 0 001 0 0 0 8L 001 РТ 0 FI 90 18 001 УР 0 OOL 76 OOT I ST 91 69 GI 001 15 0 90 IS 001 IT $ OT OOT 0 001 001 0 0 SI OOT 8 0 8 0 001 001 LS 0 69 OOT 001 0) 8 8 GL OC 00T GL 0 0 001 001 9 Fr 8 GL 19 001 68 0 0 OOT 001 ST IT sI GL IT 001 1$ 0 001 0 001 SI G SI «_) r) &) a) (O) eV zV iV sO 1) re) (94) Aouonboi} spurq 9561915 0 ST 0 0 L 0 S 0 8 0 L 0 9 0 91 0 pl 0 a 10) 9919441990) DO © © 1 © m1 © © © = — — $1 SI posn speunu® 119) ‘ON РАЦ Ш] 291$ qnayed) ysermey nqy BAN [A UINOJABY Y 621) ве L выриехэ[у $94207] '(5$91195-Я 94] виНзэхэ) вимрирха]р рызтруашо jo suonepndod 6 ит spurq э$е49}59 иоцииоо Jo Áduanba.y pur oqUINN “ZA TAVL ESTERASES OF BIOMPHALARIA 119 pattern of the Giza and Tanta individuals was almost alike. Biomphalaria camerunensis Eight esterase bands are always present (see Fig. 1 and Table 3). Biomphalaria alexandrina wansoni This species is identical to B. cam- erunensis (see Fig. 1 and Table 3). Biomphalaria sudanica tanganyicensis Unfortunately only a limited amount of material (6 specimens) was at my disposal. The middle bands (b series) of Biomphalaria sudanica tanganyicensis (see Fig. 1) are identical with those of B. alex- andrina from Ismailiya. DISCUSSION The division of the African Biompha- laria species has caused many problems. Mandahl-Barth (1958) described con- chological and anatomical differences for a division of species, but drew attention to the fact that a separation based on these characters was doubtful because, in re- spect of both characters “almost every intermediate stage has been found, so that it seems reasonable to collect them into one species, as some authors have actually done.’ He continues: “However, in na- ture some of them behave as separate species, for they have been found living in the same small place without inter- breeding.” As a help for a systematic examination of African species of Biomphalaria and Bul- inus electrophoresis has previously been applied by Wright (1963, 1965, 1966), Coles (1970) and Burch € Lindsay (1967). Wright (1966) conjectured that esterases from the hepato-pancreas might be useful for further examination of the taxonomy when mature snails are kept on a standard diet (lettuce), a method which has been followed in this work. Coles (1970), on the other hand, doubted that esterases could be of any value in distinguishing between species. Burch € Lindsay (1967) showed that 2 species groups in the genus Bulinus that are difficult to distinguish by morphological characters could be characterized by their esterase patterns. My results show that the Biomphalaria pfeifferi, B. alexandrina, B. sudanica tanganyicensis and B. camerunensis diagnosed on morphological characters, have different esterases and therefore also different genes. The morphological characters can thus be used in identifica- tion of the snail populations in question. According to Dr. Mandahl-Barth's per- sonal comments, В. “alexandrina” wan- soni is related more closely to B. camerunensis than to B. alexandrina. His views are supported by the present work, which shows that B. camerunensis and B. “alexandrina” wansoni have identical es- terases. B. wansoni can be considered an inland form of B. camerunensis (see Fig. 2): The electrophoretic technique em- ployed in this study reveals great varia- tion in the populations of Biomphalaria alexandrina examined. In contrast the populations of B. camerunensis and B. pfeifferi examined showed hardly any variation in the esterase pattern although the geographical distance between the populations of B. pfeifferi was much greater than that between the different B. alexandrina populations (see Fig. 2). Cridland (1968) showed that different Egyptian populations of Biomphalaria alexandrina vary in their susceptibility to infection with Egyptian strains of S. man- soni, whereas B. pfeifferi from geo- graphically widely separated localities all have the same high susceptibility widely separated localities all have the same high susceptibility to infection. The results ob- tained in this work thus demonstrate a correlation with (1) the lack of variation in the esterase pattern and the uniform sus- ceptibility to infection in B. pfeifferi, and (2) a corresponding variation of both fea- tures in B. alexandrina. The populations from Giza and Tanta have almost the same esterase pattern and same susceptibility to infection, but apart from this finding it has not been possible to observe a direct rela- tion between the occurrence of certain esterases and susceptibility in B. alex- 120 С. WIUM-ANDERSEN TABLE 4. Mean measurements of shell and rachidian of 10 fully grown Biomphalaria alexandrina from each of the 8 Egyptian localities, carried out by Dr. G. Mandahl-Barth. Localities Shell A D H X $ X $ Ismailiya 6.0 129 0.13 3.4 0.06 Giza 5:3 I3100:18 41 0.05 Alexandria 5.6 13.3 0.36 4.1 0.13 Suez Sac TELS 20:07 3.9 0:04 El Minya 55 13.8 ? 43 ? Qalyub 5.3 11.5 0.09 3.3 0.04 Tanta 5.4 13:35 0:94. 4:37. 40.08 Abu Rawaash 5.8 12.8 0.23 4.4 0.07 Central tooth U Ux 100 Hx 100 X $ Н D length ши 5.3 0.11 156 26.4 10-11 46 0.12 112 31.3 12 5.5 0.16 134 30.8 12 40 0.07 103 34.5 12 4.9 ? 114 31.2 14 4.8 0.06 146 28.7 14 5.0 0.09 116 32.3 15 44 0.08 100 34.4 15 A = number of whorls D = greatest diameter of shell in mm H = height of last whorl behind aperture in mm U = greatest diameter of umbilicus in mm A s = standard error of the mean X = mean TABLE 5. Mean measurements of shell and rachidian of 10 fully grown Biomphalaria from each of 5 species, carried out by Dr. G. Mandahl-Barth. Biomphalaria sp. Shell Central tooth (Localities) D H U Ux 100 H x 100 A X 5 X 5 X 5 H D length in u wansoni (Kisangani) 5.3 14.2 0.10 42 002 55 0.14 131 29.6 13 camerunensis (Lubudi) 5.5 14.6 0.18 4.9 0.07 5.8 0.09 118 33.6 15 sundanica tanganyicensis 6.0 (Mwanza) 6.0 15 0.20 4.4 0.04 5.6 0.13 127 27.6 11 pfeifferi (Katanga) 50 131 0.22 50 0.02 43 0.06 86 38.2 17 typical sudanica (Sudan) 6.0 14.4 0.27 3.8 0.14 5.7 0.18 150 26.4 10 A = number of whorls U = greatest diameter of umbilicus in mm D = greatest diameter of shell in mm s = standard error of the mean H = height of last whorl behind aperture X = mean in mm andrina. length of the central radular tooth and ex- The Biomphalaria alexandrina popu- lation from Ismailiya shows similarity with В. sudanica tanganyicensis as regards the B-series. The Ismailiya population is the only В. alexandrina population having C*, while the remaining esterases in the Ismailiya population are identical with those of the other 3 populations of B. alex- andrina. Esterase band No. A? in B. alex- andrina occurs in B. pfeifferi and band A! in B. sudanica. Dr. Mandahl-Barth has measured the amined the shape of the shell (see Tables 4 and 5). The central tooth in Biomphalaria pfeifferi was 17 и, in В. sudanica tanganyi- censis Ши and in В. alexandrina it varied from 10 to 15 a. The ratio 410 had a value of 86 in B. pfeifferi from Katanga and of 150 in typical B. sudanica, it varied from 100 to 156 in populations of B. alex- andrina. In the length of the central tooth and in shell shape the Ismailiya popula- tion showed great conformity with B. sudanica. The question therefore arises ESTERASES OF BIOMPHALARIA 121 whether this population should not be con- sidered as an isolated population of B. sudanica. The esterase pattern shows a great genetic polymorphism within and be- tween populations in Biomphalaria alex- andrina, as the other characters used (susceptibility, length of central teeth, ratio of umbilicus to height of the shells) have also shown. B. alexandrina is prob- ably a species in evolution. ACKNOWLEDGEMENTS I am greatly indebted to Drs. G. Mandahl-Barth and C. C. Cridland for much good advice and inspiration. My thanks are also due to Dr. T. Bennike who collected the material. This study was supported by a grant from the WHO Snail Identification Cen- tre, Charlottenlund. LITERATURE CITED BURCH: TB... & LINDSAY, С.К., 1967, Electrophoretic analysis of esterases in Bulinus. Amer. malacol. Union ann. Reps., 34:39-40. COLES, G.C., 1970, Enzyme electrophoresis and speciation of Schistosoma intermediate hosts. Parasitology, 61: 19-25. CRIDLAND, C.C., 1968, Results of exposure of batches from highly susceptible and less- susceptible strains of Biomphalaria alex- andrina from Egypt to strains of Schistosoma mansoni from Cairo and Alexandria. Bull. Wild. Hlth. Org., 39: 955-961. CRIDLAND, C.C., 1970, Susceptibility of the snail Biomphalaria alexandrina alexandrina from the UAR and the Sudan to infection with a strain of Schistosoma mansoni from Tanzania. Bull. Wid. Hlth. Org., 43: 809- 815. MANDAHL-BARTH, G., 1958, Intermediate hosts of Schistosoma. World Health Organization, Geneva, Monograph Series No. 37. p 46. WRIGHT, C.A. € ROSS, G.C., 1963, Electro- phoretic studies of blood and egg proteins in Austrolorbis glabratus, (Gastropoda, Planorbidae). Ann. trop. Med. Parasitol., 57: 47-51. WRIGHT, C.A. € ROSS, G.C., 1965, Electro- phoretic studies of some planorbid egg pro- teins, Bull. Wid. Hlth. Org., 32: 709-712. WRIGHT, CA, FILE, 5.К. & ROSS. СЕ. 1966, Studies on the enzyme systems of planorbid snails. Ann. trop. Med. Parasitol., 60, 4: 522-525. ZUSAMMENFASSUNG UNTERSUCHUNGEN MIT HILFE DES ELEKTROPHORS AUF ESTERASEN BEI EINIGEN AFRIKANISCHEN BIOMPHALARIA-ARTEN (PLANORBIDAE) G. Wium-Andersen Esterasen aus dem Hepato-Pankreas afrikanischer Biomphaoarien-Arten wurden mittels Stärkel-Gel-Elektrophorese untersucht. Auf Grund der Esterasen war es möglich, die folgenden nach ihren morphologischen Charakteren bestimmten Arten ebenfalls zu unterscheiden: Biomphalaria pfeifferi (Krause). B. alexandrina (Ehrenberg), B. camerunensis (C. R. Boettger) und B. sudanica tanganyicensis (Smith). B. alexandrina wansoni Mandahl-Barth ist in Bezug auf die Esterase-Zusammensetzung identisch mit B. camerunensis. Die Esterasen bestätigen die Ähnlichkeit, die zwischen Biomphalaria alexandrina von Ismailia und B. sudanica tanganyicensis auch in der Morphologie der Schale festgestellt wurde. Bei B. alexandrina variieren die Esterasen zwischen den einzelnen Populationen, während sie bei allen Populationen von В. pfeifferi gleich blieben. Mit dieser Variabilität ist eine stark unterschiedliche Empfänglichkeit für die Infektion mit Schistosoma mansoni Sambon in den untersuchten Populationen von B. alexandrina verbunden, und eine konstante Empfänglichkeit für Infektion mit diesem Parasiten bei den untersuchten Populationen von B. pfeifferi. H. 2. bo bo G. WIUM-ANDERSEN RESUME ETUDES PAR ELECTROPHORESE SUR LES ESTERASES DE QUELQUES ESPECES AFRICAINES DU GENRE BIOMPHALARIA (PLANORBIDAE) G. Wium-Andersen Les estérases de l'hépato-pancréas d'espèces africaines de Biomphalaria ont été examinées au moyen de |’ électrophorése sur gel d'amidon. Sur la base des estérases il a été possible de séparer les espèces suivantes déterminées d'après leurs caractères morphologiques: B. pfeifferi (Krauss), B. alexandrina (Ehrenberg), B. camerunensis (C. R. Boettger) et B. sudanica tanganyicensis (Smith). B. alexandrina wansoni Mandahl- Barth est identique à B. camerunensis en ce qui concerne les données en estérase. Les estérases accentuent la conformité, déjà reconnue par la morphologie de la coquille, entre Biomphalaria alexandrina de Ismailiya et B. sudanica tanganyicensis. Chez В. alexandrina les estérases varient d'une population à l'autre tandis qu'elles sont tout-ä-fait constantes dans toutes les populations examinées de В. pfeifferi. Cette variabilite est a mettre en parallele avec une grande variation de la susceptibilité à l'infection par Schistosoma mansoni Sambon envers les populations examinées de В. alexandrina et la constante susceptibilité à l'infection par 5. mansoni dans les populations examineés de B. pfeifferi. AL RESUMEN ESTUDIOS ELECTROFORETICOS SOBRE ALGUNAS BIOMPHALARIA SPP. AFRICANAS (PLANORBIDAE) G. Wium-Andersen Esterasas del hepato-pancreas de Biomphalaria spp. de Africa fueron examinadas por medio de almidón-gel-electrofóresis. Sobre tal base fue posible separar las siguientes especies determinadas por $us caracteres morfológicos: B. pfeifferi (Krauss), B. alexan- drina (Ehrenberg), B. camerunensis (C. R. Boettger), y B. sudanica tanganyicensis (Smith). B. alexandrina wansoni Mandahl-Barth es idéntica a B. camerunensis en lo que respecta al patrón de esterasa. Las esterasas acentúan la conformidad encontrada en la morfología conchológica entre Biomphalaria alexandrina de Ismailiya y B. sudanica tanganyicensis. En B. alexandrina las esterasas varian de una población a otra, mientras que fueron completamente constantes en todas las poblaciones observadas de B. pfeifferi. Esta variabilidad es paralela a la gran variación en susceptibilidad a la infección con Schistosoma mansoni Sambon constatada en las poblaciones de B. alexandrina examinadas, y una suscep- tibilidad constante a la infección con S. mansoni en las poblaciones de B. pfeifferi. Te ABCTPAKT ЭЛЕКТРОФОРЕТИЧЕСКОЕ ИЗУЧЕНИЕ ЭСТЕРАЗЫ НЕКОТОРЫХ АФРИКАНСКИХ ВИЛОВ BIOMPHALARIA (PLANORBIDAE) Г. ВИУМ- АНДЕРСЕН одом крахмально-гелевого электрофореза изучалась эстераза из о-панкреаса видов Biomphalaria. На основании изучения эстеразы 3 лось возможным разделение следующих видов моллюсков, определенных по их морфологическим признакам: В. pfeifferi, (Krauss), В. alexandrina (Ehren- berg), В. camerunensis (Boettger) и В. sudanica tanganyicensis (Smith). По своей эстеразе В. alexandrina wansoni Mandal-Barth оказалась идентичной В. сатетипеп- 515. Эстераза подтверждает сходство, найденное по морфологии раковины у В. alexandrina из Исмаилии и В. sudanica tanganyicensis. У В. alexandrina acTepa3a изменялась от одной популяции к другой, ау всех изученных популяций В. pfeifferi она была совершенно постоянной. Эта вариабильность оказалась параллельной большим колебаниям в восприимчивости к инфекции Schistosoma № mansoni Sambon, найденной B исследованных популяциях В. alexandrina. Наблюдается ПОСТОЯНСТВО в восприимчивости к инфекции S. mansoni E изученных популяциях В. pfeifferi. Z.A.F. MALACOLOGIA, 1978, 12(1): 123-150 EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) I. GENERAL OUTLINES OF DEVELOPMENT! Emile 5. Demian? and Fouad Yousif? ABSTRAGT The present series of embryological investigations is an extension of the basic morphological, biological and ecological studies currently in progress on the aquatic gastropod Marisa cornuarietis (Linnaeus), а snail of potential importance in the biological control of schistosome-transmitting snails. This part is concerned with the early cleavage, gastrulation and general outlines of embryogenesis in Marisa. The egg undergoes total spiral cleavage, which was followed up till the 24-cell stage. The first 2 divisions are equal; the 3rd is unequal and dexiotropic. Gastrulation is epibolic, and the blastopore closes by the end of that process. Embryogenesis takes 8 days at 25-30°C and 20 days at 15-20°C. The blastula is fully developed in 14 hours, and gastrulation is completed in 22 hours at the former temperature range. Torsion occurs through the differential growth of the 2 sides of the embryo; it starts about 3% days after egg-deposition and lasts for about 2 days. Twelve distinct embryonic stages were distinguished during embryonic development after gastrulation. The age, dimensions and distinctive anatomical features of each of these embryonic stages are given, together with an outline of the development of the different organ systems, except for the reproductive system which develops mainly after hatching. Findings partly diverge from earlier reports for related ampullariid snails, in particular as regards the origin and development of the mantle, mantle cavity, pericardium, heart, kidney, ureter, renal vestibule and digestive gland. INTRODUCTION The freshwater snail Marisa cornuarietis (Linnaeus) has recently attracted con- siderable attention as a potential antagon- ist of some snail vectors of schistosomiasis and fascioliasis. The present series of in- vestigations is another contribution to the basic morphological, biological and eco- logical studies currently undertaken at Ain Shams University, Cairo, with the main objective of gaining as much fundamental knowledge about this snail as possible, be- fore any attempt is made to introduce it as a biological control agent against schistosome-transmitting snails into areas outside its present range of distribution in the neotropics. The Ampullariidae (syn. Pilidae: Meso- gastropoda, Architaenioglossa), to which Marisa cornuarietis belongs, are lower pro- sobranchs specialized for an amphibious existence in a way unparallelled by any other prosobranch. Among other char- acteristics, they possess a lung in addition to a monopectinate gill, and have 2 func- tional excretory chambers. The develop- ment of the lung of the Ampullariidae, the origin of their 2 renal chambers and the homologies of some of their organs have been so far variously interpreted and dis- puted by many authors. The homologies of their right gill with the left gill of the Mesogastropoda, and of their 2 renal chambers with the single left kidney of other mesogastropods are still question- able. The points which have remained un- decided in the ontogeny of the Am- This investigation was supported in part by research grants (AI 04906 and Al 07696) from the National Institute of Allergy and Infectious Diseases, U.S. Public Health Service. "Department of Zoology, Faculty of Science, Ain Shams University, Cairo. 3Laboratory of Bilharziasis Research, National Research Centre, Cairo. 124 DEMIAN AND YOUSIF pullariidae are perhaps more numerous than in any other prosobranch family. The present paper is the first in a series that deals with the embryonic develop- ment of a member of the ampullariid genus Marisa (syn. Ceratodes), the devel- opment of which has hitherto not been ex- amined. In this paper, a description is given of the early cleavage, the gastrula- tion and the outline of ontogeny in M. cornuarietis before hatching. Details on the origin and organogenesis of the dif- ferent organ systems, excepting the repro- ductive system which develops mainly after hatching, are dealt with in sub- sequent parts of this series. The bearing of our results on the various ontogenetic problems and on the phylogenetic rela- tions in the family Ampullariidae are dis- cussed in the relevant parts of this series. HISTORICAL The literature pertaining to the embry- onic development of freshwater proso- branchs is generally limited and mostly concerned with a few familiar forms such as Paludina (=Viviparus). Marine pro- sobranchs as well as opisthobranchs and pulmonates were subject to more numerous and elaborate embryological investigations. A detailed review of the literature on molluscan development is be- yond the scope of the present report. Extensive historical reviews are included in the works of Fretter € Graham (1962) and Hyman (1967). Moreover, a general survey of the present state of knowledge of descriptive and experimental molluscan embryology was given by Raven (1966), with special emphasis on cytological and cytochemical aspects of development. Comparatively little work has been done on the embryonic development of the Ampullariidae. The earliest of these studies are probably those made by Semper (1862) on Ampullaria polita De- shayes, and by Ryder (1889) on A. de- pressa Say. These were brief reports mostly concerned with cleavage divisions. Scott (1934) gave a somewhat more detailed account of the development of A. canali- culata Lamarck wnich, however, was limited to an external description of some embryonic stages. The most elaborate in- vestigation was probably that of Ranjah (1942) which included a detailed descrip- tion of the embryonic development of Pila globosa (Swainson) and an extensive dis- cussion of the older literature dealing with the embryology of the Gastropoda. Studies largely concerned with specific ontogenetic problems of the Ampul- lariidae are those by Brooks € McGlone (1908) on the origin of the lung in Ampul- laria depressa Say, by Fernando (1931) on the ontogeny of the kidney in A. gigas Spix, by Nagaraja (1943) on the develop- ment of the alimentary canal in Pila virens (Lamarck), and by Raja (1943) on the formation of the shell gland in P. globosa (Swainson). The observations made by these earlier authors are discussed in the relevant sections of the present series. MATERIAL AND TECHNIQUES Marisa cornuarietis used in the present study were reared in the laboratory from an original Puerto Rican stock. A large colony was maintained in 3- and 10-gallon glass aquaria filled with continuously aerated tap water. The snails were liberally fed on fresh romaine lettuce every other day. Egg masses were carefully scraped off the side walls of the aquaria immediately after deposition and isolated in Petri dishes in dechlorinated tap water. The water was changed every other day, and a daily record was kept of the maximum and min- imum water temperatures in these dishes. Since temperature is undoubtedly a major factor affecting the rate of develop- ment, embryogenesis was followed up twice, under 2 different temperature con- ditions: once during June and July when the water temperature in the incubating dishes ranged between 25 and 30°C, and also during the following January and Feb- ruary at a temperature range of 15-20%C. Each time observations on the developing eggs were made in more than 100 egg masses. To follow up embryonic development, eggs were successively separated from the egg mass, 2 at a time, at intervals ranging EMBRYOLOGY OF MARISA from % to 12 hours according to the age of the egg mass. Each egg was immediately dissected with a pair of sharply pointed needles in saline solution under a stereo- microscope. The embryo was carefully taken out of the egg capsule and freed from the surrounding albumen. Some em- bryos were examined fresh, while others were fixed, stained and mounted whole, or infiltrated with paraffin wax and sec- tioned. Drawings were made of both fresh and stained embryos with the aid of a camera lucida. Several fixatives were used with varying degrees of success. The best results were ob- tained with the Duboscq-Brazil modification of Bouin s fluid (Gatenby € Beams, 1950) which was therefore largely used. The material was washed in 70% ethanol for at least 48 hours after fixation then stained for 1-3 hours in alcoholic borax carmine solution (Grenacher, 1879), dehydrated in ascending grades of ethanol, cleared in xylol or cedar wood oil, and mounted in canada balsam. Embryos fixed in the above mentioned way, but stained only very lightly with alcoholic borax carmine for 15 minutes, were infiltrated with paraffin wax and sec- tioned to the thickness of 54. The light borax carmine staining facilitated rapid orientation of the embryo in the paraffin block, under a stereomicroscope. Several sets of serial transverse and sagittal sec- tions were cut in every embryonic stage and stained mainly with Delafield's haematoxylin and eosin or with Mallory $ triple stain. Graphic reconstructions of the embryo and of its internal organs were made in each stage with the help of these series of serial sections. OBSERVATIONS The egg, egg mass, egg laying and mating behaviour of Marisa cornuarietis have been described in a previous paper (Demian & Ibrahim, 1970/71). The ferti- lized ovum (Fig. 1A) is spherical, opaque, light brownish and measures about 110 in diameter. The first indication of polar dif- ferentiation in the ovum can be noted a few minutes after oviposition, when 2 clear . I. GENERAL DEVELOPMENT 12: QU polar bodies (PB) are extruded, one after the other, at one end of the ovum, which represents the animal pole. These bodies remain attached to the segmenting ovum during early cleavage until the 16-cell stage is reached. Two hours after the appearance of these polar bodies and before the first cleavage, a small translucent area becomes con- spicuous at the animal pole, and the nucle- us migrates into this region from the centre of the ovum. The rest of the cyto- plasm remains opaque and condensed with yolk, whereby the animal and vegetative poles become well-differentiated. More or less similar processes of polar differentia- tion have been recognized before the on- set of the Ist cleavage in the eggs of Ampullaria canaliculata and Pila globosa by Scott (1934) and Ranjah (1942) respec- tively. 1. Cleavage The egg undergoes the typical total spiral cleavage common to the Gastro- poda. In eggs maintained at temperatures of 25-30°C, the Ist cleavage (Fig. 1B,C) takes place 2%-3 hours after egg-deposi- tion. It starts at the animal pole and pro- ceeds meridionally towards the vegetative pole, dividing the ovum into 2 equal spherical blastomeres. These blastomeres soon lose their regular spherical form as they become pressed against each other. The 2nd cleavage is also meridional and passes at right angles to the 1st cleavage. It starts about 1 hour after the completion of the 1st cleavage, and results in the forma- tion of 4 equal spherical blastomeres or quadrants (A, B, C, D, Fig. 1D) enclosing a narrow central cleavage cavity in be- tween them. However, these blastomeres soon press against each other, lose their spherical form and the cavity between them consequently disappears. The first indication of the spiral char- acter of this cleavage appears about 45 minutes after the commencement of the 2nd division, when the cleavage planes cease to be strictly meridional and make an angle with the polar axis of the egg. In consequence, at the animal pole, the 126 DEMIAN AND YOUSIF FIG. 1. Early cleavage divisions: A, Fertilized ovum. В, Beginning of Ist cleavage. С, 2-cell stage. D,E, 4-cell stage as seen from the side and from the vegetative pole. F,G, 8-cell stage as seen from the side and from the animal pole. H,I,J, 12-, 16- and 24-cell stages as seen from the animal pole. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 127 KEY TO LETTERING ON FIGURES (All drawings are of Marisa cornuarietis (L.)) A auricle AM _ aortic ampulla ANP anal cell-plate APP apical cell-plate AT archenteron BL blastocoel BV buccal vestibule CG cerebral ganglion CM cerebral commissure CML. columellar muscle CN ctenidium COP crop or mid-oesophagus DGA anterior lobe of digestive gland DGP posterior lobe of digestive gland В еуе EN — endoderm ET ectoderm F foot GZS — sorting area of gizzard СИТ cuticularized region of gizzard H head HP head plate 1 intestine K kidney JE lung LAB labial palp LGS left gastric streak LOC lateral odontophoral cartilage ES larval stomach M mouth MS mesoderm or mesenchyme cells MT mantle MTC mantle cavity MTE mantle edge OE _ oesophagus OER pro-oesophagus blastomeres B and D move apart while A and C approach one another, a deep polar furrow developing along the line of con- tact between them (Fig. 1E); whereas, at the vegetative pole, the blastomeres A and C move apart while B and D touch each other and a polar furrow, comparable but at right angles to that formed at the animal pole, appears between them. The 8rd cleavage (Fig. 1F) is lati- tudinal, but passes nearer to the animal pole so that the egg may be considered moderately telolecithal. It occurs about 5 hours after egg-deposition and results in the formation of 8 blastomeres of 2 dif- ferent sizes. The upper tier of 4 blasto- meres, ог lst quartette of micromeres (la- 14), is considerably smaller than the set of OET post-oesophagus OP operculum ОРГ. opercular lip OS osphradium Р pericardium PB polar bodies PDGR pedal groove PDGL pedal gland РОМ pedal commissure PDP _ pedal cell-plate PHK common primordium for pericardium, heart and kidney ES peristome РТ prototroch RC radular collostyle RGS right gastric streak RI rudimentary intestine RNV renal vestibule RS radular sac RT rectum SD stomodaeum SDB _ buccal region of stomodaeum SDO_ oesophageal region of stomodaeum SH shell (protoconch) SHG shell gland SHGR rudimentary shell gland SLG | salivary gland SOR subradular organ SS style sac STC statocyst TN tentacle U ureter V ventricle УГ. velum VS visceral sac macromeres below (1A-1D). The spindle axis of cleavage soon becomes oriented obliquely to the polar axis of the seg- menting ovum as the micromeres shift slowly and come to lie over the angles formed by the contiguity of the macro- meres below them (Fig. 1G). In other words, the micromeres rotate clockwise through approximately 45% above the macromeres, clearly indicating that the 3rd cleavage is dexiotropic. The 4th cleavage (Fig. 1H) starts about 6 hours after egg-deposition. It is again latitudinal, but anti-clockwise or laeo- tropic and cuts the 4 macromeres into 8 cells of 2 different sizes. The 4 smaller ones constitute the 2nd quartette of micro- meres (2a-2d); the rest are labelled 2A-2D. 128 DEMIAN AND YOUSIF The Ist quartette of micromeres divide about half an hour later (Fig. 11), also laeotropical- ly; thus 4 small cells (la'-1d') are cut off towards the animal pole, the remainder (1a?- 1d?) lie below them, and the 16-cell stage is established. Right after the completion of the 3rd and of 4th cleavage divisions, the dividing cells are yet spherical; between them there is a narrow irregular cleavage cavity. But these cells soon get pressed against one an- other, losing their regular spherical form, and the cavity in between them dis- appears before the commencement of the succeeding cleavage. The 5th cleavage (Fig. 1]) takes place about 7% hours after egg-deposition. At this cleavage, a 3rd quartette of micro- meres (3a-3d) is cut off by a dexiotropic division from the macromeres, the ге- mainder of which are labelled 3A-3D. The 2nd quartette of micromeres divide al- most simultaneously, in a similar dexio- tropic direction, into 2a'-2d' and 2a?-2d?, and the 24-cell stage is thus reached. cleavage cavity appears at this stage nearer to the animal pole and persists throughout subsequent stages as the blastocoel. The following divisions of the macro- and micromeres are rapid, and the regular pattern of the spiral cleavage is soon lost. The dividing cells are pressed against each other after every division, the cell bound- aries become vague, while the egg re- tains its regular spherical form. The blastula is fully developed about 14 hours after oviposition. It is spherical, about 110 y in diameter, and has its cells ar- ranged in a single layer enclosing a rela- tively large segmentation cavity. 2. Gastrulation Gastrulation is mainly epibolic, not em- bolic as described for Pila globosa by Ranjah (1942). It is completed about 22 hours after egg-deposition. Shortly after the formation of the blastula, the embryo becomes slightly flattened at both poles. The smaller micromeres overgrow and en- close the larger yolk-laden macromeres, while the latter simultaneously become elongated and protrude into the segmenta- tion cavity; these will form the future endoderm. A widely open rounded blasto- pore is thus formed at the vegetative pole, but it gradually shifts towards the other pole and simultaneously narrows by the gradual approach of its lateral lips until it completely closes by the end of gastrula- tion. Meanwhile, a narrow irregular space, the archenteron (AT, Fig. 2), makes its appearance in between the dividing mega- meres. Since cell-lineage was not followed up in detail beyond the 24-cell stage, the origin of the mesoderm could not be determined with certainty in the present study. How- ever, there is good indication, derived from repeated preliminary observations on live and sectioned embryos, that the meso- derm in Marisa is teloblastic in origin, as in Pila globosa (Ranjah, 1942) and several other prosobranchs (Raven, 1966). It is most probably derived from micromere 4d which is cut off from macromere 3D during the 6th cleavage, and which later propagates 2 loose strands of small ovoid or polygonal mesoblastic cells, with a densely granular cytoplasm and large spherical nuclei, in the segmentation cavi- ty. The fully formed gastrula (Fig. 2) ovoid in outline. The ectodermal cells (ET) are transparent, range from short cuboi- dal to tall columnar and have a granular and deeply stainable cytoplasm and rela- tively large spherical nuclei. The endo- derm (EN) forms a spheroidal inner mass of cells which are even more varied in form and size. They are opaque, heavily loaded with yolk granules and impart a distinct yellowish colour to the gastrula. 3. General outlines of embryonic develop- ment after gastrulation Development in Marisa cornuarietis is direct, as in most other freshwater gas- tropods. Twelve distinct embryonic stages have been distinguished from the end of gastrulation till hatching. Before going in- to the details of the origin and develop- ment of the different organ systems, it will be expedient to give a brief general out- line of the whole process of embryonic EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 129 o вед SHGR : Fed Se 2 e © “= 5 So alge > - ANP FIG. 2. Sagittal section of the gastrula. FIG. 3. The embryo in Stage I: A, Left lateral view. B, Dorsal view. FIG. 4. Median sagittal section of the embryo in Stage I. FIG. 5. The embryo in Stage II: A, Left lateral view. B, Dorsal view. C, Ventral view. FIG. 6. Median sagittal section of the embryo in Stage II. 130 TABLE Stage IT] \ VI VII VIII IX days days 14 X - Es he days 28 DEMIAN AND YOUSIF Embryonic stages of Marisa cornuarietis 9 34 a 40 5 48 6 56 7 70 9 82 10 90 11 2 Age at eve 30 15-2 0 Dimensions Length Breadth Diagnostic characters ee А 120 160 190 240 300 450 970 630 100 12% 650 670 100 130 160 180 200 300 310 330 450 Bilaterally symmetrical, with distinct prototroch; apical, pedal and anal cell-plates; stomodaeum in early stage of differentiation. Bilaterally symmetrical; with invaginated rudimentary stomodaeum; rudiments of shell gland and ureter in early stage of differentiation; 2 rudimentary aggregates of mesoderm cells differentiated on either side of endodermal sac. Bilaterally symmetrical externally, but asymmetrical internally; with prominent rudimentary foot and visceral sac on lower side; stomodaeal in- vagination communicating with archenteron; rudiments of shell gland and ureter invaginated; a single right rudimentary mesodermal vesicle representing a common primordium for pericardium, heart and kidney. Bilaterally asymmetrical both externally and internally; with shell gland rudiment shifted left of median line; pericardium and kidney differen- tiated from common primordium; rudimentary ureter communicating with rudimentary kidney. Pear-shaped with well-developed velum; cup-shaped rudimentary shell gland opening widely on left side of visceral sac; rudiments of ctenidium and osphradium, and those of cerebral, pedal, pleural and intestinal ganglia in early stage of differentiation; endodermal sac differentiated into larval stomach and rudimentary intestine. Foot cone-shaped; rudimentary shell gland everted and cap-like; rudiments of sorting and cuticularized regions of gizzard differentiated in wall of larval stomach; rudiments of auricle and ventricle differentiated and inter-communicating; ureter U-shaped; rudiments of statocysts in- vaginated, and rudiments of most nerve ganglia delaminated from ec- toderm. Torsion is first noticeable; visceral sac slightly rotated anti-clockwise; foot elongated with flattened creeping sole; statocysts form closed vesicles below ectoderm; reno-pericardial tube developed; rudiments of hepatic vestibule, buccal ganglia and visceral ganglion differentiated. Visceral sac makes an angle of 30° with longitudinal head-foot axis; mantle cavity first noticeable as shallow depression on right dorsolateral side of visceral sac; pericardium, kidney and osphradium displaced to left side; ureter oriented transversely to longitudinal axis of body; style sac and intestine differentiated. Visceral sac makes an angle of 45° with longitudinal axis of head and foot; mantle cavity enlarged and bowl-shaped; ctenidium has 3 ctenidial lamellae and projects, with osphradium, at opening of mantle cavity; oper- culum, tentacles and eye rudiments differentiated; anus first recognized, opening together with renal vestibule in mantle cavity. Torsion completed; visceral sac cone-shaped, with apex pointing downwards; mantle cavity deep, opening widely behind head vesicle; ctenidium and osphradium enclosed within mantle cavity, lung rudiment differentiated between them; about 7 ctenidial lamellae developed; heart chambers beating rhythmically; tentacles stumpy, eyes form closed EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 131 vesicles below ectoderm; 2 rows of teeth developed within radular sac; all nerve commissures and connectives established. Visceral sac showing early signs of spiral coiling, with apex pointing forwards; mantle thin, mantle cavity has assumed definitive form and posi- tion; ctenidium elongated with about 12 ctenidial lamellae; ureter and heart projecting on roof of mantle cavity; velum diminished; foot with well-differentiated operculum, pedal gland and columellar muscle; 5 rows of teeth developed within radular sac; gizzard U-shaped and fully formed; XI 6 16 750 600 intestine long and W-shaped. mm mm ХИ т» 18 1.3 0.9 Minature of adult; head, tentacles, eyes, labial palps and nuchal lobes well-developed; pedal cell-plate has disappeared; visceral sac makes 1% coils; ctenidium stretched far in front of ureter, with about 20 ctenidial lamellae; 6-7 rows of teeth developed within radular sac; oesophageal pouches and anal gland differentiated; lateral odontophoral cartilages, jaws and buccal muscles well-recognizable; rudiments of 2 lobes of digestive gland elongated and approximated to one another at rear of lar- val stomach; aortic ampulla well-differentiated and lodged below pericar- dium; kidney dorso-ventrally flattened and stretched transversely behind ureter; all nerve ganglia at definitive locations. development and to characterize each of the 12 embryonic stages recognized. The distinctive anatomical features of each stage, its dimensions and approximate age (as developed at 2 different temperature ranges of 25-30 and 15-20%C) are sum- marized in Table 1. Stage I (Figs. 3A,B, 4) The embryo is spheroidal, bilaterally symmetrical both externally and т- ternally and about 1204 long. It shows a marked advance over the gastrula stage as evidenced by the development of the pro- totroch and the differentiation of the apical, pedal and anal cell-plates. The prototroch (PT), or preoral ciliated band, shows as a slightly projecting, trans- lucent, circular band located nearer to the upper‘ (dorsal) side. It consists of a double row of large pyramidal cells which carry short cilia on their free edges and present a vacuolated and highly acidophilic cyto- plasm. A few large transparent ectodermal cells on the dorsal surface of the embryo con- stitute the apical cell-plate (APP). These cells are narrower than those of the proto- troch, but they similarly carry short cilia and have a markedly acidophilic, vacuo- lated cytoplasm. Ventrally 2 other groups of more or less similar, large, transparent, ciliated ectodermal cells also become con- spicuous: the anterior pedal and posterior anal cell-plates (PDP and ANP re- spectively). (Terminology after Conklin, 1897, and Ranjah, 1942.) The ectoderm, in a small circular area just below the prototroch, thickens form- ing the rudiment of the stomodaeum (SD). This rudiment is situated just in front of the site of closure of the blasto- pore which has shifted forward to the opposite pole by the end of gastrulation. The endoderm (EN) forms a central spheroidal mass which still encloses a small irregular archentric cavity (AT, Fig. 4); its wall is still more than one cell thick. Stage II (Figs. 5A-C, 6) The embryo is considerably elongated, measures about 160 и in length and starts rotating actively inside the egg capsule with the help of its cilia. The pedal (PDP) and anal (ANP) cell-plates become more prominent as their cells further enlarge. The rudiment of the stomodaeum (SD) deeply invaginates, but does not yet con- ‘The dorso-ventral axis of the embryo at this stage is at right angles to the animal-vegetative polar axis. FIG. FIG. FIG. FIG. DEMIAN AND YOUSIF E ($) $) ay qe A Pe & . The embryo in Stage Ш: A, Left lateral view. В, Dorsal view. С, Ventral view. 8. Median sagittal section of the embryo in Stage III. 9. The embryo in Stage IV: A, Left lateral view. B, Right lateral view. C, Dorsal view. 10. Median sagittal section of the embryo in Stage IV. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 133 nect with the archenteron. The ectoderm, in a small circular area on the posterior side, thickens forming the rudimentary shell gland (SHGR). Another smaller and less conspicuous thickened ectodermal plate is also differentiated to the right side of the anal cell-plate: the rudiment of the renal vestibule and ureter (U). The endodermal sac (EN, Fig. 6) en- larges and assumes an ovoid outline; its cells become somewhat flattened and are arranged in a single layer surrounding a relatively wide archenteron (AT). Two compact masses of mesenchyme cells (MS, Fig. 5A) of unequal size become con- spicuous in the posterior region of the embryo, on both sides of the endodermal sac. The right mass is slightly larger and a little posterior to the left one. The latter will soon disappear, while the former per- sists and represents a common primordium for the pericardium, heart and kidney. Stage Ш (Figs. 7A-C, 8) The embryo is slightly more elongated, bilaterally symmetrical externally but asymmetrical internally, and measures about 190 и in length. It has developed 2 rounded prominences on the ventral side which represent the rudiments of the foot (F, Fig. 7A) and visceral sac (VS). Two new ectodermal cell-plates, the head plates (HP, Figs. 7B, 8), have dif- ferentiated anteriorly, above the level of the prototroch. They consist of densely granular, columnar cells with central spherical nuclei. These cells will later de- velop into the tentacles, eyes and cerebral ganglia. The stomodaeum invagination (SD) deepens further, its cavity communicates with the archenteron (AT, Fig. 8), and the cells in its roof develop short cilia. The anterior opening of the stomodaeum, or mouth (M), is rounded and faces antero- ventrally. The rudimentary shell gland (SHGR) is enlarged and forms а сир- shaped median invagination on the posterior side. The rudiment of the renal vestibule and ureter (U, Fig. 7A) becomes invaginated. The left aggregate of mesoderm cells has disappeared. The right mass, a com- mon rudiment for the pericardium, heart and kidney (PHK, Fig. 7A), enlarges in this stage, shifts a little upwards and hol- lows out, forming an ovoid vesicle with a small central cavity, the coelom. Stage IV (Figs. 9A-C, 10) The embryo measures about 240 и in length. It starts to lose its external sym- metry as the rudimentary shell gland (SHGR) further enlarges and slightly shifts towards the left side. The stomodaeal tube is now roughly divisible into an anterior buccal region (SDB) and a narrower pos- terior oesophageal part (SDO). The rudi- ment of the radular sac (RS, Fig. 10) be- comes noticeable as a small evagination in the floor of the oesophageal region. The endodermal sac (EN) is pear-shaped, with the narrower end pointing postero- ventrally. No clear differentiation of parts is yet visible in this sac. The archenteron (AT) is filled with the albuminous fluid that apparently reaches it through the mouth opening (M). The common rudiment for the peri- cardium, heart and kidney (PHK, Fig. 9B) becomes incompletely divided by a con- striction into 2 parts: a larger and thinner- walled anterior portion that will develop into the pericardium and heart, and a smaller, thicker-walled posterior part that represents the rudiment of the kidney. The invaginated rudiment of the renal vesti- bule and ureter (U) deepens and connects with the cavity of the rudimentary kidney. Stage V (Figs. 11A-D, 12) The embryo has grown pear-shaped with a broader anterior region, and measures about 300 и in length. The foot rudiment (F) juts out more prominently; it tapers ventrally so that its transverse sec- tion is V-shaped. The cells of the pedal cell-plate (PDP) are further enlarged and are now arranged in a median longi- tudinal double row on the lower edge of the foot. The prototroch protrudes more markedly on either side of the head vesicle forming a conspicuous larval velum (VL). DEMIAN AND YOUSIF вх &- ADAL A a HS За # Or om BIS MO) Paper’ CCS js y) Ta m № KDE 13 ls y = u > on SI wa SH Se | | N, PRET N n ¢ us LE FIG. 11. The embryo in Stage V: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. FIG. 12. Sagittal section of the embryo in Stage V passing to the left of the median line. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 135 The rudimentary shell gland (SHGR) is considerably enlarged and entirely shifted to the left side. It forms a large, deep, cup- shaped depression that is lined with a thin cuticular secretion, the protoconch or lar- val shell (SH, Fig. 12). The cells found at the periphery of this depression thicken in subsequent stages and form the shell gland of the adult. Rudiments of the ctenidium (CN) and osphradium (OS, Fig. 11B) differentiate as thickened oval areas of the ectoderm on the right dorso-lateral wall of the visceral sac. Rudiments of the cerebral, pedal, pleural and intestinal ganglia, as well as the rudiments of the statocysts (STC), all also start to differentiate at this stage as small ectodermal thickenings. A tubular evagination develops postero- ventrally from the rear of the endodermal sac which thus becomes differentiated into an anterior larval stomach (LS, Fig. 11A) and a posterior rudimentary intestine (RI). The former is ovoid, much larger, thicker- walled and has a wider lumen than the latter. It presumably serves in absorbing and digesting the albuminous fluid of the egg throughout embryonic life. Only small parts of it will contribute to the formation of the adult s stomach; the rest will be re- placed by the digestive gland a short while after hatching. The rudimentary intestine is short, tubular, points downwards and ends blindly. The rudiment of the pericardium and heart (P, Fig. 11B,D) enlarges further and shifts backwards behind the larval stomach. The rudimentary kidney (K, Fig. 11B) acquires a tubular form and lies be- hind the pericardial rudiment, with which it still widely communicates. Rudiments of several blood vessels and sinuses start to differentiate at this stage as irregular spaces or as parts of the segmentation cavity surrounded by mesenchyme cells. Stage VI(Figs. 13A-D, 14) A considerable growth in length has taken place so that the embryo is 450 u long. The foot (F) has further enlarged and assumed a conical form; its antero-ventral edge starts flattening, thus marking the beginning of the formation of the creeping sole. The visceral sac (VS) is also much en- larged and rounded in outline, but some- what laterally compressed. The skin around the mouth forms a thickened rudi- mentary lip in the form of an incomplete ring, and the radular sac evagination (RS) enlarges. The rudimentary shell gland is further enlarged and thickened at the periphery, while its central part, formerly concave, thins and bulges outward so that the whole rudiment assumes a cap-like shape. The thickened periphery (SHG, Fig. 13A) represents the actual rudiment of the adult’s shell gland, while the thin central part will subsequently form the skin of the visceral mass and will also contribute to the formation of the mantle fold. Close around the thickened periphery, the ecto- derm is slightly raised so as to form a pro- jecting circular fold (MTE) which will form the mantle edge of the adult. Rudiments of the cerebral, pedal, pleural and intestinal ganglia become de- laminated from the ectodermal layer and form compact cellular masses below it, and rudiments of the statocysts (STC) become invaginated. The larval stomach (LS) has grown con- siderably in size and its cells are much en- larged (Fig. 14). A narrow longitudinal streak, referred to here as the right gastric streak (RGS, Fig. 13B), makes its appear- ance on the right dorso-lateral side of the larval stomach. The cells in this streak will develop into the cuticularized portion of the adults gizzard. The cells in a small oval area on the left wall of the larval stomach also start differentiating at this stage, eventually developing into the sort- ing area of the adult's gizzard. The rudi- mentary intestine (RI) is sharply bent downwards and still ends blindly. The rudiment of the pericardium and heart elongates in the antero-posterior direction; its wall becomes deeply in- vaginated at 2 points, 1 on the left side and the other on the postero-dorsal side. The 2 chambers thus formed communicate and represent the ventricle (V) and auricle (A) respectively (Fig. 13B). The opening be- 136 DEMIAN AND YOUSIF ER a CAE age ES q RDA y FIG. 13. The embryo in Stage VI: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. FIG. 14. Median sagittal section of the embryo in State VI. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 137 FIG. 15. The embryo in Stage VII: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. FIG. 16. The embryo in Stage VIII: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. 138 DEMIAN AND YOUSIF tween the pericardial cavity and the rudi- mentary kidney (К) becomes simul- taneously more constricted (Fig. 14). The posterior portion of the kidney has dilated and shifted up and to the left towards the median line. The rudimentary ureter (U, Fig. 13B,C) is more elongated and bent in the shape of a U with 2 unequal arms. The shorter dorsal arm communicates anterior- ly with the rudimentary kidney, while the ventral arm opens into the renal vestibule (RNV). The 2 arms are thick-walled; they communicate by a cross connection in the form of a thin double lamella. The spaces between the different inter- nal organs are now almost completely occupied by scattered stellate mesen- chyme cells (MS, Fig. 14). Stage УП (Fig. 15A-D) Torsion begins as the embryo reaches this stage, after about 82 hours of incuba- tion at 25-30°C, and as it attains a length of about 570 и. The process of torsion takes about 2 days, i.e. until the embryo passes through Stage X. It is apparently due to differential growth of the 2 sides of the embryo, since no distinct muscles have as yet been developed. In this stage, the foot (F) appears more elongated and its apex points backwards, making an acute angle with the longi- tudinal axis of the body. It has developed a broad flattened sole which is now used for creeping on the inner surface of the egg capsule. The rudiment of the adult's shell gland (SHG) is further enlarged. The visceral sac (VS) also enlarges and is more laterally compressed so that it assumes the form of a thick circular disc. The first sign of torsion is manifest by the position this sac now assumes relative to head and foot. It is no longer parallel to the longitudinal axis of these organs, but has started rotating anti- clockwise: its postero-ventral part has slightly moved to the right and upwards, while its antero-dorsal part has shifted to the left and downwards. The anal cell- plate (ANP) is consequently displaced to the right side of the median line. The rudiments of the ctenidium (CN) and osphradium (OS) are further thickened and shifted forwards (Fig. 15B). Rudiments of the buccal ganglia and the visceral ganglion become differentiated, and each pedal ganglion fuses with the pleural ganglion of its respective side. The 2 intestinal ganglia appear rotated anti- clockwise around the larval stomach; the left ganglion thus becoming sub-intestinal and the right one supra-intestinal. Nerve commissures and connectives start to dif- ferentiate as thin extensions from the nerve ganglia. The statocysts (STC, Fig. 15B) separate from the ectoderm and form 2 closed vesicles below it. The larval stomach (LS) enlarges and extends further backwards in the lumen of the visceral sac. A 2nd longitudinal streak, referred to here as the left gastric streak (LGS, Fig. 15A), is seen running along the entire length of the left ventro-lateral side of the larval stomach. The cells in this streak will develop into the hepatic vesti- bule of the adult. The still closed tip of the rudimentary intestine (RI) is shifted to the right as a result of the slight rotation of the visceral sac. The heart chambers within the peri- cardial cavity start to show some irregular contractions. The kidney (K) becomes ovoid and communicates with the peri- cardial cavity through a narrow reno-peri- cardial tube. The 2 arms of the U-shaped ureter (U) come to lie so close to each other that the space between them is re- duced to a mere furrow. The afferent and efferent ureteral veins, which supply and drain the ureter, become conspicuous at this stage. The renal vestibule (RNV) shifts a little upwards, thus coming to open near the center of the right face of the visceral sac. Stage VIII (Fig. 16A-D) The embryo appears more asym- metrical due to further torsion and measures about 630 и in length. The foot is now well-demarkated from both the head and visceral sac. The sole assumes a triangular outline. А thickened circular area projects on the postero-dorsal side of the foot: the rudiment of the opercular lip EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 139 (OPL, Fig. 16A), which will later secrete the operculum. Some glandular cells appear within the foot, marking the begin- ning of differentiation of the pedal gland. The visceral sac is more twisted and lies at an angle of 30° to the longitudinal axis of the head and foot. As a result of this twisting, a broad shallow depression forms on the right side of the visceral sac near its dorsal edge, marking the beginning of de- velopment of the mantle cavity (MTC, Fig. 16B). As torsion proceeds during further development, the rudimentary shell gland enlarges gradually until it covers the whole of the visceral sac, then prolongs forward to form the mantle skirt. In other words, the skin now found on the left side of the visceral sac, which is covered by the shell (SH) and encircled by the adults shell gland (SHG), will grow enormously so as to form the whole of the outer covering of the future visceral mass, as well as the outer epithelium of the mantle fold in front. Meanwhile, the mantle edge thickens, the mantle cavity enlarges, and the skin which now covers the right side of the visceral sac is gradually enfolded in- side the deepening mantle cavity, to form its inner lining as well as the inner epithelium of the mantle fold. The ctenidium (CN) and osphradium (OS), which have already been differentiated on this skin, on the right dorso-lateral side of the visceral sac, will accordingly pass in- side the mantle cavity in subsequent stages. In Stage VIII, and as a result of torsion, the kidney (K, Fig. 16A,B) comes to lie postero-dorsally to the pericardium (P), and both become displaced leftwards. The aperture of the renal vestibule (RNV, Fig. 16B) now points forwards; the ureter (U, Fig. 16C,D) lies almost transversely to the longitudinal axis of the body; it takes from the right side of the kidney. The rudimentary intestine becomes dif- ferentiated into a proximal funnel-shaped style sac (SS, Fig. 16A) and a distal tubu- lar intestine. All nerve ganglia are con- siderably enlarged, and the sub-intestinal ganglion shifts forwards close to the right pleuro-pedal ganglionic mass. Stage IX (Figs. 17A-D, 18) The embryo is slightly more elongated, measuring about 650 и in length. Torsion is more pronounced. The visceral sac now lies at an angle of 45° to the longitudinal axis of the head and foot. The foot (F) assumes its definitive shape and position; the opercular lip (OPL) be- comes more prominent and secretes a thin cuticular covering, the operculum (OP, Fig. 18). The tentacles (TN) develop on the head plates as 2 small conical pro- tuberances, and the eyes become dif- ferentiated on the same plates as 2 slightly invaginated circular discs lying close be- hind the tentacles. The deepening mantle cavity (MTC, Fig. 17B) grows bowl-shaped and is thus better recognized. The mantle opening is semi-lunar and the mantle edge (MTE) is considerably thickened. The ctenidium (CN) and osphradium (OS) become en- closed in the mantle cavity, and now hang down from its roof close behind the mantle edge. The ctenidium shows 3 transverse epithelial folds, the first 3 ctenidial lamel- lae to develop. The tubular radular sac evagination (RS, Figs. 17A, 18) becomes much elongated and S-shaped. Rudiments of the odon- tophoral cartilages and some buccal mus- cles differentiate as 2 symmetrical aggre- gates of mesenchyme cells below the radu- lar sac, and the salivary glands start to develop as 2 small tubular evaginations from the roof of the buccal region of the stomodaeum. The rudiments of the adult's digestive gland are first noticeable in this stage as 2 narrow circular bands located close above and below the rudiment of the sorting area of the gizzard (GZS), which has already differentiated in Stage VI on the left wall of the larval stomach (LS). The style sac (SS, Fig. 17A,D) is further enlarged and shifted to the left due to the enlargement of the larval stomach. The intestine (1) is much elongated; leading from the style sac at the rear of the larval stomach, it bends and runs anteriorly along its right side. It 140 DEMIAN AND YOUSIF FIG. 17. The embryo in Stage IX: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. FIG. 18. Median sagittal section of the embryo in Stage IX. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 14] SHG FIG. 19. The embryo in Stage X: A, Left lateral view. B, Right lateral view. C, Dorsal view. D, Ventral view. FIG. 20. Median sagittal section of the embryo in Stage X. 142 DEMIAN AND YOUSIF now opens in the mantle cavity by the anus, a new perforation first seen in this stage. The ventricle (V, Fig. 17A) is pear- shaped, and there appear irregular in- ternal folds projecting into its lumen. The opening between the auricle and ventricle has become much constricted. The rudi- ment of the aortic ampulla differentiates as a compact aggregate of mesoderm cells lying below the pericardium. The opening of the renal vestibule (RNV, Fig. 18) is now pushed inside the mantle cavity, and the greater part of the U-shaped ureter (U) lies in front of the kidney (K, Fig. 17C). Stage X (Figs. 19A-D, 20) Torsion is completed at this stage of de- velopment, when the embryo is about 670 и long. The tentacles (TN) are further elongated and finger-like. The eyes (E) form 2 ovoid closed vesicles below the ectoderm. The opercular lip (OPL) is more clearly marked off from the foot, the operculum (OP) more distinct, and the columellar muscle (CML, Fig. 20) is dif- ferentiated within the substance of the foot. The visceral sac is cone-shaped, with a downward pointing apex, and is entirely covered by a thin yellowish shell (SH). The mantle (MT) has grown to the fore, and the ctenidium (CN) and osphradium (OS) have been engulfed inside the mantle cavity and are no longer visible externally. The ctenidium has further enlarged, is J- shaped and presents about 7 transverse ctenidial lamellae. The lung (L, Fig. 19C) starts to differentiate at this stage as a thickened concave area of the inner epithelium of the mantle, lying between the ctenidium and osphradium. Two transverse rows of radular teeth are now visible within the distal end of the radular sac (RS, Fig. 20) The rudi- mentary salivary glands (SLG, Fig. 19A) are elongated and extend on either side of the oesophagus (OE). As the anterior part of the larval stomach (LS) starts to diminish in size, the opening of the oesophagus into it shifts to the rear. The rudiments of the anterior and posterior lobes (DGP, Fig. 20) of the digestive gland enlarge at the expense of the epithelium in the wall of the larval stomach. The heart is now oriented antero- posteriorly (Fig. 19A), with the auricle (A) lying in front of and a little dorsal to the ventricle (V); both chambers beat rhyth- mically. The kidney (K) is further en- larged, and the ureter (U, Figs. 19B,C, 20) extends along the mantle skirt parallel with the intestine (1) and ctenidium (CN). It connects with the kidney through a short tube lying a little in front of the opening of the ureter into the renal vesti- bule. All nerve commissures and connec- tives are now established. Stage XI (Figs. 21A-C, 23) The embryo is about 750 u long. The velum has diminished considerably in size. The head (H) begins to acquire its definitive form. The tentacles (TN) are further elongated and the eye vesicles (E) appear enlarged and are carried on 2 short ectodermal projections, the eye stalks. A retina and a lens are now differentiated in each eye. The opening of the pedal gland (PDGR) is noticeable as a transverse slit running across the anterior edge of the foot. The operculum (OP), opercular lip (OPL) and columellar muscle (CML, Fig. 23) are all well-recognizable. The stato- cysts (STS) become spheroidal, shift from their original locations to lie on either side of the foot, and a few statoconi appear in- side them. The mantle (MT) has become thinner and is prolonged anteriorly, forming a con- tinuous cloak around the body, behind the head. The visceral mass is also much en- larged and starts to show signs of spiral coiling as its apex runs forwards and a little to the right. The ctenidium (CN) is more elongated and shows about 12 ctenidial leaflets. It has shifted forwards along with the forward extension of the mantle so that it comes to lie in front of the heart, and ex- tends obliquely along the mantle (Fig. 21A,C). The osphradium (OS) also shifts forwards and presents 2 small folds on its free surface. The rudiment of the lung (L, Fig. 21C) becomes further invaginated. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 143 FIG. 21. The embryo in Stage XI: A, Left lateral view. В, Right lateral view. С, Dorsal view. FIG. 22. The embryo in Stage XII: A, Left lateral view. В, Dorsal view. 144 DEMIAN AND YOUSIF 0.1т т ES K AD ES 2 Sy a) E E В A eine »] А A | e & А >, Ci a RT AS Later NS e) DGP FIG. 23. Median sagittal section of the embryo in Stage XI. FIG. 24. Median sagittal section of the embryo in Stage VII. EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 145 The pallial fold or epitaenia starts to de- velop as a small epithelial fold projecting horizontally across the right posterior cor- ner of the floor of the mantle cavity. Five transverse rows of teeth are now conspicuous inside the radular sac (RS, Fig. 23), and the subradular organ (SOR) starts differentiating on the floor of the buccal cavity. The gizzard ( GZT, GZS, Fig. 21A) becomes fully formed and assumes its characteristic U-shape. The intestine (1) is further elongated, W- shaped; the anus opens at the right an- terior end of the mantle cavity. The heart now lies in front of the style sac (SS), embedded in the left posterior corner of the roof of the mantle cavity. The aortic trunk, aortic ampulla and cephalic aorta as well as the cephalopedal and vis- ceral haemocoelic sinuses are well- established. The kidney (K, Fig. 21C) has grown into a spacious chamber which lies to the right side of and behind the heart, and a few inner folds project from its roof. The afferent and efferent renal veins supplying the kidney are also well- differentiated. The ureter (U) has become almost as long as the ctenidium and runs obliquely along the roof of the mantle cavity. The renal vestibule (RNV) assumes its definitive position, opening at the right posterior corner of the mantle cavity. The opening of the ureter into the renal vestibule lies behind and to the right side of the short tubular passage connecting the ureter with the kidney. Stage XII (Figs. 22A,B, 24) The embryo is now almost a miniature of the adult. It measures about 1.3 mm in length. It has a somewhat dorso-ventrally compressed head (H), with 2 short conical labial palps (LAB) projecting anteriorly on either side of the ventral mouth opening. The right and left nuchal lobes are also de- veloped as 2 projecting ectodermal ridges on either side of the head. The eyes (E) have developed dense black pigment, and the inner and outer cornea have become differentiated in each. The pedal cell-plate has disappeared, while the anal cell-plate still exists. The visceral sac is further coiled, showing about 1% spiral coils. Six to seven rows of teeth are developed inside the radular sac (RS, Fig. 24). The jaws, lateral odontophoral cartilages (LOC), and most of the buccal muscles are well-recognizable. The oesophageal pouches start to differentiate in this stage as 2 lateral tubular evaginations from the roof of the buccal mass. The anterior portion of the larval stomach, formerly within the head vesicle, has disappeared. The oesophagus con- sequently is much elongated. It opens pos- teriorly on the left ventro-lateral side of the gizzard. The 3 main regions of the oesophagus, namely the pro-oesophagus (OER), crop (COP) and post-oesophagus (OET), are histologically differentiated (Fig. 24). The posterior portion of the lar- val stomach (LS), however, is still large and fills the greater part of the visceral sac. The intestine (1) has greatly increased in length, and the anal gland has begun to differentiate as a narrow tubular evagina- tion from its distalmost part, or rectum (RT, Fig. 22B). The rudiments of the an- terior (DGA, Fig. 22A,B) and posterior (DGP, Figs. 22A, 24) lobes of the diges- tive gland are also further enlarged and meet behind the gizzard. The aortic trunk and aortic ampulla (AM, Fig. 22A) are now lodged below the pericardium. The kidney (K) becomes dorso-ventrally flattened, extending almost transversely behind the ureter (U); numerous inner folds appear projecting from its roof. The ctenidium (CN) stretches far in front of the ureter and pre- sents about 20 ctenidial lamellae. How- ever, the greater portion of this organ still lies to the left side of the median line. No further changes take place in the lung rudiment (L) until the embryo hatches. All nerve ganglia have now attained their definitive shapes and positions. The osphradium has developed much more and shows 4 transverse folds on its free surface. The embryo is now capable of re- tracting within its shell, and the egg albu- men is almost completely utilized. Rudi- ments of the genitalia are not yet recogniz- 146 DEMIAN AND YOUSIF able, and no new structures appear until the embryo hatches. The egg increases in average diameter from 2.5 to 4.8 mm during this embryonic life. DISCUSSION Early cleavage divisions in Marisa cor- nuarietis are basically similar to those de- scribed by Scott (1934) in Ampullaria canaliculata and by Ranjah (1942) in Pila globosa in that the first 2 divisions are equal and the 3rd cleavage is unequal. The relative inequality in the size of the re- sulting micro- and macromeres is com- parable to that noted in P. globosa, while a less marked difference between the size of the corresponding micro- and macro- meres seems to exist in the case of Ampul- laria canaliculata, the eggs of which may have a relatively smaller amount of yolk. As is the general rule in dextral gas- tropods, the 3rd cleavage is dexiotropic, and subsequent cleavages follow according to the law of alternating cleavages. Sinis- trality is associated with reversed 3rd and subsequent cleavages such as have been observed in Physa (Crampton, 1894; Wierzejski, 1905) and Planorbis (Rabl, 1879: Holmes, 1900). Narrow recurrent cleavage cavities, which probably serve as a mechanism for osmotic regulation (Raven, 1966), appear between the dividing blastomeres following the 3rd and 4th cleavage divisions, but they soon dis- appear. It is the cleavage cavity that develops during the 5th cleavage that per- sists as the blastocoel in Marisa. Gastrulation was found to be epibolic, as in the majority of gastropods with yolk- rich eggs (Raven, 1966), and not embolic as described in Pila globosa by Ranjah (1942). Gastrulation occurs by embolic in- vagination in certain prosobranchs with microlecithal eggs such as Paludina (= Viviparus) (Erlanger, 1891; Otto & Ténniges, 1906), while in other prosobranchs, such as Crepidula (Conklin, 1897), Littorina (Delsman, 1914) and Patella (Smith, 1935), epiboly and emboly seem to be of equal importance in gas- trulation. While there is a general agreement in the literature as to the origin of the ecto- derm and endoderm in the Pro- sobranchia, some dispute still exists as re- gards the origin and development of the mesoderm, of which extensive reviews are given by Ranjah (1942), Fretter & Graham (1962), Raven (1966) and Hyman (1967). Although the details of cell-lineage were not followed up in Marisa beyond the 24- cell stage, preliminary observations made during the present study would indicate that the mesoderm in this snail is most probably teloblastic, or entirely derived from micromere 4d, as in Pila globosa (Ranjah, 1942). Although Smith (1935), Crofts (1938) and Creek (1951) have claimed that the mesoderm in Patella, Haliotis and Pomatias, respectively, is not derived from micromere 4d, but from macromere 4D, this contention, according, to Raven (1966), can hardly be accepted as yet. Development beyond the gastrula stage follows the general pattern described in other ampullariids (Semper, 1862; Scott, 1934; Ranjah, 1942). The 12 embryonic stages recognized here are readily com- parable to those described by Ranjah (1942) for Pila globosa, yet the present observations are not in complete agree- ment with those made by that author. Apart from some minor differences as regards the differentiation of certain organs in relation to age, there are other more important differences concerning the origin and development of a number of organs. Ranjah states that, in P. globosa: a) the blastopore persists after gastrulation and forms the anus; b) the mantle cavity develops at a very early stage as a mid- ventral ectodermal invagination; c) the pericardium develops from 2 symmetrical mesodermal masses which later approach each other and shift together to the right side of the body; d) the kidney arises by 2 rudiments from the pericardial epithelium; e) the ureter develops as an in- vagination from the lining of the mantle cavity; f) the rudimentary stomach trans- forms early into the adults digestive gland; g) the mantle skirt develops as 2 ectodermal folds which approach one EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT 147 another at a late stage and meet to form the roof of the mantle cavity; and h) the statocysts develop relatively late. Similar observations were made by Fernando (1931) on the origin and development of the pericardium, heart, kidney, ureter and mantle cavity in Ampullaria gigas. These observations conflict with the present fin- dings in Marisa cornuarietis. The dif- ferences between these earlier accounts and the present observations will be dis- cussed in detail in the relevant sections of the present series of studies. The average period for embryonic development in M. cornuarietis was 8 days at a temperature range of 25-30°C, and 20 days at 15-20°C. For other ampul- lariids, the corresponding incubation period was reported as less than 14 days for Ampullaria polita (Semper, 1862), 2-6 weeks for A. gigas (Kohler, 1905), 28 days in the natural environment in the shade for A. canaliculata (Scott, 1934), and 10-14 days at 90-100°F or 3 weeks at 70-80°F for Pila globosa (Ranjah, 1942). ACKNOWLEDGEMENTS The authors gratefully acknowledge the valuable contribution of Dr. K. Mansour, Emeritus Professor of Zoology, Faculty of Science, Ain Shams University, Cairo, in the supervision of the present series of studies, his enthusiastic support and help- ful criticism. The writers are also highly in- debted to Dr. B. Hubendick, Director of the Natural History Museum in Gothenberg, Sweden, for directing this re- search project and for his continuous help during the course of the work. LITERATURE, CITED BROOKS, W.K. & McGLONE, B., 1908, The origin of the lung of Ampullaria. Carnegie Inst. Publ., 102: 95-104. CONKLIN, E.G., 1897, The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gastropods. J. Morphol., 13: 1-226. CRAMPTON, H.E., 1894, Reversal of cleavage in a sinistral gastropod. Ann. N.Y. Acad. Aci., 8: 167-170. CREEK, G.A., 1951, The reproductive system and embryology of the snail Pomatias elegans (Muller). Proc. zool. Soc. Lond., 121: 599-640. CROFTS, D.R., 1938, The development of Haliotis tuberculata, with special reference to organogenesis during torsion. Phil. Trans. Roy. Soc. Lond., В, 228:219-268. DELSMAN, H.C., 1914, Entwicklungs- geschichte von Littorina obtusata. Tijdschr. ned. dierk. Ver., 13: 170-340. DEMIAN, E.S. & IBRAHIM, A.M., 1970/71, The egg mass, egg laying and mating behaviour of the snail Marisa cornuarietis (L.). Bull. zool. Soc. Egypt, 23: 1-12. ERLANGER, R. von, 1891, Zur Entwicklung von Paludina vivipara. 1. Morph. Jb., 17: 337-379. FERNANDO, W., 1931, The development of the kidney in Ampullaria (Pila) gigas. Proc. 2001. Soc. Lond., 62: 745-750. FRETTER, V. & GRAHAM, A., 1962, British prosobranch molluscs, their func- tional anatomy and ecology. Ray Soc., Lond., 755 p. GATENBY, J.B. & BEAMS, H.W., 1950, The microtomist s vade-mecum. Churchill Ltd., Lond., 118 Ed.,755'p. GRENACHER, H., 1879, Einige Notizen zur Tinctionstechnik besonders zur Kernfär- bung. Arch. mikrosk. Anat., 16: 463-471. HOLMES, 5.]., 1900, The early devel- opment of Planorbis. J. Morphol., 16: 369- 458. HYMAN, L.H., 1967, The Invertebrates, Vol. VI, Mollusca I. McGraw Hill, Inc., 792 p. KÖHLER, W., 1905, Über Laichgeschäft und Geschlechtsunterschiede bei Ampullaria gigas Spix. Blätt. Aquar. Terrar.-Kunde, 16: 438-439. NAGARAJA, S., 1943, A note on the devel- opment of the alimentary canal in Pila. Proc. Indian sci. Congr., 30: 59. OTTO, H. & TÖNNIGES, C., 1906, Untersuchungen über die Entwicklung von Paludina vivipara. Zt. wiss. Zool., 80: 411- 514. RABL, C., 1879, Uber die Entwicklung der Tellerschnecke. Morph. Jb., 5: 562-660. RAJA, S.N., 1943, A preliminary account of the development and disintegration of the shell gland in Pila globosa. Proc. Indian sci. Congr., 29: 154. RANJAH, A.R., 1942, The embryology of the Indian apple-snail, Pila globosa (Swainson) (Mollusca, Gastropoda). Rec. Indian Mus., 44: 217-322. RAVEN, C.P., 1966, Morphogenesis: The 148 DEMIAN AND YOUSIF analysis of molluscan development. Pergamon Press, 2nd Ed., 365 p. RYDER, J.A., 1889, Notes on the development of Ampullaria depressa Say. Amer. Natur., 23: 735-737. SCOTT, M.I.H., 1934, Sobre el desarrollo embrionario de Ampullaria canaliculata. Rev. Mus. La Plata, 34: 373-385. geschichte der Ampullaria polita Deshayes. Naturkund. Verh. provinc. Kunsten. Wetensch., Utrecht, 1: 1-20. SMITH, F.C.W., 1935, The development of Patella vulgata. Phil. Trans. Roy. Soc. Lond., B, 225: 95-125. WIERZEJSKI, A., 1905, Embryologie von Physa fontinalis L. Zt. wiss. Zool., 83: 502- SEMPER, Es 1862, Entwicklungs- 706. ZUSAMMENFASSUNG EMBRYONALENTWICKLUNG UND ORGANOGENESE BEl DER SCHNECKE MARISA CORNUARIETIS (MESOGASTROPODS: AMPULLARIIDAE) I. ALLGEMEINE GRUNDZUGE DER ENTWICKLUNG E. S. Demian und F. Yousif Die vorliegende Serie embryologischer Untersuchungen schliesst an die grundlegenden morphologischen, biologischen und ökologischen Studien an, die zur Zeit uber die Wasserschnecke Marisa cornuarietis (Linnaeus), durchgeführt werden. Die Art ist möglicherweise wichtig für die biologische Kontrolle der Schistosoma-Zwischenwirte. Dieser Teil behandelt die ersten Zellteilungen, Gastrulation und allgemeine Grundzuge der Embryogenese bei Marisa. Das Ei unterliegt der Spiralfurchung bis zur Erreichung des 24-Zellen-Stadiums. Die ersten zwei Teilungen erfolgen zu gleichen Teilen, die dritte ist ungleich und dexiotrop. Die Gastrulation ist epibolisch, und der Blastoporus schliebt sich am Ende des Prozesses. Die Embryogenese dauert 8 Tage bei 25-30°C und 20 Tage bei 15-20°C. Die Blastula entwickelt sich vollständig innerhalb 14 Stunden, und die Gastrulation ist in 22 Stunden bei den obigen Temperaturen beendet. Die Torsion erfolgt durch das verschiedene Wachstum der beiden Seiten des Embryos; sie beginnt 3% Tage nach Eiablage und dauert etwa 2 Tage. Zwölf verschiedene Stufen der Embryonalentwicklung nach der Gastrulation werden unterschieden. Alter, Masse und wesentliche anatomische Merkmale jeder dieser Entwicklungsstufen werden gegeben, dazu ein Überblick uber die Entwicklung der verschiedenen Organsysteme, ausgenommen das Genitalsystem, das sich hauptsächlich nach dem Schlüpfen entwickelt. Die Betunde weichen teilweise von früheren Berichten über verwandte Ampullariiden ab, besonders in bezug auf Ursprung und Entwicklung des Mantels, der Mantelhohle, des Pericardiums, des Herzens, der Niere, des Ureters, des Nierenvorhofes und der Verdauungsdrüse. HZ: RESUME DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGENESE CHEZ MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) I. ESQUISSES GENERALES DU DEVELOPPEMENT E.S. Demian et F. Yousif La présente série d investigations embryologiques est une extension aux études fondamentales qui progressent actuellement sur la morphologie, la biologie et l'écologie du gastropode aquatique Marisa cornuarietis (L.). Cette espece a une importance potentielle dans le controle biologique des mollusques vecteurs de la bilharziose. La EMBRYOLOGY OF MARISA. I. GENERAL DEVELOPMENT présente partie envisage la segmentation, la gastrulation et les grandes lignes de l'embryologie de Marisa. Les oeufs subissent une segmentation totale et spirale, qui a été suivie jusqu au stade 24-cellules. Les 2 premiéres divisions sont egales; la 3e est inégale et dexiotropique. La gastrulation se fait par épibolie et le blastopore se bouche à la fin de ce processus. L'embryogenèse dure 8 jours à 25-30°C et 20 jours à 15-20°C. La blastula est complétement développée en 14 heures et la gastrulation terminée en 22 heures a 25-30°C. La torsion s'établit par suite d'une croissance différentielle entre les 2 côtés de l'embryon; elle débute environ 3 jours et demi après la ponte et dure pendant environ 2 jours. On a distingué 12 stades embryonnaires après la gastrulation. La durée, les dimensions et les caractères anatomiques distinctifs de chacun de ces stades embryonnaires sont décrits ainsi que l’esquisse du développement de chaque appareil, à l'exception de l'appareil reproducteur qui se développe principalement après l'eclosion. Les résultats sont partiellement différents des précédents rapports établis sur des Ampallariides voisins, en particulier en ce qui concerne le manteau, la cavité palleale, le péricarde, le coeur, le rein, l'uretére, le vestibule rénal et la glande digestive. ALE: RESUMEN DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) I. DESARROLLO GENERAL E. S. Demian y F. Jousif Esta serie de investigaciones embriológicas es una extensión de los estudios básicos- morfológicos, biológicos y ecológicos-que se estan realizando sobre el gastrópodo acuatico Marisa cornuarietis (Linnaeus), de importanica potencial en el control biologico de los caracoles transmisores de Schistosoma. Esta primera parte trata de la división tem- prana, gastrulación y aspectos generales de la embriogenesis. El huevo experimenta una division celular espiral que se continúa hasta la 24-célula. Las primeras dos divisiones son iguales; la tercera es desigual y dexiotropica. La gastrulación es epibólica y el blastoforo se cierra al terminar el proceso. La embriogenesis tarda 8 días a 25-30°C y 20 días a 15-30°C. La blastula se desarrolla completamente en 14 horas y la gastrulación se completa en 22 horas a las mismas temperaturas. La torsión se produce a través del crecimiento diferencial de los dos lados del embrión: empieza después de tres días y medio de la ovoposición y dura dos días. Se distinguieron estados embrionarios diferentes después de la gastrulación. La edad, dimensiones, y aspectos anatómicos diferenciales de cada uno se dan conjun- tamente con las líneas generales de desarrollo en los varios sistemas organicos. Los resultados obtenidos en la investigación difieren en parte con los conocidos para otros ampularidos, particularmente en los orígenes y desarrollo del manto y cavidad paleal, pericardio, corazón, riñón, uretra, vestibulo renal y glándula digestiva. JE 149 | 0 DEMIAN AND YOUSIF ABCTPAKT ЭМБРИОЛОГИЧЕСКОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS (MESOGASTROPODA, AMPULLARIIDAE) 1. ОБЩЕЕ РАЗВИТИЕ Э.С. ДИМИЭН, ©. ЮЗИФ Настоящая серия эмбриологических работ представляет собой развитие основных морфологических и экологических исследований по моллюскам - гастроподам Marisa cornuarietis (L.), имеющим большое потенциальное значение для биологического контроля над моллюсками-переносчиками шистозомиазиса. Эта часть работы касается ранних стадий дробления, гаструляции и общего эмбриогенеза у Marisa. Яйцо проходит полное спиральное дробление, которое прослеживается до стадии 24 клеток. Первые два деления - равные, 3-e - неравное и декситропическое. Гаструляция эпиболическая, бластопор замыкается в конце этого процесса. При температуре 25-30°C эмбриогенез занимает 8 дней, а при 15-2096 - 20 дней. Бластула, полностью развивается за 14 часов, гаструляция завершается за 22 часа (при указанных выше температурах). Торсия происходит во время ростовой дифференциации с обеих сторон эмбриона, начинается примерно через 3.5 дня после откладки яиц и длится около 2 дней. Во время эмбриогенеза после гаструляции различаются 12 различных стадий развития. Возраст, размеры и отдельные анатомические черты каждой из этих стадий рассматриваютея вместе с общим развитием систем различных органов, за исключением половой системы, которая развивается, главным образом, после вылупления. Обнаруженные факты частично расходятся с ранее известными для родственных Форм моллюсков Ampullariidae, особенно с точки зрения происхождения и развития мантии, мантийной полости, перикардия, сердца, почек, уретры, почечной вестибулы и пищеварительной железы. Z.A.F. MALACOLOGIA, 1973, 12(1): 151-174 EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) Il. DEVELOPMENT OF THE ALIMENTARY SYSTEM! Emile S. Demian? and Fouad Yousif? ABSTRACT The alimentary system of Marisa cornuarietis (Linnaeus) comprises: a) an ectodermal stomodaeum from which the radular sac, oesophageal pouches and salivary glands are developed, and b) an endodermal mesenteron differentiated into a gizzard, digestive gland, style sac and intestine. The stomodaeum develops early as an ectodermal invagination that later opens into the endodermal sac, then differentiates into an anterior buccal region and a posterior oesophageal one. The mouth is a new perforation, arising close to the site of blastopore closure. The radular sac develops as a mid-ventral evagination from the buccal region of the stomodaeum. The radular teeth are secreted by successive transverse bands of odontocytes, which are produced by cell proliferation from a mass of odontoblasts located at the distal end of the radular sac, and are continuously added to the subradular epithelium. Successive bands of odontocytes are separated by transverse bands of weakly secretory cells which produce the radular membrane. The supraradular epithelium is also developed by cell proliferation from a mass of cells located in front of the odontoblasts, the supraradular plug. It contributes to the formation and shaping of the radular teeth. The jaws are secreted shortly before hatching within a differentiated mandibular region of the buccal cavity. The salivary glands and oesophageal pouches develop relatively late as tubular evaginations from the roofing epithelium of the buccal mass. The entire oesophagus is ectodermal in origin. It starts differentiating into pro-, mid- and post-oesophagus before hatching. The odontophoral cartilages, radular collostyle and buccal muscles are all mesodermal in origin and develop from mesenchyme cells which aggregate in early stages below the rudimentary stomodaeum. The endodermal sac differentiates early into a larval stomach and a rudimentary intestine. The former serves in absorbing and digesting the albuminous material during embryonic life. Only small portions of its wall take part in the formation of the adult s stomach and digestive gland. The rest diminishes during late embryonic development and disappears shortly after hatching, when it is replaced by the digestive gland. The gizzard develops from certain differentiated cells which line a distinct longitudinal streak on the right wall of the larval stomach and a small oval area on the left wall. Cells which line another streak on the left wall of the larval stomach give rise to the hepatic vestibule. The digestive gland arises by 2 rudiments on the left posterior wall of the larval stomach. The intestine is entirely endodermal in origin, develops as a posterior tubular prolongation of the endodermal sac, and opens into the mantle cavity by the anus at a relatively late stage. No proctodaeal ectodermal invagination is developed. The anus forms as a new perforation independently of the blastopore, which closes by the end of gastrulation. This investigation was supported in part by research grants (AI 04906 and AI 07696) from the National Institute of Allergy and Infectious Diseases, U.S. Public Health Service. "Department of Zoology, Faculty of Science, Ain Shams University, Cairo. Laboratory of Bilharziasis Research, National Research Centre, Cairo. 151 152 DEMIAN AND YOUSIF INTRODUCTION The present investigation is the second in a series dealing with the embryonic de- velopment and organogenesis of Marisa cornuarietis (L.), a snail of potential im- portance in the biological control of schis- tosomiasis. These studies also aim at clari- fying certain ontogenetic problems and phylogenetic relations in the family Am- pullariidae. In the first part of the series (Demian & Yousif, 1972), a description was given of the early cleavage, gastrulation and gen- eral outlines of the process of embryonic development of M. cornuarietis. The ap- proximate age, dimensions and distinctive anatomical features were given for each of the 12 stages distinguished during the embryonic life of this snail, and the de- velopment of the different organs through- out these stages was briefly described. The present report comprises a detailed description of the origin and embryonic development of the alimentary system of M. cornuarietis. Observations were made on the same material and sets of serial sec- tions which furnished the basis for all other parts of the series. The material and tech- niques employed have already been de- scribed in the lst part of the series. Ref- erence may be made to that part also for the age, dimensions and diagnostic char- acters of the different embryonic stages which are frequently referred to below. The terminology adopted in the present account is based on the works of Demian (1964) and Lutfy & Demian (1964a,b, 1967) on the gross and microscopic anatomy of the alimentary system of adult M. cornuarietis. OBSERVATIONS 1. Early stomodaeum and endodermal sac By the end of gastrulation, the blasto- pore has shifted from the vegetative pole towards the opposite pole. In the Ist embryonic stage, the rudiment of the stomodaeum starts to differentiate just in front of the site of blastopore closure. This rudiment shows as a thickened circular ectodermal plate just below the level of the prototroch. The cells in this plate appear taller and stain darker than neighbouring ectodermal cells, and show а distinctly granular cytoplasm and spherical central nuclei. The endoderm in this stage forms a yellowish spheroidal opaque mass which occupies the greater part of the blastocoel and encloses a narrow irregular archentric cavity. The endodermal cells are mostly cuboidal and have a lightly acidophilic cytoplasm. Their nuclei are large, spheroidal, central in position and relative- ly rich in chromatin; each presents a conspicuous nucleolus. As development proceeds, the rudi- mentary stomodaeal plate invaginates for- ming a simple narrow blind tube which ex- tends backwards until in Stage II its distal tip comes to touch the endodermal sac. The wall of this tube is single-layered; its cells range from tall columnar at the proximal end of the tube, to cuboidal at the distal end. Meanwhile the endo- dermal cells proliferate and arrange them- selves in a single layer, enclosing a rela- tively wide archenteron. In Stage III, the stomodaeal tube further elongates and opens distally in the endodermal sac. The archenteron thus communicates with the outside through the anterior opening of the stomodaeal tube, the mouth. This opening is rela- tively wide and faces antero-ventrally. In Stage IV, the stomodaeum becomes funnel-shaped and thus roughly divisible into 2 regions: a wider anterior buccal region, and a tubular posterior oesophageal one. A slight median evagina- tion shows on the floor of the former region, marking the beginning of forma- tion of the radular sac. Meanwhile the endodermal sac becomes much enlarged and pear-shaped. Reference may be made to figs. 3-10 of Part I of this series (Demian & Yousif, 1972) to follow up these early steps in the development of the stomodaeum and endodermal sac. 2. Radular sac and radula As development proceeds beyond Stage IV, the radular sac evagination grows into EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 153 FIG. 1. Part of a median sagittal section of the embryo in Stage V. FIGS. 2-4. Median sagittal sections of the radular sac of the embryo in Stages VI, VIII and IX respectively. 154 DEMIAN AND YOUSIF KEY TO LETTERING ON FIGURES (All drawings are of Marisa cornuarietis (L. )) A auricle AB albuminous material ALP alary process of radula AM aortic ampulla ANP anal cell-plate AT archenteron BC buccal cavity BL blastocoel BML buccal muscles BRI inner region of dorsal buccal ridge BRO outer region of dorsal buccal ridge BV buccal vestibule CG cerebral ganglion CH collostylar hood CML columellar muscle CN ctenidium COP стор or mid-oesophagus CT cuticle ОСА anterior lobe of digestive gland DGC digestive cell DGP posterior lobe of digestive gland EXC excretory cell F foot FC food channel FGC fusiform gland cell GB goblet cell GZS sorting area of gizzard СИТ cuticularized region of gizzard HV _ hepatic vestibule I intestine И jaw K kidney LOC lateral odontophoral cartilage LGS left gastric streak ES larval stomach M mouth MN _ mitotic nucleus MS mesoderm or mesenchyme cells MT mantle MTC mantle cavity a long tube (RS, Figs. 1-6), which gradual- ly flattens out in the dorso-ventral direc- tion, starting from its anterior (proximal) end backwards. This flattening is ас- companied by a gradual upward reflec- tion of the 2 lateral edges of the tube, pro- ducing a crescent-shaped transverse зес- tion (Fig. 6B). The distal third of the tube, however, retains its tubular form and wide lumen. It curves upwards, though, so that the radular sac eventually assumes an S- shape. The cells in the wall of the tube be- MTE mantle edge OC! Ist band of odontocytes ОС? 2nd band of odontocytes OD — odontoblastic cushion ОЕ — oesophagus OEP oesophageal pouch OER pro-oesophagus OET post-oesophagus IR pericardium PDP pedal cell-plate PRL post-radular ledge PS peristome R radula RC radular collostyle RGS right gastric streak RI rudimentary intestine RM radular membrane RS radular sac SDB buccal region of stomodaeum SDO__ oesophageal region of stomodaeum SE subradular epithelium SH shell (protoconch) SHG shell gland SLD | salivary duct SLG | salivary gland SMB subradular membrane SNC sublingual cavity SOC | superior odontophoral cartilage SOR subradular organ SPE supraradular epithelium SPP supraradular plug SS style sac STC statocyst TL’,- lateral tooth of 2nd TL’ and 5th rows TM” marginal tooth of 5th row TR',- rachidian or median TR’,- tooth of Ist, ТК’ 2nd and 5th rows V ventricle VL velum come considerably differentiated as these developments take place. Thus, in a sagit- tal section of the tube in Stage VIII (Fig. 3), the wall in the proximal third of the tube is formed of narrow columnar cells with densely granular cytoplasm and oval, basal or central nuclei. This part of the tube will not form part of the future radular sac, but will later be pushed for- wards and incorporated in the lining epithelium of the buccal cavity. The rest of the tube constitutes the actual rudiment of the radular sac (RS). Its roof is formed of EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 155 broad columnar cells with relatively large, ovoid, central or apical nuclei. The floor consists of much narrower columnar cells which decrease gradually in height anteriorly and present ovoid or elliptical, basal nuclei. The odontoblasts (OD) start to differentiate in this stage at the distal end of the floor as remarkably tall colum- nar cells which have dense spheroidal nuclei located at different levels within their basal halves. The differentiation of these odontoblasts marks the beginning of formation of the odontoblastic cushion de- scribed in the radular sac of the adult snail by Lufty & Demian (1964а). In Stage IX, the radular sac (RS, Fig. 4) appears further enlarged; its distal globu- lar portion curves more pronouncedly. Thus the odontoblasts come to lie at the posterior wall of the sac, where they form a distinct crescent-shaped odontoblastic cushion. The odontoblasts in this cushion proliferate actively, giving rise to suc- cessive transverse bands of teeth- producing cells, or odontocytes, which gradually pass forward and are added to the subradular epithelium in the floor of the radular sac. The Ist band of odontocytes (OC') is produced late in Stage IX. It consists of 6 adjacent transverse rows of cells which are distinctly shorter and narrower than the odontoblasts, and have smaller basal nuclei and a more acidophilic cytoplasm. Numerous acidophilic secretory granules and fibrillae appear in the apical regions of these odontocytes, indicating that they have become engaged in active secretion: they produce the basic chitinous material of which the earliest row of teeth is formed. The Ist row actually consists of a single rachidian or median tooth (TR') which is secreted directly above the odon- tocytes. A 2nd transverse band of odonto- cytes (OC?, Fig. 5A,B) is developed in Stage X and secretes a row of 3 teeth above it, 1 median (TR?) and 2 laterals (TL?). The 3rd band of odontocytes appears early in Stage XI. It is longer than the first 2 bands and is curved like a horse-shoe, following the curvature of the odontoblastic cushion. This band secretes a 3rd row of 5 radular teeth, 1 median, 2 laterals and only 2 marginals. Five bands of odontocytes and 5 transverse rows of teeth are developed by the end of Stage XI (Fig. 6A). The 5th band is the first to produce a full row of the usual 7 teeth, i.e. 1 median ( TR’, Fig. 6B), 2 laterals (TL*), and 2 inner and 2 outer marginals (TM). When first formed, the teeth of each row stand up almost vertically over the band of odontocytes which secretes them. But as they are conveyed forwards along the radular sac, the lateral edges of the radular ribbon are gradually reflected up- wards so that the marginals are directed horizontally (Fig. 6C). The bands of odontocytes are separated from one another by narrower bands of taller and somewhat broader cells which carry no teeth, have a less acidophilic cyto- plasm and are apparently not engaged in as much active secretion as the odonto- cytes (Fig. 6A). These cells secrete a thin layer of a similar nature and staining reac- tions as the substance elaborated by the odontocytes, but their secretion only con- tributes to the formation of the radular membrane (RM) which binds successive rows of teeth together at their bases. The difference in height between the alternate bands of odontocytes and of these weakly secretory cells will account for the irregu- larity in thickness of the subradular epithelium of the adult which has been re- ported by Lutfy & Demian (1964а). The secretory activity of the odonto- cytes and of the other weakly secretory cells decreases gradually as they move for- wards towards the open end of the radular sac. However, mitotic figures continue to appear within these cells, especially in the weakly secretory cells, which apparently proliferate at a faster rate causing suc- cessive rows of teeth to be more widely separated from each other as they grow older. As successive bands of odontocytes are formed at the odontoblastic cushion and are added to the subradular epithelium, other cellular elements are seen pro- liferating at the rear of the radular sac adding to the supraradular epithelium 156 DEMIAN AND YOUSIF Loc dl | 7 SPE RC MEA Se PLE SOR FIG. 5. A, Part of a median sagittal section of the embryo in Stage X. B. Transverse section of the radular sac, same stage. FIG. 6. A, Part of a median sagittal section of the embryo in Stage XI. B,C, Transverse sections of the radular sac at the same stage, passing at the level of the 5th row of radular teeth (B), and near the proximal end of the sac (C). EMBRYOLOGY OF MARISA. Il. ALIMENTARY SYSTEM 157 (SPE, Fig. 6A-C) in the roof of the sac. These cells form a compact mass that lies above and in front of the odontoblastic cushion and constitutes what has been re- ferred to in the adult as the supraradular plug (SPP) by Lutfy & Demian (1964a). The cells of this plug are remarkably tall, narrow, have relatively large nuclei lo- cated at different levels, and present numerous mitotic figures. Newly formed cells of the supraradular epithelium gain gradually in breadth and their nuclei be- come basal as they move forwards, away from the supraradular plug. Meanwhile several vesicles of different sizes appear in their cytoplasm so that they stain lighter with routine histological stains than any other cells in the radular sac. Later on their apices project into the spaces found be- tween the teeth so that the supraradular epithelium becomes serrated at its free surface. The supraradular epithelium 15 ар- parently moved forwards at the same pace as the subradular one. Thus when a row of teeth is secreted and shifted forwards, the overlying cells of the supraradular epithelium are moved forwards along with it. With this continuous movement of the radula, the tooth first formed reaches the opening of the radular sac in Stage XII. By that time 6-7 rows of teeth have already developed in the radular sac, and the anteriormost part of the growing supra- radular epithelium has become reflected backwards so as to form a cap, the col- lostylar hood (CH, Fig. 6A), covering an aggregate of mesenchyme cells which lies within a median furrow shaped on the dorsal side of the radular sac. These cells represent the precursor of the radular collostyle (RC) As development pro- ceeds, the radula is pushed further for- wards so as to project outside the opening of the radular sac and extend on the an- terior surface of the odontophoral mass as far as the subradular organ (SOR). As mentioned above (p. 154), the anterior third of the original radular sac evagina- tion does not take part in the formation of the radular sac proper, but is pushed for- wards in Stage XI, beyond the opening of the radular sac. The epithelium in its floor thus spreads over the rudiments of the odontophoral cartilages (LOG, Fig. 6A), and a median stripe of it will later be sur- mounted by the radula as it protrudes from the opening of the radular sac. This epithelium produces a thin cuticular secre- tion, the subradular membrane, below the radular ribbon. The roofing epithelium, on the other hand, thins out and contributes to the formation of the post-radular ledge (PRE): Contrary to what has been reported by Ranjah (1942) for Pila globosa, the cells of both sub- and supraradular epithelia ap- parently contribute to the secretion and shaping of the radular teeth. The teeth in the youngest 2 rows always stain uni- formly red with haematoxylin and eosin (H-E) and blue after Mallory’s triple stain, just as the radular membrane. In the next row in front, the apices of the teeth start to acquire a bluish colour with H-E and stain deep blue after Mallory’s stain. In the fol- lowing 2 rows of older teeth, the cor- responding apices of the teeth stain deep blue and reddish-violet after H-E and Mallory's stain respectively, but no change takes place in the staining property of the basal parts of the teeth. This may add further support to the suggestion made by Lutfy & Demian (1964a) that the supra- radular epithelium elaborates certain sub- stances which diffuse into the basic material of the teeth originally laid down by the subradular epithelium, thus modifying the chemical nature and con- sistency of the teeth. Two narrow longitudinal strands of tall columnar cells start differentiating along the 2 dorso-lateral edges of the radular sac at Stage XI. These cells secrete a dense globular secretion (ALP, Fig. 6C) that stains blue with H-E and red with Mal- lory's stain, and accumulates in the angles between the sub- and supraradular epithelia ( SE and SPE) on both sides. This secretion later on forms the 2 chitinous rods which extend on either side of the ex- posed radular ribbon, and also contributes to the formation of the upper layer of the 2 alary processes of the radula (ALP, Fig. 158 DEMIAN AND YOUSIF SA). 3. Peristome and lining epithelium of buccal cavity The epithelial covering of the peristome is first differentiated in Stage IV in the form of a few tall, narrow, non-ciliated ectodermal cells which lie below the mouth opening, have a densely granular cytoplasm and contain spherical basal nuclei. These cells increase in number in subsequent stages (PS, Figs. 1, 5A, 6A, for Stages V, X and XI respectively). They gradually extend upwards on either side of the mouth opening, until they form an in- complete circle around it. After Stage X, the nuclei in these cells become topped each with a small elongated cone of dense cytoplasm, and their ground cytoplasm becomes distinctly vacuolated. The rounded mouth opening simultaneously acquires an oval outline, and finally assumes the shape of a vertical slit in Stage AL. The epithelium of the buccal vestibule, or the anteriormost part of the buccal cavity, also starts to differentiate in Stage IV as a few tall ciliated columnar cells, readily recognized in the roof and floor of the mouth opening (BV, Figs. 1, 5A, 6A). As the stomodaeum enlarges during further development, the buccal vestibule gradually elongates while its cells become highly vacuolated and their cilia markedly longer. The region of the buccal cavity right be- hind the vestibule will enclose the jaws and is therefore described as the man- dibular region (Lutfy & Demian, 1967). This region becomes laterally compressed during late embryonic development, and a small evagination from it passes below the developing odontophore to form the sub- lingual cavity (SNC, Figs. 5A, 6A). The 2 jaws (J, Fig. 7A) are not secreted until the embryo reaches Stage XI, when the mandibular region of the buccal cavity becomes so much compressed that it appears as an inverted T in transverse sec- tion. The epithelium on both sides of the vertical limb of this T-shaped cavity con- sists of narrow columnar cells with central, ovoid to elliptical, dense nuclei and a highly acidophilic cytoplasm loaded with fine acidophilic secretory granules (Fig. 7B). The granules are elaborated by the cells in the form of narrow columns staining pink with H-E and orange-red with Mallory 5 stain, and appear regularly arranged parallel to the longitudinal axes of the underlying secretory cells. These columns, which represent the main com- ponent of the jaws, gradually gain in height after hatching. The rest of the epithelium lining the mandibular region of the buccal cavity secretes a thin homo- geneous cuticular layer (CT, Fig. 7A) that stains red with H-E and blue with Mal- [огу $ stain. The mandibular region is followed Бу the odontophoral region of the buccal cavity (Fig. 8A). The latter becomes dorso- ventrally compressed during late embry- onic development as a result of the enor- mous growth of the odontophoral mass below it. А mid-dorsal longitudinal food channel (FC), lined with ciliated cuboid cells, becomes conspicuous in the roof of this cavity as early as Stage X. The epithelium on either side of this channel gradually thickens so as to form the 2 dorsal buccal ridges. A longitudinal fur- row appears on each ridge in Stage XII, dividing it into an inner medial region (BRI) and an outer lateral one (BRO). Two types of cells become well-differentiated in the epithelium of the former region in this stage: ordinary ciliated columnar epithelial cells with relatively large, ovoid, central nuclei and vacuolated cytoplasm; and much narrower, non-ciliated fusiform gland cells (FGC, Fig. 8C) with densely granular cytoplasm and small oval nuclei. Two other types of cells can also be recog- nized in the epithelial covering of the outer region of each dorsal buccal ridge. The first consists of non-ciliated columnar cells with vacuolated cytoplasm and ovoid nuclei, and the second comprises large, pear-shaped or saccular secretory cells with basal, ovoid nuclei and a cytoplasm filled with numerous secretory spherioles, which stain purple with H-E and faint blue with Mallory's stain. [ag GR i [7 32 MO FIG. Т.А, Transverse section of the head region of the embryo in Stage XII, passing across the mandibular region of the buccal cavity. B, Enlarged portion of the same section showing the jaw and its secretory epithelium. FIG. 8. A, Transverse section of the head region of the embryo in Stage XII, passing across the odontophoral region of the buccal cavity. B,C, Enlarged portions of the same section showing the cells of the lateral odontophoral cartilage (B), and the epithelium of the inner region of the dorsal buccal ridge. FIG. 9. Transverse sections of the pro-oesophagus (A), crop (B) and post-oesophagus (C) of the embryo in Stage XO: 160 DEMIAN AND YOUSIF The subradular organ (SOR, Fig. 6A) becomes conspicuous in Stage XI as a rounded prominence that projects on the floor of the buccal cavity in front of the opening of the radular sac. The glandular nature of the covering epithelium of this organ becomes apparent in Stage XII, when large saccular gland cells, similar to those found in the outer regions of the dorsal buccal ridges, start to differentiate in it. 4. Odontophoral cartilages and buccal muscles The 2 pairs of odontophoral cartilages and all buccal muscles are mesodermal in origin. They develop from mesoderm cells (MS, Fig. 1) which in early stages are arranged in thin longitudinal strands below the stomodaeum. As development proceeds, these cells proliferate actively and form distinct aggregates of mesenchyme cells around the developing radular sac. At least 10 of these masses can be recognized in Stage IX. The largest 3 of them lie 1 below and 2 on either side of the radular sac. The 2 lateral masses form the lateral odontophoral cartilages and some associated muscles, while the ventral mass develops mainly into the infraventral carti- lage tensor muscle. Three other smaller aggregates of mesenchyme cells lie above the radular sac, of which the median one forms the radular collostyle, whereas the 2 lateral masses develop mainly into the sus- pensor muscles of the radular sac. Two more strands of mesoderm cells lie below the rear of the radular sac, and 2 others lie dorsal to the buccal region of the stomodaeum. These cells contribute to the formation of various other buccal muscles. More aggregates of similar mesoderm cells become conspicuous during further development, until, when the embryo reaches Stage XII, the rudiments of most of the buccal muscles (as described in the adult snail by Demian, 1964) become easily identifiable in the embryo. The majority of the cells in these rudi- mentary mesodermal masses are stellate or spindle-shaped. They have a_ highly acidophilic cytoplasm and oval or ellipti- cal nuclei relatively rich in chromatin material, with 1 or 2 nucleoli each. The 2 lateral odontophoral cartilages (LOC, Fig. 8A) develop somewhat earlier than the 2 superior ones (SOC). However, both pairs of cartilages are easily dis- tinguishable in Stage XII. The cells of these cartilages (Fig. 8C), as well as those of the radular collostyle, are considerably enlarged and assume various shapes. They have a highly vacuolated, lightly acidophilic cytoplasm, and relatively small, oval or spheroidal, peripheral nuclei. 5. Oesophageal pouches The 2 oesophageal pouches (OEP, Fig. 9A) start to develop late in Stage XII as tubular evaginations from the dorso-lateral walls of the buccal mass, close behind the 2 dorsal buccal ridges. The cells in these evaginations are columnar, non-ciliated and have basal spherical nuclei. They show no further differentiation until the embryo hatches. 6. Salivary glands These glands first appear in Stage IX as 2 small outpocketings from the roof of the odontophoral region of the buccal cavity. These rudiments grow rapidly into 2 long tubular evaginations (SLG, Fig. 13) which run backwards on either side of the oesophagus (OE). In Stage XI, the distal portions of these tubes become pro- nouncedly dilated, and develop small lateral diverticula, thus acquiring a digitate form. Their cells enlarge and become cuboidal and their nuclei become basal and denser, while large secretory spherioles form in their cytoplasm. How- ever, the proximal parts of these rudi- mentary tubes retain their narrow tubular form and simple walls formed of cuboid cells with spherical central nuclei. These portions will form the salivary ducts. As development proceeds to Stage XII, the rudiments of the salivary glands further enlarge and their lateral diverti- cula increase in size and number (Fig. 16A). The diverticula develop secondary branches and continue to ramify until the EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 161 2 glands eventually assume their com- pound acinar structure after hatching. Meanwhile the surrounding mesenchyme cells form connective tissue strands which ensheath the developing salivary glands and bind their acini together. The secretory cells in these glands in- crease in number, and numerous secre- tory globules accumulate in them. There- fore, the ground cytoplasm becomes con- fined to thin peripheral strands. A few secretory cells of the same nature make their appearance in the walls of the sali- vary gland ducts. At the same time some fusiform gland cells (FGC, Fig. 9A) as well as ordinary ciliated columnar epithelial cells appear wedged in between the secre- tory elements of both the salivary glands and their ducts. The 2 ducts open in the buccal cavity through 2 minute apertures located near the middle of the dorsal buc- cal ridges. 7. Oesophagus The oesophageal region of the stomodaeum (SDO, Fig. 10A) differ- entiates early in Stage V. As development continues, this oesophageal rudiment (OE, Figs. ПА, 12A, 13) gradually elongates until it attains а length of 200 и in Stage X. Until then, its walls present a uniform histological picture. The floor is formed of ciliated columnar cells with granular cyto- plasm and spherical to ovoid nuclei, and the roof is mostly composed of broader cells having vacuolated cytoplasm and spheri- cal basal nuclei. By the time the embryo reaches Stage XII, the oesophagus attains a length of 420 и and has 3 morphologically differen- tiated regions corresponding to the pro-, mid- and post-oesophagus of the adult snail (Lutfy & Demian, 1967). The most anterior region (OER, Fig. 16A) is much shorter and narrower than the other 2 parts. It is laterally compressed and sur- rounded on both sides by the salivary glands (SLG, Fig. 9A). Its cells develop long cilia and attain different heights, thus forming a few longitudinal internal folds. A few fusiform gland cells (FGC), loaded with minute acidophilic secretory glo- bules, make their appearance among these cells. The middle and longest region, the crop or mid-oesophagus (COP, Fig. 16A), is almost regularly cylindrical and its wall is composed of cuboid to columnar cells with short cilia, vacuolated cytoplasm and spherical basal nuclei (Fig. 9B). The posterior region, or post- oesophagus (OET, Figs. 9C, 16A), has a somewhat dorso-ventrally compressed lumen and presents 2 longitudinal ridges on one side. The epithelium on these ridges is formed of relatively large ciliated cells, the cytoplasm of which encloses numerous secretory vesicles, and their basal nuclei have corrugated nuclear membranes. The rest of the wall is lined with much narrower and shorter ciliated columnar to subcolumnar cells with less vacuolated cytoplasm. No part of the endoderm shares in the formation of the oesophagus which is thus entirely ecto- dermal in Marisa cornuarietis. 8. Gizzard and hepatic vestibule Starting with Stage V, the endodermal sac becomes clearly divisible into 2 por- tions: a much more dilated and thicker- walled anterior larval stomach (LS, Fig. 10A,B), and a short tubular posterior rudi- mentary intestine (RI). The cells of the larval stomach are relatively large, have spherical basal nuclei and their cytoplasm encloses globules of albuminous material (AB). The globules stain red with H-E and blue with Mallory's stain, as does the albuminous fluid that fills the archen- teron (АТ). The larval stomach apparently func- tions in absorbing and digesting the albu- men reserve of the egg during embryonic life since only small portions of it take part in the formation of the adult s stomach. The rest diminishes gradually until it dis- appears shortly after hatching and is re- placed by the digestive gland. As develop- ment proceeds after Stage V, the larval stomach continues to enlarge (LS, Fig. 12A-C, for Stage VIII); it becomes pear- shaped, with a wider anterior part and a smaller posterior one. Meanwhile its wall DEMIAN AND YOUSIF 2063 [ 625 FIG. 10. А. Reconstruction of the alimentary system of the embryo in Stage У. В, Transverse section of the embryo, same stage; plane of section indicated by a stippled line in A. FIG. 11. A, Reconstruction of the alimentary system of the embryo in Stage VI. В, Transverse section of the embryo, same stage; plane of section indicated by a stippled line in A. EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 163 FIG. 12. A, Reconstruction of the alimentary system of the embryo in Stage VIII. B,C, Transverse sections of the embryo, same stage; planes of sections indicated by stippled lines in A. FIG. 13. Reconstruction of the alimentary system of the embryo in Stage X. 164 DEMIAN AND YOUSIF further thickens and its cells become gradually saccular, with elongated oval peripheral nuclei. The posterior portion grows faster and projects more and more backwards within the cavity of the visceral sac rudiment, so that by the time the embryo reaches Stage X, the anterior and posterior regions of the larval stomach become equal in size (Fig. 13). There- after, the anterior region starts to diminish in size (Fig. 16A) until it disappears shortly before hatching. Meanwhile the posterior region continues to enlarge. It persists for a short while after hatching, when it becomes replaced by the growing diges- tive gland. A conspicuous longitudinal streak, here referred to as the right gastric streak (RGS, Fig. 11A,B), makes its appearance on the wall of the larval stomach in Stage VI. It runs along the entire length of the right dorso-lateral side of the organ. The cells lining that streak will develop into the cuticularized part of the adults gizzard. They differ markedly from neighbouring cells as they are narrow columnar, smaller, have basal spheroidal nuclei and their cytoplasm is devoid of albuminous globules. Together with the appearance of the right gastric streak, the epithelium in a small oval area (GZS) on the left posterior side of the larval stomach becomes dif- ferentiated. In this area also, there develop narrow columnar cells with spheroidal sub- basal nuclei and a granular cytoplasm de- void of albumen globules. These cells com- prise the rudiment of the sorting region of the adult's gizzard. As the larval stomach is rotated anti- clockwise during torsion, the right gastric streak is gradually shifted upwards and then over to the left until it comes to lie on the left wall of the larval stomach in Stage XI (RGS, Fig. 14A,B.). Meanwhile its cells start to secrete a thin surface layer of cuticle (CT, Fig. 14B). With the dis- appearance of the anterior portion of the larval stomach in the following stage, this streak becomes much shortened, widened and confined to the left wall of the remaining posterior part of the larval stomach, where its cells develop gradually to form the cuticularized portion of the gizzard (СИТ, Fig. 16А). The rudiment of the sorting area of the gizzard (GZS, Fig. 12A,C) simultaneously enlarges and its epithelium thins out and forms a broad evagination on the left pos- terior side of the larval stomach. This rudi- ment shifts gradually upwards during tor- sion until, in Stage XI, it comes to lie on the left dorso-lateral side of the larval stomach (Fig. 14A,B). Its epithelium con- nects posteriorly with that of the right gastric streak. These 2 differentiated epithelial sheets gradually enfold as the rest of the wall of the larval stomach diminishes in size, eventually forming a U- shaped tubular sac, the gizzard. A second streak, the left gastric streak (LGS, Fig. 12A,B.), lined with narrow columnar cells having a highly acidophilic cytoplasm and sub-basal nuclei, starts to differentiate on the left ventro-lateral side of the larval stomach (LS) in Stage VII. The epithelium in this streak represents the rudiment of the hepatic vestibule through which the digestive gland leads into the gizzard. Its posterior half is gradually shifted downwards and then to the right during torsion, until it comes to lie on the right side of the larval stomach in Stage XI (Fig. 14A,B). As the larval stomach diminishes in size during later development, this rudiment shifts gradual- ly nearer to the cuticularized portion of the gizzard, and enfolds to form the hepatic vestibule (HV, Fig. 16B). 9. Digestive gland The 2 lobes of the digestive gland develop from 2 unequal bands of columnar epithelial cells, with densely granular cyto- plasm and large ovoid basal nuclei, which differentiate in the wall of the larval stomach in Stage IX. These bands (DGA and DGP, Fig. 13) lie immediately above and below the rudiment of the sorting area of the gizzard (GZS); the lower band is longer and broader than the upper one. The 2 bands enlarge considerably in the following stage (Fig. 14A, for Stage X) at the expense of the epithelium in the wall EMBRYOLOGY OF MARISA. П. ALIMENTARY SYSTEM 165 DGA 625 FIG. 14. A, Reconstruction of the alimentary system of the embryo in Stage XI. В, Transverse section of the embryo, same stage; plane of section indicated by a stippled line in A. FIG. 15. A-D, Transverse sections of the pro-intestine (A), mid-intestine (B), post-intestine (C) and rectum (D) of the embryo in Stage XI. 166 DEMIAN AND YOUSIF of the larval stomach. In Stage XII (Fig. 16A), the 2 bands meet behind the rudimentary gizzard (GZS and GZT). Meanwhile 2 types of cells become differentiated among their or- dinary columnar cells. The first type (EXC, Fig. 16D) consists of cone-shaped cells with a granular and highly chromo- philic cytoplasm and large spherical sub- basal nuclei. The second type (DGC) con- sists of narrower and taller columnar cells with broad corrugated apices and ovoid central or basal nuclei; their cytoplasm contains small vesicles enclosing globules of the albuminous fluid. These cell types correspond to the excretory and digestive cells described in the adults digestive gland by Lutfy & Demian (1967). The epithelium in the 2 rudiments of the digestive gland starts to show small inner foldings about the time of hatching. By that time, a considerable portion of the wall of the larval stomach is still existing. It consists of large vacuolated cells loaded with albuminous globules. But shortly after hatching, these cells are rapidly re- placed by the increasing cells of the diges- tive gland, the 2 types being morpho- logically quite distinct from each other. At the same time, the inner folds of the diges- tive gland epithelium increase in size and number and develop secondary folds, so that the lumen of the larval stomach is largely obliterated soon after hatching. 10. Style sac and intestine As mentioned above (p 161), the endo- dermal sac becomes differentiated in Stage V into an anterior larval stomach (LS, Fig. 10) and a short tubular posterior rudi- mentary intestine (RI). The latter region has a thinner wall composed of short columnar cells with central ovoid nuclei and a granular cytoplasm devoid of albumen globules. This rudimentary intes- tine gradually elongates and bends sharply downwards during further development until, in Stage VIII, it becomes differen- tiated into 2 parts: a proximal funnel- shaped style sac (SS, Fig. 12A) which widely connects with the larval stomach, and a distal tubular intestine (1). With sub- sequent enlargement of the posterior region of the larval stomach and torsion of the visceral mass, the style sac gradually shifts upwards and forwards until it comes to occupy its definitive position anterior to the sorting area of the gizzard (Fig. 14). Meanwhile the intestine is displaced to the right and carried upwards to run on the right side of the body. In Stage X, the opening between the larval stomach and the style sac (SS, Fig 13) comes to lie above the rudiment of the sorting area of the gizzard (GZS). Its wall then appears formed of sub-columnar cells with short cilia, granular cytoplasm and large ovoid nuclei. The intestine (Г) is much elongated and courses from the style sac to the right around the rear of the larval stomach, then forwards along its right side to open by the anus in the mantle cavity. The anus first appears in Stage IX as a new perforation in the ecto- dermal layer lining the mantle cavity, close behind the anal cell-plate. No trace of a proctodaeal ectodermal invagination was noticed. Therefore the whole of the intestine is endodermal in origin in Marisa cornuarietis. As development proceeds, the intestine becomes more elongated and curves in the shape of a W. Serial cross sections of the embryo at Stage XI show that the 4 regions of the adults intestine start differen- tiating in this stage. The most proximal region next to the style sac, or the pro- intestine (Fig. 15A), shows a single inner longitudinal ridge on the dorsal side. The following part, or mid-intestine (Fig. 15B), is slightly longer and presents 2 main inner longitudinal ridges. The 3rd region, or post-intestine (Fig. 15C) is the widest and shows a single inner longitudinal ridge, while the most distal and narrowest por- tion, or rectum (Fig. 15D), presents no internal ridges. The cells in the walls of these 4 regions of the intestine do not show any appreciable differences at this stage, and seem to be mostly columnar with an acidophilic granular cytoplasm and ovoid basal or sub-basal nuclei. In Stage XII, 2 adjacent longitudinal inner folds develop on the ventral side of EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 167 FIG. 16. A, Reconstruction of the alimentary system of the embryo in Stage ХИ. В, Transverse section of the embryo, same stage; plane of section indicated by a stippled line in A. C-E, The epithelia of the pro-intestine (C), digestive gland (D) and style sac (Е) of the embryo in Stage ХИ. 168 DEMIAN AND YOUSIF the style sac. They correspond to the major and minor typhlosoles of this region. The rest of the wall of the style sac (Fig. 16D) is formed of remarkably tall columnar cells carrying long cilia. The intestine further elongates at this stage, and the cells in its 2 proximal regions (Fig. 16C) develop cilia and a few goblet cells (GB), while the cells in the 2 distal regions аге relatively shorter, non-ciliated and exhibit a more acidophilic cytoplasm. A small tubular evagination, which represents the rudi- ment of the anal gland, develops in this stage also from the wall of the rectum, a little behind the anal aperture. DISCUSSION The present study has revealed that the stomodaeum develops very early in Marisa cornuarietis as an ectodermal invagina- tion, and that the mouth arises as a new perforation just in front of the site of blas- topore closure. Marisa more or less con- forms in this respect with Achatina (Ghose, 1962), but differs from such prosobranchs as Littorina (Delsman, 1914), Patella (Smith. 1935) and Pomatias (Creek, 1951) in which the blastopore persists as the mouth opening, and from Crepidula (Conklin, 1897) and Melania (Ramamoorthi, 1955) in which the mouth opens at the same spot where the blas- topore was located. The radular sac in M. cornuarietis arises by a single evagination in the floor of the stomodaeum. It starts to differentiate only after the connection between the stomodaeum and endodermal sac has been established, a condition similar to that ob- served in Ampullaria canaliculata by Scott (1934) and in Pila globosa by Ranjah (1942). These authors, however, did not indicate when the radula was first secreted or noticed. Ranjah only stressed that the lateral teeth are the first to develop in each transverse row of the radula in P. globosa, the inner marginals developing next, fol- lowed by the outer marginals and the median tooth. In contrast, the present study indicates that, in Marisa сот- nuarietis. the median tooth is secreted first, and that the Ist row of the radula is composed of a single median tooth. The inner and outer marginals are secreted next, and the laterals appear last in each transverse row. An extensive review is given by Raven (1966) of the previous literature per- taining to the development of the radular sac in various molluscs. It seems that no differentiation has been made before be- tween the cells actually involved in tooth secretion, here called odontocytes, and those which produce the tooth-secreting cells, or odontoblasts. Both cell types are commonly referred to in the literature as the odontoblasts and generally considered responsible for tooth production. The so-called oesophageal pouches proved to be buccal structures which arise as tubular evaginations from the roofing epithelium of the buccal mass shortly be- fore hatching. They are thus quite distinct from the mid-oesophageal glands de- veloped in some other gastropods (Graham, 1939). The oesophagus is en- tirely ectodermal in origin, as is the case in Pila (Ranjah, 1942; Nagaraja, 1943) and the majority of the Gastropoda (Raven, 1966). It is neither wholly nor even partly endodermal as reported for Pomatias (Creek, 1951) and Limax (Meisenheimer, 1898). In most ampullariids, as in other prosobranchs with yolk-rich eggs, the originally uniform endodermal cells of the so-called primitive or larval stomach dif- ferentiate during development into some large yolk-filled cells and some other small ones. The former cells act as a larval liver and usually disappear at the end of em- bryonic life, while the latter cells form the epithelium of the definitive stomach (Biitchli, 1877; Erlanger, 1891; Delsman, 1914; Scott, 1934; Ranjah, 1942; Nagaraja, 1943; Raven, 1966). In Marisa, the epithelium of the greater part of the adults stomach develops from similar small-celled regions which differentiate in the wall of the larval stomach, forming 2 distinct longitudinal streaks on that wall, recognized here as the right and left gastric streaks. Earlier investigations of embryonic development in various am- EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM 169 pullariids, however, did apparently not follow up the development of the stomach closely enough to suggest with any рге- cision which regions of the primitive stomach give rise to the different com- ponents of the organ in the adult. Ranjah (1942) recognized 2 longitudinal bands of small cells in the primitive stomach of Pila globosa, which are comparable to the right and left gastric streaks here described. However, he simply referred to these streaks as the rudiment of the alimentary canal proper, and did not relate them exactly to the cuticularized region of the adult gizzard and hepatic vestibule, as was ascertained in the present work. He also noticed an area in the wall of the primi- tive stomach of Pila which he defined as the rudiment of the true stomach, but which corresponds to the rudiment of the sorting area of the gizzard in Marisa. Semper (1862), Scott (1934) and Nagaraja (1943) all described a single streak in the primitive stomach of the different am- pullariids they examined, corresponding to the right gastric streak of M. cornuarietis, but they did not relate it to the adult's gizzard. There seems to be general agreement in the literature that the digestive gland in the Prosobranchia develop from 1 or 2 rudiments in the wall of the primitive stomach (Erlanger 1891, Drummond, 1903; Otto € Tónniges, 1906; Delsman, 1914; Crofts, 1938; Creek, 1951). In M. cornuarietis, the 2 lobes of the digestive gland arise from 2 rudiments differen- tiating early on the left posterior side of the larval stomach. The greater part of the larval stomach diminishes gradually during late embryonic development while it is replaced by the developing digestive gland until it disappears after hatching. These observations are not in agreement with those made for Pila globosa by Ran- jah (1942) who suggested that the large cells in the wall of the primitive stomach passed directly into the digestive gland of the adult. According to this author they enlarged and became vacuolated during late embryonic development, as a result of the absorption and deposition of ingested albumen, and thereby transformed into the digestive gland. This interpretation is presumably erroneous, and may explain why Ranjah considered the digestive gland of Pila as formed of only one lobe. Naga- raja (1943) also denied that the so-called primitive stomach persists and transforms into the adults digestive gland in P. globosa. He considered it an embryonic or larval organ that disappears during em- bryonic life. However, he assumed that the disappearance of this larval organ was due to the activity of certain phagocytic nuchal cells, similar to those characteristic of the embryos of pulmonates; an assumption which is not confirmed by the present observations. The intestine arises as a posterior pro- longation of the endodermal sac which meets the ectoderm of the body wall, breaking through it to open by the anus; no ectodermal proctodaeum is developed. The intestine is, therefore, entirely endo- dermal in origin as in other ampullariids (Semper, 1862; Scott, 1934; Ranjah, 1942) and most gastropods (Conklin, 1897; Wierzejski, 1905; Smith, 1935; Carrick, 1939; Creek, 1951; Ghose, 1962; Raven, 1966). The anus in M. cornuarietis forms as a new perforation, independently of the blastopore. This observation conflicts with Ranjah's (1942) in Pila globosa, that the blastopore persists after gastrulation and forms the anus. ACKNOWLEDGEMENTS The authors gratefully acknowledge the valuable contribution of Dr. K. Mansour, Emeritus Professor, Faculty of Science, Ain Shams University, Cairo, in the super- vision of the present work. Thanks are also due to Dr. B. Hubendick, Director of the Natural History Museum in Gothenberg, Sweden, for directing this research project and for his continuous help during the course of the work. LITERATURE CITED BÚTCHLI, O., 1877, Entwicklungs- geschichtliche Beiträge. I. Zur Entwicklungs- geschichte von Paludina vivipara Müller. 170 DEMIAN AND YOUSIF Zt. wiss. Zool., 29: 216-254. CARRICK, R., 1939, The life history and development of Agriolimax agrestis L., the grey field slug. Trans. Roy. Soc. Edinb., 59: 563-597. CONKLIN, E.G., 1897, The embryology of Crepidula, a contribution to the cell lineage and early development of some marine gastropods. J. Morph., 13: 1-226. CREEK, GA. 1951, The reproductive system and embryology of the snail Pomatias elegans (Müller). Proc. zool. Soc. Lond., 121: 599-640. CROFTS, D.R. 1938, The development of Haliotis tuberculata, with special references to organogenesis during torsion. Phil. Trans. Roy. Soc. Lond., B. 228: 219-268. DELSMAN, H.C., 1914, Entwicklungs- geschichte von Littorina obtusata. Tijdschr. ned. dierk. Ver., 13: 170-340. DEMIAN, Е.5., 1964, The anatomy of the alimentary system of Marisa cornuarietis (L.) Medd. Géteborgs Mus. Zool. Avd. 138 (Göteborgs К. Vetensk.-Vitterh.-Samh. Handl., Ser. В, 9: 1-75). DEMIAN,. E.S., € YOUSIF, F., 1972, Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogas- города: Ampullariidae). I. General outlines of development. Malacologia, 12(1): 123-149. DRUMMOND, I.M., 1903, Notes on the devel- opment of Paludina vivipara, with special reference to the urino-genital organs and theories of gastropod torsion. Quart. J. microsc. Sci., 46: 97-143. ERLANGER, R. von, 1891, Zur Entwicklung von Рашата vivipara. П. Morph. Jb., 17: 636-680. GHOSE, K.C., 1962, Origin and development of the digestive system of the giant land snail Achatina fulica Bowdich. Proc. Roy. Soc. Edinb., B, 68: 186-207. GRAHAM, A., 1939, On the structure of the alimentary canal of style-bearing proso- branchs. Proc. zool. Soc. Lond., В, 109: 75-112. LUTFY, В.С. & DEMIAN, E.S., 1964a, The histology of the radula and the radular sac of Marisa cornuarietis (L.). Ain Shams Sci. Bull., 10: 97-118. LUTFY, В.С. & DEMIAN, E.S., 1964b, On the histology of the odontophoral cartilages of Marisa cornuarietis (L.). Ain Shams Sci. Bull., 10: 119-129. LUTFY, В.С. & DEMIAN, E.S., 1967, The histology of the alimentary system of Marisa cornuarietis (Mesogastropoda: Ampullariidae). Malacologia, 5: 375-422. MEISENHEIMER, J., 1898, Entwicklungs- geschichte von Limax maximus L. Zt. wiss. Zool., 63: 573-664. NAGARAJA, S., 1943, A note on the devel- opment of the alimentary canal in Pila. Proc. Indian sci. Congr., 30: 59. OTTO, Н. € TÖNNIGES, C., 1906, Untersuchungen über die Entwicklung von Paludina vivipara. Zt. wiss. Zool., 80: 411-514. RAMAMOORTHI, K., 1955, Studies in the embryology and development of some melaniid snails. J. zool. Soc. India, 7: 25-34. RANJAH, A.R., 1942, The embryology of the Indian apple-snail, Pila globosa (Swainson) (Mollusca, Gastropoda). Rec. Indian Mus., 44: 217-322. RAVEN, С.Р., 1966, Morphogenesis: The analysis of molluscan development. Pergamon Press, 2nd Ed., 365 p. SCOTT, M.IH., 1934, Sobre el desarrollo embrionario de Ampullaria canaliculata. Rev. Mus. La Plata, 34: 373-385. SEMPER, C., 1862, Entwicklungsgeschichte der Ampullaria polita Deshayes. Naturkund. Verh. Province. | Kunsten. Wetensch., Utrecht, 1: 1-20. SMITH, F.G.C., 1935, The development of Patella vulgata. Phil. Trans. Roy. Soc. Lond., B, 225: 95-125. WIERZEJSKI, A., 1905, Embryologie von Physa fontinalis L. Zt. wiss. Zool., 83: 502- 706. EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM ZUSAMMENFASSUNG EMBRYONALENTWICKLUNG UND ORGANOGENESE BEI DER SCHNECKE MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) Il. ENTWICKLUNG DES ERNAHRUNGSSYSTEMS Е. $. Demian und Е. Yousif Der Ernährungstrakt von Marisa cornuarietis (Linnaeus) umfasst: a) ein ektodermales Stomodaeum, von dem die Radula-Tasche, Schlundtaschen und Speicheldrusen entwickelt werden, und b) ein entodermales Mesenteron, das in Magen, Verdau- ungsdriise, Stielsack und Darm unterteiltist. Das Stomodaeum bildet sich frúhzeitig als eine Einstulpung des Ektoderms, die sich später in den entodermalen Sack öffnet und sich dann in eine vordere Mundregion und eine hintere Schlundregion differenziiert. Der Mund ist eine neue Offnung, die nahe bei dem geschlossenen Blastoporus entsteht. Der Radula-Sack bildet sich als eine Ausstülpung mitten auf der Unterseite der Mundregion des Stomodaeums. Die Radulazáhne werden von aufeinanderfolgenden Querreihen von Odontocyten ausgeschieden, die aus den Odontoblasten am Distalende des Radulasackes hervorsprossen und laufend dem Epithel unter der Radula angefugt werden. Aufeinanderfolgende Reihen von Odontocyten werden voneinander durch guerbänder schwach sezernierender Zellen getrennt, die die Radula-Membran bilden. Das Epithel über der Radula wird ebenso durch Zell-Sprossung aus einer Zellmasse vor den Odontoblassen gebildet, dem Supraradula-Zapfen. Er trägt bei zur Bildung und Formung der Radula-Zähne. Die Kiefer werden kurz vor dem Schlüpfen in einer besonderen mandibularen Region der Mundhöhle gebildet. Die Speicheldrusen und Schlundtaschen entwickeln sich verhältnismässig spät als schlauchförmige Ausstülpungen des Deck-Epithels der Buccalmasse. Der ganze Oesophagus ist von ektodermaler Herkunft. Er beginnt, sich vor dem Schlüpfen in Vorder-Mittel- und Hinter-Oesophagus zu unterteiln. Die zahntragenden Knorpel der Radula-Collostyle und die Mundmuskeln sind sämtlich mesodermalen Ursprungs und entwickeln sich aus Mesenchym-Zellen, die sich in fruhen Entwicklungsstufen unter dem rudimentären Stomodaeum sammeln. Der Entodermsack differenziiert sich früh in den larvalen Magen und einen rudimentären Darm. Der erste dient zur Aufnahme und Verdauung von Eiweiss während des Embryonalstadiums. Nur kleine Teile seiner Wand haben an der Bildung des endgültigen Magens und der Verdauungsdrüse teil. Der Rest nimmt während der späteren Embryonalentwicklung ab und verschwindet kurz nach dem Schlüpfen, er wird dann durch die Verdauungsdrüse ersetzt. Der Magen entwickelt sich aus gewissen differenziierten Zellen, die einen abgegrenzten Längsstreifen an der rechten Wand des Larvenmagens bedecken und einem kleinen ovalen Feld an der linken Wand. Zellen, die einen anderen Streifen an der linken Wand bedecken, werden zum Leber-Vorhof. Die Verdauungsdruse bildet sich aus 2 Resten an der linken Hinterwand des larvalen Magens. Der Darm ist ganz und gar entodermaler Herkunft, er entwickelt sich als eine hintere schlauchförmige Verlangerung des Entodermalsackes und offnet sich erst in einer verhaltnismässig spaten Stufe mit dem Anus in die Mantelhöhle. Von diesem Ende aus findet keine Einstülpung des Ektoderms statt. Der After bildet sich als neue Kör- peröffnung unabhängig vom Blastoporus, der sich am Ende der Gastrulation schliesst. HZ: al 17: DEMIAN AND YOUSIF RÉSUMÉ DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGÉNÈSE CHEZ MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) Ik DEVELOPPEMENT DE L’APPAREIL DIGESTIF Е. $. Demian et Е. Yousif L'appareil digestif de Marisa cornuarietis (Linnaeus) comprend: a) un stomodeum ectodermique.a partir duquel se developpent le sac radulaire, les poches oesophagiennes et les glandes salivaires, b) un mésenteron endodermique différencié en gésier, glande digestive, sac du stylet et intestin. Le stomodeum se développe tót sous forme d'une invagination ectodermique qui, plus tard, s ouvre dans la cavité endodermique et qui, ensuite, se différencie en une région buccale antérieure et une oesophagienne postérieure. La bouche est une nouvelle perforation, apparaissant tout près de l'emplacement de | occlusion du blastopore. Le sac radulaire se développe comme une évagination de la région buccale du stomodeum. Les dents radulaires sont sécrétées par des bandes transversales successives d'odontocytes, qui sont produits par multiplication cellulaire d'une masse d odon- toblastes, localisés à l'extrémité distale du зас radulaire. Les bandes successives d odontocytes sont séparées par des bandes transversales de fines cellules secrétrices qui produisent la membrane radulaire. L'épithélium supraradulaire se développe aussi par multiplication cellulaire d'une masse de cellules, le bouchon” supraradulaire, localisée en avant des odontoblastes. П contribue 4 la formation et au modelage des dents radulaires. Les mächoires sont secrétées un peu avant | éclosion dans une région mandibulaire différenciée dans la cavité buccale. Les glandes salivaires et les poches oesophagiennes, se développent relativement tard sous forme d' évaginations tubulaires à partir de |’ épithélium supérieur de la masse buccale. L'oesophage est en entier d'origine ectodermique. I] commence a se différencier еп pro-, méso- et post-oesophage avant I éclosion. Les cartilages odontophoraux, le collostyle radulaire et les muscles buccaux sont tous d'origine mésodermique et se développent à partir de cellules mésenchymateuses qui 5 accumulent dès les premiers stades au-dessous du stomodeum rudimentaire. La cavité endodermique se différencie tôt en un estomac larvaire et un intestin rudimentaire. Le premier sert à absorber et digérer les substances albuminoïdes pendant la vie embryonnaire. Seulement de petites portions de sa paroi prennent part dans la formation de l'estomac de l'adulte et de la glande digestive. Le reste diminue durant la fin du developpement embryonnaire et disparaît peu après l'éclosion. Le gésier se développe à partir de certaines cellules différenciées qui tapissent un sillon longitudinal distinct sur la paroi droite de l'estomac larvaire et une petite aire ovale sur la paroi gauche. Les cellules qui tapissent un autre sillon de la paroi gauche de l'estomac larvaire donnent naissance au vestibule hépatique. La glande digestive se forme à partir de 2 rudiments sur la paroi postérieure gauche de l'estomac larvaire. L'intestin, entièrement d'origine endodermique, se développe comme un prolonge- ment tubulaire postérieur de la cavité endodermique et $ souvre dans la cavité palléale par l'anus, à un stade relativement tardif. Aucune invagination proctodéale ectoder- mique ne se développe. L'anus se forme comme une nouvelle perforation indépendante du blastopore, qui s est fermé vers la fin de la gastrulation. Apt? EMBRYOLOGY OF MARISA. II. ALIMENTARY SYSTEM RESUMEN DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE) II. DESARROLLO DEL SISTEMA DIGESTIVO Е. $. Demian у F. Jousif El sistema digestivo comprende: a) un stomodeum ectodermico del cual se desarrollan los sacos radular y esofágico, y glándulas salivares; b) un mesenterón endodermico en el que se distinguen la molleja, saco del estilete, glándula digestiva e intestino. El stomodeum se desarrolla primero como una invaginación ectodermica, se abre en un saco endodermal, diferenciándose después en una región bucal anterior y una posterior esofágica. La boca es una abertura nueva cerca del sitio del cierre blastogórico. El saco radular crece como una invaginacion medio-central, de la región bucal del stomadeum. Los dientes radulares son secretados por bandas transversales y sucesivas de odontocitos, los cuales se producen por proliferación celular de una masa de odon- toblastos localizada al término distal del saco radular, y se van agregando continuamente al epitelio subradular. Las sucesivas bandas de odontocitos estan separadas por otras transversales de células secretoras débiles las cuales producen la membrana radular. El epitelio supraradular tambien se desarrolla por proliferación celular de una masa de células ubicadas frente a los odontoblastos, la espita u obturador supraradular. Esto con- tribuye a la formación de los dientes radulares y a sus configuraciones. Las mandíbulas son secretadas poco antes del nacimento del embrión dentro de una región mandibular diferenciada de la cavidad bucal. Las glándulas salivares y sacos esofágicos se desarrollan relativamente tarde como evaginaciones tubulares del epitelio en el techo de la masa bucal. El esófago entero es de origen ectodermico; empieza diferenciándose entre pro-medio- y post-esófago antes de la eclosión. Los cartílagos odontoforicos, colostilo radular y músculos bucales, son todos de origen mesodermico y se desarrollan de células mesenquimales, que se aglomeran en las primeras fases debajo del stomodeum rudimentario. El saco endodermal comienza una diferenciación temprana entre un estómago larval rudimentario y un intestino. El primero sirve para absorber y digerir las materias albuminoideas durante la vida embrionaria. Sólo pequeñas prociones de sus paredes toma parte en la formación del estómago del adulto y la glándula digestiva. El resto se reduce durante el desarrollo embrionario posterior y desaparece poco antes de la eclo- sión, siendo reemplazado por la glándula digestiva. La molleja es creada por ciertas células diferenciadas que forran una faja longitudinal distinta sobre la pared derecha del estómago larval y una pequeña area oval de la pared izquierda. Células que forran otra banda de la pared izquierda dan desarrollo al vestíbulo hepatico. La glándula digestiva se forma de 2 rudimentos sobre la pared izquierda posterior del estómago larval. El intestino es totalmente de origen endodermico, se desarrolla como una prolongación tubular posterior del saco endodermico y se abre, en un estado larval tardío, en la región anal de la cavidad paleal. No hay invaginación ectodermica proctodeal. El ano se forma como una nueva perforación independiente del blastofore, el cual se cierra al final de la gastrulación. те 173 174 DEMIAN AND YOUSIF ABCTPAKT ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗУ MARISA CORNUARIETIS (MESOGASTROPODA, AMPULLARIDAE) П. РАЗВИТИЕ ПИЩЕВАРИТЕЛЬНОЙ СИСТЕМЫ Э.С. IMM3H И 0. ЮЗИФ Пищеварительная система Marisa cornuarietis включает В себя: a) эктодермальный стомодеум, из которого развиваются радулярный мешок, карманы пищевода и слюнные железы и 6) эндодермальный мезентерон, дифференцирующийся в 306, пищеварительную железу, мешок стебелька и кишку. Стомодеум развивается рано, как эктодермальное впячивание, которое затем открывается в оэндодермальный мешок, потом дифференцируется в переднюю буккальную и заднюю пищеводные области. Рот является новым отверстием, возникающим близко от места закрытия бластопора. Радулярный мешок развивается как выпячивание в середине нижней части буккальной области стомодеума. Зубы радулы секретируются последовательными поперечными рядами одонтоцитов, которые возникают в результате пролиферации клеток из массы одонтобластов, расположенных на дистальном конце радулярного мешка, и непрерывно добавляются к субрадулярному эпителию. Последовательные ряды одонтоцитов разделяются поперечными рядами слабо секретирующих клеток, производящих радулярную мембрану. Супрарадульный эпителий так же развивается за счет пролиферации клеток из массы клеток, расположенных впереди одонтобластов - супрарадулярной пробки. Он способствует образованию и Формированию радулярных зубов. Челюсти секретируются незадолго перед вылуплением внутри дифференцированной мандибулярной области буккальной полости. Слюнные железы и карманы пищевода развиваются относительно поздно в виде трубчатых выпячиваний эпителия крыши буккальной массы. Весь пищевод по происхождению эктодермальный. Он начинает дифференцироваться в передний, средний и задний отделы пищевода перед вылуплением. Хрящи одонтофора, радулярный коллостиль и буккальные мускулы - мезодермального происхождания и развиваются из тех клеток мезенхимы, которые аггрегируются на ранних стадиях под рудиментарным стомодеумом. Эндодермальный мешок рано дифференцируется в ларвальный желудок и рудиментарную кишку. Первый служит для всасывания и переваривания белкового материала в течение эмбриональной жизни. Лишь небольшие части его стенки принимают участие в формировании желудка взрослой особи и пищеварительной железы. Остальная его часть уменьшается во время позднего эмбрионального развития и исчезает вскоре после вылупления, когда ларвальный желудок замещается пищеварительной железой. Зоб развивается из определенных дифференцированных клеток, выстилающих в виде продольной полоски правую стенку личиночного желудка и небольшую овальную область на левой стенке. Клетки, выстилающие другую полоску на левой стенке личиночного желудка, дают начало преддверию печени. Пищеварительная железа возникает в виде 2 рудиментов на левой задней стенке ларвального желудка. Кишка, по происхождению полностью оэндодермальна, возникает как трубчатое продолжение эндодермального мешка и на относительно поздней стадии открывается в мантийную полость анусом. Эктодермального выпячивания проктодеума не возникает. Анус образуется назависимо от бластопора, закрывающегося к концу гаструляции. Z.A.F. MALACOLOGIA is published by the Institute of Malacology, 1336 Bird Road, Ann Arbor, Michigan 48104, U.S.A. The Sponsor Members of this Institute, also serving as editors, are listed below. N. F. SOHL, President Е. G. BERRY R. ROBERTSON, President Elect J. B. BURCH Je Е. ALLEN, Vice-President | М. В. CARRIKER С. В. STASEK, Secretary а. М. DAVIS К. J. BOSS, Treasurer A. G. SMITH Subscription price per volume (Vols. 11 and 12) for individual (personal) sub- scribers is US$ 7.00. Institutional subscriptions are US$ 10.00 per volume. If subscriptions are handled through a North American subscription agency, add US$ 1.00 for extra handling costs. Subscription requests, payments and inquiries should be sent to MALACOLO- GIA, c/o Department of Mollusks, Academy of Natural Sciences, Nineteenth and the Parkway, Philadelphia, Pennsylvania 19103, U.S.A. Vol. 12, No. 1 MALACOLOGIA CONTENTS В. Н. POHLO Feeding and associated functional morphology in Tagelus californianus and Florimetis obesa (Bivalvia: Tellinacea)............ E. G. DRISCOLL and D. E. BRANDON Mollusc-sediment relationships in northwestern Buzzards Bay, ha Massachusetts, USA iat Со ОО ene fear! M. CASTAGNA and P. CHANLEY Salinity tolerance of some marine bivalves from inshore and estuarine environments in Virginia waters on the western | Midatlantic coasts os ae 0e и A AE AAN Oy 2 M.J. IMLAY À | Effects of potassium on survival and distribution of freshwater | mussels SEATS О РН NEE ИННА AD AO EN RE. Е fé G. WIUM-ANDERSEN АИТ | Electrophoretic studies on esterases of some African Biomphalaria + spp. (Planorbidae) Be ANA ER RATES Lu E S. DEMIAN aad в. YOUSIF (otha tee A te у | р _ Embryonic development and organogenesis in the snail Marisa nf Bar cornuarietis (Mesogastropoda: Ampullariidae) AR ae Sea Дер i) у ñ I. General outlines of development ..... RUBI be | LE $ DEMIAN and F. YOUSIF ВНИИ i Embryonic development and organogenesis in the snail Marisa. | cornuarietis (Mesogastropoda: Ampullariidae) Tey he II. Development of the alimentary. system NN w +, A ‘ ER ar у N | aR ' F h NA 4 { LS ‘ \ iF à y wai Е a’ $ E 7 41 LA К $ à 1 Y са 1 | ан LA q | ON ED | | AS | pd Cie In Fe » fi / ARA ee Fa у } vias PRAY ety E О NA de ORG ET N Whe р НХ A ote ТИ ВИЙ ag VARTA il be 6 NX y al EN A \ (TPE РН М 12 (NO 2 у 19,78. a MUS. COMP. ZOOL | и. о LIBRARY | MAR 25 1074 | Aa, MALACOLOGIA Weed x N u VOL. ух Kin ÿ y 1 rh International Journal of Malacology | ens Y _ Revista Internacional de Malacologia ~~ AN > а: ti x : Journal International de Malacologie => h | _ Международн ый Журнал Малакологии | oie k $ Нопа!е Malakologische Zeitschrift — SE ni ' ae AN 7 eon Ka \ » inthe р À A ANDA E 4 ‘ у “à r ( Mn Y и ne y р Se tne = Ieee AE | MALACOLOGIA Editor-in-Chief J. B. BURCH General Editors С. J. BAYNE ANNE GISMANN Secretary J. WHITE-RUDOLPH Editorial Office Museum of Zoology University of Michigan Ann Arbor, Michigan 48104 Ue Sa A. Subscription Office Department of Mollusks Academy of Natural Sciences Philadelphia, Pennsylvania 19103 ASAS EDITORIAL BOARD P. O. AGÓCSY, Budapest, Hungary E. E. BINDER, Geneva, Switzerland C. R. BOETTGER, Braunschweig, Germany A. H. CLARKE, Ottawa, Canada E. S. DEMIAN, Cairo, Egypt C. J. DUNCAN, Liverpool, U.K. Z. A. FILATOVA, Moscow, U.S.S.R. E. FISCHER-PIETTE, Paris, France A. FRANC, Paris, France V. FRETTER, Reading, U.K. Р. GALTSOFF, Woods Hole, U.S.A. А. У. GROSSU, Bucharest, Rumania T. HABE, Tokyo, Japan A. D. HARRISON, Waterloo, Canada K. HATAI, Sendai, Japan М. A. HOLME, Plymouth, U.K. В. HUBENDICK, Göteborg, Sweden A. M. KEEN, Stanford, U.S.A. М. А. KLAPPENBACH, Montevideo, Uruguay Y. KONDO, Honolulu, U.S.A. T. KURODA, Kyoto, Japan H. LEMCHE, Copenhagen, Denmark AKLILU LEMMA, Addis Ababa, Ethiopia J. LEVER, Amsterdam, The Netherlands A. LUCAS, Brest, France N. MACAROVICI, lasi, Rumania D. Е. MeMICHAEL, Sydney, Australia С. MEIER-BROOK, Tübingen, Germany J. E. MORTON, Auckland, New Zealand W. К. OCKELMANN, Helsingór, Denmark J. OKLAND, Oslo, Norway W. L. PARAENSE, Brasilia, Brazil J. J. PARODIZ, Pittsburg, U.S.A. ' С. М. PATTERSON, Ann Arbor, U.S.A. W. F. PONDER, Sydney, Australia A. W. В. POWELL, Auckland, New Zealand В. D. PURCHON, London, U.K. C. P. RAVEN, Utrecht, The Netherlands О. RAVERA, Ispra, Italy С. Е. Е. ROPER, Washington, D.C., U.S.A. N. W. RUNHAM, Bangor, U.K. S. G. SEGERSTRALE, Helsinki, Finland F. STARMUHLNER, Wien, Austria J. STUARDO, Concepcion, Chile F. TOFFOLETTO, Milano, Italy W. S. 5. VAN BENTHEM JUTTING, Domburg, The Netherlands J. A. VAN EEDEN, Potchefstroom, S. Africa С.О. VAN REGTEREN ALTENA, Leiden, Neth, B. R. WILSON, Perth, Australia C. M. YONGE, Edinburgh, U.K. H. ZEISSLER, Leipzig, С. D. В. A. ZILCH, Frankfurt, Germany 1 * VOL. 12 NO. 2 1973 MALACOLOGIA International Journal of Malacology Revista Internacional de Malacologia Journal International de Malacologie Международный Журнал Малакологии Internationale Malakologische Zeitschrift In Memoriam G. P. Kanakoff N. H. J. Odhner R. V. Seshaiya MALACOLOGIA EDITORS MALACOLOGIA, 1973, 12(2): 175-194 EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). Ш. DEVELOPMENT OF THE CIRCULATORY AND RENAL SYSTEMS! Emile $. Demian? and Fouad Yousif? ABSTRACT The pericardium, heart and kidney of Marisa cornuarietis arise from a single common mesodermal anlage which differentiates early (Stage IT) on the right side of the embryo. This common rudiment develops a central cavity, the coelom, by the separation of its cells, then divides by a constriction into an anterior pericardial sac and a posterior kidney. A corresponding left rudiment soon disappears, disintegrating into mesenchyme. Thus the 2 rudiments do not fuse to form a single sac, as previously reported for some ampullariids. The auricle and ventricle do not develop as a single tube which later constricts in the middle, but as 2 separate invaginations from 2 opposite sides of the rudimentary pericar- dial sac. They subsequently inter-communicate (Stage VI), forming a tubular heart which initially lies almost fransversely. Torsion later shifts the pericardium to the left dorso-lateral side and brings the auricle in front of the ventricle. Haemocoelic sinuses and blood vessels develop independently of the pericardium and heart from irregular spaces in the mesenchyme within the blastocoel. Most of these become well-established during embryonic life, connecting with the heart at a late stage. The aortic ampulla was shown to develop as a haemocoelic sinus below the pericardium and later not to lie within the pericardial sac, but to be lodged in a deep inward bulge of the thin floor of that sac. The anterior part of the rudimentary kidney transforms into a short ciliated reno- pericardial tube. The remainder forms the kidney which, first tubular, then saccular, develops a thick plexus of blood vessels in its roof. Torsion shifts the kidney dorso- laterally to the left. The ureter, a fully functional excretory organ previously thought to be another kidney, is ectodermal in origin and arises by a tubular invagination on the right side only of the embryo. It later communicates with the mesodermal kidney (Stage IV). Its proximal part forms a funnel-shaped renal vestibule, first described here. The walls of the ureter develop transverse internal foldings which become richly vascularized, serving an ex- cretory function. The ureter shifts in front of the kidney during torsion, coming to lie in the roof of the mantle cavity, while the excretory opening and the renal vestibule become deeply enclosed in the mantle cavity. By demonstrating that the kidney is homologous with the topographically left kidney of the Archaeogastropoda and that the ureter is not homologous with their right kidney but with the ureter of other Mesogastropoda, this study contributes to the clarification of the controversial homologies of these organs in the Ampullariidae. INTRODUCTION |, naeus), an ampullariid snail which has recently gained considerable importance This is the 3rd paper in a series dealing as a biological control agent against with the embryonic development and schistosome-transmitting snails. These organogenesis of Marisa cornuarietis (Lin- studies are meant to contribute to a better ! This investigation was supported in part by research grants (AI 04906 and AI 07696) from the National Institute of Allergy and Infectious Diseases, U.S. Public Health Service. 2 Department of Zoology, Faculty of Science, Ain Shams University, Cairo. 3 Laboratory of Bilharziasis Research, National Research Centre, Cairo. (175) 176 DEMIAN AND YOUSIF knowledge of this species, and to clarify certain ontogenetic problems and phylogenetic relations in the family Am- pullariidae to which the snail belongs. The Ist part of the series (Demian & Yousif, 1973a) included a description of the early cleavage, gastrulation and the general outlines of the process of em- bryonic development of Marisa сот- nuarietis during the 12 embryonic stages recognized and described. The 2nd part (Demian & Yousif, 1973b) was concerned with the embryogenesis of the alimentary system. The present paper comprises a detailed description of the origin and embryonic development of the circulatory and renal systems of Marisa cornuarietis. These 2 systems are here treated together since their main organs arise from a common primordium. Findings are compared with earlier information on other Am- pullariidae. Observations were made on the same material and sets of serial sections which were used in all other parts of the series. The material and techniques employed have been described in the Ist part of the series, to which reference should also be made for the age, dimensions and diagnostic features of the different em- bryonic stages which are frequently referred to below. KEY TO LETTERING ON FIGURES! A auricle AM aortic ampulla ANP anal cell-plate APP apical cell-plate ARV - afferent renal vein AT archenteron АСУ afferent ureteral vein BE blastocoel С coelom CN ctenidium CON - excretory concretions DGP _ posterior lobe of digestive gland EN endoderm ET ectoderm EUV | efferent ureteral vein FR lateral furrow on ureter GZS sorting area of gizzard I intestine K kidney LS larval stomach MS mesoderm or mesenchyme cells MT mantle МТС mantle cavity MTE mantle edge MYB myoblasts E pericardium E pericardial cavity PDP _ pedal cell-plate РНК common primordium for pericardium, heart and kidney PT prototroch RGS right gastric streak RENO external renal opening RNV renal vestibule RPT reno-pericardial tube RT rectum SD stomodaeum SH shell (protoconch) SHG shell gland SHGR rudimentary shell gland SS style sac U ureter V ventricle OBSERVATIONS 1. Early rudiments The pericardium, heart and kidney of Marisa cornuarietis are all mesodermal in origin and arise from a single common primordium; the ureter is ectodermal. Rudiments of all these organs start to differentiate early, in Stage II of the em- bryo, which generally corresponds to the free trochophore larva of marine prosobranchs. Two small compact masses of mesoderm cells (MS, Fig. 1A,B) make their appearance at that stage on either side of the endodermal sac (EN), nearer to the posterior end? of the embryo. These masses most probably arise by cell proliferation from 2 teloblasts derived from the micromere 4d (Demian & Yousif, 1973a). They consist of ovoid or polygonal ЗАП drawings are of Marisa cornuarietis (L.). The general views are reconstructions of the circulatory and renal organs made from serial transverse and sagittal sections. "The antero-posterior axis of the embryo at this stage corresponds to the animal-vegetative polar axis. EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 177 ANP 0.1mm B 0.1mm FIG. 1. A, Embryo in Stage II, left lateral view. B, Transverse section of the embryo, same stage; plane of section indicated by stippled line in A. FIG. 2. A, Embryo in Stage III, left lateral view. B, Transverse section of the embryo, same stage; plane of section indicated by stippled line in A. FIG. 3. A, Embryo in Stage IV, left lateral view. B, Part of a sagittal section of the embryo (same stage) passing through the common primordium of pericardium, heart and kidney. 178 DEMIAN AND YOUSIF cells with highly chromophilic granular cytoplasm and large spherical nuclei. The left mass is somewhat smaller, lies a little anterior to the right one and remains con- spicuous for only a short period. It then diminishes gradually in size until it dis- appears completely in the following em- bryonic stage (Fig. 2A), disintegrating into mesenchyme. The right mass, on the other hand, persists and constitutes a common rudiment for the pericardium, heart and kidney (PHK). The rudiment of the ureter (U, Fig. 1A,B) also differentiates in Stage II as a small thickened circular plate in the ec- toderm, to the right of the anal cell-plate (ANP). The common rudiment of the pericar- dium, heart and kidney (PHK, Fig. 2A,B) slightly enlarges in Stage Ш, shifts a little upwards and transforms into an ovoid vesi- cle that measures about 35 и in length. Its cells move apart and arrange themselves in a single layer, surrounding a small central cavity (C, Fig. 2B) which is the sole coelomic cavity to develop in the embryo; the coelom is thus a schizocoel. This rudimentary mesodermal vesicle becomes further enlarged in Stage IV. A distinct constriction develops nearer to its posterior end, dividing it incompletely into 2 parts which communicate freely with one another. The anterior part is larger, thinner-walled, measures about 50 w in diameter and represents a rudimentary pericardial vesicle (P, Fig. 3A,B) from which the heart will also develop later. The posterior part measures only 20 u in diameter and constitutes the rudiment of the kidney (K); it communicates posterior- ly with the rudimentary ureter (U) by the end of Stage IV. 2. Pericardium and heart The rudimentary pericardial vesicle (P, Fig. 4A,B) shifts a little backwards in Stage V, and its wall thins out all over except in 2 small areas on the left and the postero- dorsal sides from which the ventricle (V, Fig. 4C) and auricle (A), respectively, develop. The cells in these 2 thickened areas are cuboid, rhomboidal or polygonal, with large spherical nuclei. The rest of the wall of the rudimentary vesicle consists of more or less flattened cells and develops into the future pericardium (P). The rudiment of the auricle starts in- vaginating late in Stage V. It gradually forms a pouch-like invagination (A, Fig. 5A-C) that projects into the rudimentary pericardial vesicle (P), and some mesenchyme cells (MS) from the blastocoel or segmentation cavity (BL) migrate into it. This process of invagina- tion is immediately followed by a similar invagination of the rudimentary ventricle (V). The latter forms a narrower and thicker-walled tubular invagination which projects diagonally to the right and up- ward into the pericardial cavity (PC) until it touches the invaginated auricle; the cavities of the 2 invaginations then com- municate. Thus a rudimentary tubular heart becomes well-established in Stage VI, extending almost transversely, with the auricle lying to the right side and a little dorsal to the ventricle. The cavity of this heart communicates widely at both ends with the primary body cavity (BL, Fig. 5C). At this stage, the pericardium (P) is thin and formed by a single layer of squamous cells with elliptical nuclei. The wall of the auricle (A) consists of less flattened cells with thickened central por- tions enclosing large spherical nuclei, while that of the ventricle (V) is made up of columnar to sub-columnar cells with ovoid nuclei and darkly stainable granular cytoplasm. In Stage VII, the pericardial sac (P, Fig. 6A) has further enlarged, measuring about 100 u in diameter. It has moved a little to the left, coming to lie medially above the rear of the larval stomach (LS). The heart stretches obliquely inside it and begins to show some irregular pulsations. Torsion causes the pericardial sac (P, Fig. 7) to shift further to the left in Stage VIII. Meanwhile, the ventricle (V) begins to lose its tubular form, becomes saccular and some minute internal projections appear on its wall. In Stage IX, the pericar- dial sac (P, Fig. 8) attains a length of 140 u. The heart pulsates rhythmically; the ven- EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 179 >, A — es 5 zent 4 VAIO ¿OY RS, = m 0.1mm 4 ger CS El | Ez Le «< ~ , de QT ee N FIG. 4. A,B, Embryo in Stage У, in left lateral (A) and dorsal (В) views. С, Part of a sagittal section of the embryo (same stage) passing through the primoridia of the pericardium, kidney and ureter. FIG. 5. A,B, Embryo in Stage VI, in left lateral (A) and dorsal (B) views. С. Part of a transverse section of the embryo, same stage; plane of section indicated by stippled line in A. 180 DEMIAN AND YOUSIF tricle (V) has become pear-shaped and shows numerous inner processes pointing in various directions. The opening between the auricle and ventricle becomes more constricted, and 2 inner septal processes develop close to it, representing 2 rudimentary auriculo-ventricular valves. As the pericardial sac continues to enlarge in subsequent stages (P, Figs. 9A; 10A), it is gradually pushed forwards along with the forward extension of the mantle skirt (MT). The auricle (A) and ventricle (V) broaden at their junction, and the cells in their walls flatten more and more (Fig. 9D). In Stage XII, 2 types of cells become well-differentiated in the walls of the auri- cle (A, Fig. 10C) and ventricle (V): squamous endothelial cells with small elliptical nuclei, and larger irregularly- shaped myoblasts (MYB) with spherical or ovoid nuclei. The latter cells have highly acidophilic attenuated ends and thick cen- tral portions containing numerous basophilic granules of different sizes. Some of these cells extend to various direc- tions within the cavities of the heart chambers, especially in the ventricle (V). They increase gradually in number after hatching, developing into numerous irregular crossing and anastomosing mus- cle strands which run within the cavities of the heart chambers in the adult. 3. Blood vessels and sinuses Blood vessels and sinuses develop, in- dependently of the pericardium and heart, from scattered irregular spaces or portions of the primary body cavity which are left in between the propagating mesenchyme cells. In early embryonic stages, these spaces are surrounded by loose mesenchyme cells of different shapes. During development, they gradually assume a tubular form, acquire a lining of simple endothelium of flattened mesenchyme cells, with ovoid or elliptical nuclei, arid finally connect with the heart. At least 8 such rudimentary blood spaces can be recognized in Stage V of the em- bryo. One of these sinuses, which lies below the stomodaeum, and another, which develops on the left side of the lar- val stomach, will join in Stage VII to form the anterior or cephalic aorta. Two other sinuses, one on either side of the stomodaeum, constitute the rudiment of the cephalopedal haemocoelic sinus. The remaining 2 pairs of sinuses will unite in later stages of development to form the visceral haemocoelic sinus: the Ist pair lies to the right and below the larval stomach, | and the 2nd to the right and behind the pericardium. In Stage IX, some mesenchyme cells aggregate below the pericardium, representing the rudiment of the main aor- ta and aortic ampulla. These cells enclose a small space which is in open communica- tion with the cavity of the ventricle. The aortic ampulla (AM, Fig. 9B,C) becomes well-established in Stage X, appearing as a thin-walled sac that lies just below the pericardium (P), on the left dorso-lateral side of the larval stomach (LS). As the stomach greatly enlarges during subse- quent development, the aortic ampulla is gradually pushed upwards and pressed against the pericardium (P) until in Stage XII, it becomes entirely lodged within a deep concavity in the floor of the pericar- dial sac. The pallial and renal blood vessels and sinuses develop relatively late and will be considered below, in connection with the development of the kidney and ureter. 4. Kidney The kidney of Marisa cornuarietis is un- paired from the beginning. After being differentiated from the persisting (right) common rudiment of the pericardium, heart and kidney in Stage IV (p 178), the rudimentary kidney (K, Fig. 3A,B) gradually elongates and assumes a tubular form. It attains a length of 40 u in Stage У (K, Fig. 4A-C) and has relatively thick walls formed by columnar cells with densely granular cytoplasm and spherical to ovoid nuclei. The posterior part of this tubular rudi- ment dilates rapidly during further development so that, as the embryo reaches Stage VII, 2 morphologically dis- EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 181 tinct regions are differentiated in the rudimentary kidney: а sbort tubular anterior or proximal part which measures 12 и in length and will develop into the reno-pericardial tube (RPT, Fig. 6A,B), and a much more dilated ovoid distal part, which measures 40 u in length and 55 u at its greatest width, and will form the kidney proper (К). The wall of the latter part con- sists of cuboid to columnar cells with vacuolated cytoplasm and basal spherical nuclei (Fig. 6B). By the end of Stage VII, the rudimentary kidney has curved about the reno-pericardial tube. In Stage VIII, the kidney (К, Fig. 7) becomes displaced to the left as a conse- quence of torsion. The ureter (U) now opens into the right side of the kidney. The reno-pericardial tube (RPT) is slightly elongated and its cells have acquired short cilia. In the following embryonic stage, the kidney (K, Fig. 8) is more enlarged and projects further forward around the reno- pericardial tube (RPT). Thus, by the end of Stage IX, the reno-pericardial tube is surrounded on all but its right side by the growing saccular kidney. The opening of the tube simultaneously comes to lie near that found between the kidney and the ureter (U). At the same time a few mesenchyme cells begin to aggregate within the primary body cavity to the right side of the reno-pericardial tube. These cells become so arranged in the following stage as to form a narrow tubular sinus, the afferent renal vein (ARV, Fig. 9C), which will later communicate with the cephalopedal haemocoel. The kidney (K, Fig. 9A) continues to enlarge in Stage X while gradually shifting to the right. It is now V-shaped, with the dorsal and ventral limbs (K, shown transversely in Fig. 9B,C) embracing the reno-pericardial tube (RPT), and projec- ting further forwards to embrace the rear of the pericardial sac (P, Fig. 9A,B). The wall of the kidney (K, Fig. 9C) consists largely of cuboid cells with distinctly vacuolated cytoplasm and basal or peripheral dense nuclei, while that of the reno-pericardial tube (RPT) is composed of tall ciliated columnar cells with densely granular cytoplasm and basal ovoid nuclei. During further development, the ven- tral limb of the kidney and the afferent renal vein are both pushed upward as a consequence of continued torsion and further enlargement of the larval stomach below them. Thus, in Stage XI, the lower limb of the kidney comes to lie to the right of, and on the same horizontal plane with, the other limb. The 2 limbs of the kidney are now so close to each other that the afferent renal vein becomes lodged in a deep longitudinal groove running dorsally between them. Another narrower tubular sinus, the efferent renal vein, also differentiates in Stage XI, dorsal to the left limb of the kidney, and later communicates with the auricle. The kidney attains its definitive shape and position and apparently starts func- tioning in Stage XII (K, Fig. 10A). It then appears covered dorsally by a thin layer of ectoderm (ET, Fig. 10B); its roof consists of cuboid and club-shaped cells with spherical basal nuclei and highly vacuolated cytoplasm. The latter is dis- tinctly more acidophilic towards the apices of the cells and contains numerous vesicles enclosing minute excretory con- cretions (CON). The floor, on the other hand, consists of a thin layer of much more flattened cells. In Stage XII, the roof of the kidney starts to show some inner foldings. Mesenchyme cells (MS, Fig. 10B) from the primary body cavity migrate into these folds and haemocoelic cavities appear between them. The folds increase steadily in number and size after hatching and produce secondary folds which press against each other so that the roof gradual- ly acquires the spongy structure characteristic of the adult's kidney. A com- plex network of blood sinuses develops within these folds and connects with the afferent and efferent renal veins. The floor of the kidney, however, remains thin and unfolded. 182 DEMIAN AND YOUSIF 0.Imm 7 K 8 OMA FIG. 6. A, Embryo in Stage VII, dorsal view. B, Transverse section of the kidney, same stage. C, Transverse section of the ureter, same stage. FIG. 7. Embryo in Stage VIII, dorsal view. FIG. 8. Embryo in Stage IX, dorsal view. EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 183 5. Ureter and renal vestibule The rudiment of the ureter (U, Fig. 1A,B), as mentioned above (p 178), differentiates early in Stage II as a small thickened circular plate in the ectoderm (about 6 cells in diameter), to the right side of the anal cell-plate (ANP). The cells in this rudiment are taller and narrower than neighbouring ectodermal cells (ET, Fig. 1B) and show a more chromophilic cytoplasm and relatively smaller, ovoid, central nuclei. In Stage III, this rudimentary ectoder- mal plate (U, Fig. 2A,B) starts in- vaginating, thus projecting deeply inwards below the common rudiment of the pericardium, heart and kidney (PHK). The invagination enlarges during further development and gradually assumes a tubular form. Its distal tip comes to touch the posterior wall of the rudimentary kidney (K, Fig. 3A), into which it opens by the end of Stage IV. It is the distal portion of this tube that constitutes the rudiment of the ureter proper (U); the proximal narrower part forms what is referred to here as the renal vestibule (RNV). No trace of a comparable rudimentary structure or invagination is seen on the opposite or left side of the embryo, i.e., the ureter is un- paired from the beginning. Nothing is developed in the embryo that can be regarded as a 2nd or left rudimentary ureter. In Stage V, the rudimentary renal vestibule (RNV, Fig. 4A,B) further enlarges and shifts a little upwards so as to lie below the pericardial sac (P). Meanwhile, the much more dilated rudimentary ureter (U) becomes laterally compressed. During subsequent development (Stage VI), the ureteral tube (U, Fig. 5A,B) further elongates. Its walls become pinch- ed centrally along the longitudinal axis so that, in cross section, the lumen appears dumbbell-shaped. Viewed in its entirety, the lumen of the organ essentially consists of a U-shaped peripheral canal, surround- ing a narrow central compressed portion. The dorsal limb of the “U” connects anteriorly with the kidney (K), while the ventral limb leads, also anteriorly, into the renal vestibule (RNV). The wall of the ureter consists of tall columnar cells with vacuolated cytoplasm and sub-basal ovoid nuclei. In the same embryonic stage (Stage VI), 2 tubular sinuses become differentiated in the segmentation cavity alongside the ureter. The Ist sinus extends along the right dorso-lateral edge of the organ, while the 2nd runs along its left ventro-lateral side. These sinuses give rise later (Stage X) to the 2 efferent ureteral veins (EUV, Fig. OBI): In Stage VII, the renal vestibule (RNV, Fig. 6A) has shifted further upward and now touches the floor of the kidney (K). At the same time, a longitudinal furrow (FR, Fig. 6C) is shaped on the left side of the ureter (U). Two further longitudinal haemocoelic sinuses become established at this stage, one within the furrow and the other along the right face of the ureter. These sinuses will later form the dorsal and ventral branches, respectively, of the afferent ureteral vein (AUV, Fig. 9B,C, for Stage X). The renal vestibule (RNV, Fig. 7) is further enlarged and appears cone-shaped in Stage VIII. Its external opening now faces forward as a result of torsion and lies within a broad concavity that represents the incipient mantle cavity (MTC). The ureter (U) has also been rotated, due to torsion, so that its longitudinal axis comes to lie transversely to the longitudinal axis of the body, and the lateral furrow (FR) faces backwards. As torsion proceeds through Stage IX, the ureter (U, Fig. 8) becomes con- siderably elongated and further rotated so that its greater part extends along the mantle roof anterior to the kidney (K), and its lateral furrow (FR) comes to face to the right. In the meantime, the opening of the renal vestibule has been completely enclosed within the developing mantle cavity. By the end of torsion in Stage X, the ureter (U, Fig. 9A-C) is about 220 u long. Its longitudinal lateral furrow (FR) faces dorso-laterally. The connection between 184 DEMIAN AND YOUSIF FIG. 9. A, Embryo in Stage X, dorsal view. B, C, Transverse sections of the embryo, same stage; stippled lines in A. D, Part of a sagittal section of the embryo (same stage) passing through the pericardium and heart. Е, Transverse section of the ureter, same stage (enlarged from В). planes of sections indicated by EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 185 FIG. 10. A, Embryo in Stage XII, dorsal view. B, Part of a transverse section of the kidney (same stage) showing folded roof (left) and thin floor (right). C, Part of a longitudinal section of the embryo (same stage) passing through the pericar- dium and heart. 186 DEMIAN AND YOUSIF the ureter and the kidney (K) is formed by a short narrow tube. Two types of cells become differentiated in the wall of the ureter (U, Fig. 9B,E) at this stage. The Ist type comprises large sub-columnar secretory cells with narrow apices, ovoid peripheral nuclei, and a highly vacuolated cytoplasm in which excretory concretions (CON) start to accumulate. The 2nd type consists of columnar cells with ovoid cen- tral nuclei and lightly acidophilic cytoplasm free of excretory material. The 2 branches of the afferent ureteral vein (AUV, Fig. 9B,C) connect posteriorly with the afferent renal vein (ARV). The renal vestibule attains its definitive shape and position in Stage XI when it appears as a small funnel-shaped invagina- tion at the right posterior corner of the mantle cavity. The ureter grows con- siderably, attaining lengths of 0.4 mm in Stage XI and 0.55 mm in Stage XII (U, Fig. 10A). Numerous inner folds project transversely from its wall. Mesenchyme cells and blood lacunae make their appearance within these folds and subse- quently connect with the afferent and efferent ureteral veins serving the organ. Thus the kidney and ureter become well- established towards the end of embryonic life. DISCUSSION Among the chief peculiarities of the mesogastropod family Ampullariidae is the possession of a peculiar ureter which is structured and functions as a kidney, with 2 symmetrical rows of transverse excretory lamellae arising on either side of 2 central longitudinal vessels: the 2 branches of the afferent ureteral vein. Two lateral efferent ureteral veins drain into the afferent ctenidial vein. Posteriorly the ureter communicates with the far more spacious saccular kidney, which has a thick spongy roof with numerous pinnately branched folds. The afferent and efferent renal veins run longitudinally within the roof and branch profusely in its inner folds. The kidney communicates with the pericardial sac by a fine ciliated reno-pericardial tube. This arrangement is essentially similar in all ampullariids (Andrews, 1965). These 2 inter-communicating and struc- turally very distinct excretory organs of the Ampullariidae have for long been thought to be 2 kidneys and were commonly referred to as either the anterior and posterior kidneys, renal chambers or renal lobes (Bouvier, 1888; Burne, 1898; Sachwatkin, 1920; Hagler, 1923; Prashad, 1925; Scott, 1934, 1957; Demian, 1954; Michelson, 1956, 1961; Fretter € Graham, 1962; Andrews, 1965; Starmühlner, 1969). The origin of these 2 functional excretory organs and their homologies with the single kidney of other Mesogastropoda (= Monotocardia or Pectinibranchia) as well as with the 2 kidneys of the Archaeogastropoda (= Diotocardia or Aspidobranchia) were the subject of exten- sive discussions by many authors. The earliest investigators of the morphology of the Ampullariidae only saw the anterior renal chamber (= ureter), which they took to be the kidney (Troschel, 1845; Jourdain, 1879; Sabatier, 1879). Bouvier (1888) was the first to describe “2 kidneys” in Ampullaria ра, an anterior lamellar kidney and a posterior saccular one, but did not mention any reno-pericardial tube. By comparing the blood vessels supplying these 2 kidneys with those supplying the 2 kidneys of an archaeogastropod like Haliotis, Bouvier conjectured that the anterior and posterior kidney chambers of Ampullaria are, respectively, homologous with the right and left kidneys of Haliotis, and of the Archaeogastropoda in general. And since Bouvier was of the opinion that the single kidney found in most Mesogastropoda cor- responded to the topographically right kidney of the Archaeogastropoda, he assumed that the anterior renal chamber (= ureter) of Ampullaria was homologous with the single kidney of other mesogastropods, while the posterior renal chamber (= kidney) of Ampullaria cor- responded to the topographically left kidney of the Mesogastropoda, which dis- appeared during development. After reviewing the then existing EMBRYOLOGY OF MARISA. III. CIRCULATORY AND RENAL SYSTEMS 187 hypotheses on the homologies of the kidney of the Mesogastropoda, Perrier (1889) surmised that the single kidney of most mesogastropods originated by fusion of what corresponded to the right and left kidneys of archaeogastropods. And since the Ampullariidae retained 2 inter- communicating kidneys, he considered them to represent an evolutionary link between the Mesogastropoda and the Archaeogastropoda. Erlanger (1892) inverted the homology suggested by Bouvier (1888) by con- sidering the anterior renal chamber (= ureter) of Ampullaria, and also the single kidney of other mesogastropods, to be homologous with the topographically left kidney of the Archaeogastropoda, while the posterior chamber was homologous with their right kidney. In most mesogastropods the rudiment of that organ disappeared during development or became incorporated in the gonoduct. Ac- cordingly, he theorized that if a reno- pericardial connection was present at all in the Ampullariidae, it should be found between the anterior renal chamber and the pericardium, a prediction proved wrong by Burne (1898). Upon discovering a reno-pericardial tube between the posterior renal chamber and the pericar- dium in A. urceus, Burne rejected Erlanger's interpretation and reverted to Bouvier's (1888) original suggestion that the posterior renal chamber of Ampullaria corresponded to the topographically left kidney of the Archaeogastropoda. Sachwatkin (1920), after surveying earlier evidence, believed that both renal chambers of Ampullaria correspond to the topographically ieft kidney of the Archaeogastropoda, while the right kidney of the Mesogastropoda was modified to form the gonoduct, as suggested by Erlanger. This view subsequently gained general acceptance, although Fernando (1931), who studied the embryonic development the excretory organs in Ampullaria gigas, refuted all previous hypotheses on the homologies of the 2 excretory organs of Ampullaria. He showed that those 2 organs were markedly different in origin and therefore could be neither 2 kidneys nor 2 parts of a single kidney, as suggested by earlier authors. He supplied evidence that only the posterior renal chamber was of mesodermal origin, retained com- munication with the pericardium throughout development, and was therefore а kidney proper. Morphologically it was the right kidney of the embryo, which assumed a position on the left side after torsion. The so-called anterior renal chamber, on the other hand, was ectodermal in origin, opened in the mantle cavity, and was therefore homologous with the ureter of other mesogastropods. Thus Fernando was the first to recognize the ureter and to differentiate between it and the kidney proper in any ampullariid. Ranjah (1942) provided further evidence in support of Fernando's (1931) findings from an extensive embryological study of Pila globosa. He, however, added that a rudimentary left kidney and a left ureter did also develop in the early embryo of Pila, but later became incorporated in the gonoduct, a statement which is neither supported by Fernando's observations in Ampullaria nor by the present findings in Marisa. In spite of the embryological evidence provided by Fernando (1931) and later confirmed by Ranjah (1942), morphologists either ignored Fernando s data (e.g., Starmühlner, 1969) or were hesi- tant to accept them (Scott, 1934, 1957; De- mian, 1954; Michelson, 1956), while some have rejected them outright (Fretter € Graham, 1962; Andrews, 1965); thus the homologies of the excretory organs in the Ampullariidae have remained in dispute. According to Fretter & Graham (1962), the “anterior renal chamber” of Ampullaria should be regarded as being homologous with the dorsal wall of the kidney of other mesogastropods, and not with the ureter, because it has inner folds covered by ex- cretory tissue and vascularized by vessels connected with the ctenidium. Andrews (1965) also did not accept the idea that the “anterior renal chamber’ in Pomacia 188 DEMIAN AND YOUSIF canaliculata and in other ampullariids represented an ectodermal ureter and, on the basis of its excretory nature and its nerve and blood supply, she suspected it to be a mesodermal contribution to the kidney. The present study vindicates Fernando ’s (1931) theory as regards the origin and homologies of the kidney and ureter in the Ampullariidae. Evidence here brought forward for Marisa indicates that this am- pullariid indeed has a single kidney—its so-called posterior renal cham- ber—corresponding to that of other mesogastropods. It is homologous with the topographically left kidney of the Archaeogastropoda. The so-called anterior renal chamber, although lamellated and apparently excretory in function, is un- questionably homologous with the ureter of other mesogastropods, for which reason it has been so termed in this paper. Also, in accordance with the present fin- dings, the terminology commonly used by previous authors (Prashad, 1925; Demian, 1954: Michelson, 1956; Andrews, 1965; Starmühlner, 1969, and others) for the blood vessels supplying the 2 excretory organs in various ampullariids is here changed. The terms afferent and efferent renal veins are now restricted to those blood vessels which have so far been referred to as the “posterior” afferent and efferent renal veins. The terms afferent and efferent ureteral veins are here in- troduced to replace the previous terms “anterior” afferent and efferent renal veins. ‚ The particulars in which the present observations diverge from earlier reports on the origin and development of the cir- culatory and renal organs in related am- pullariids are discussed below. In most molluscs, except perhaps the Cephalopoda, the pericardium, heart and kidney, and often also the gonad, are mesodermal in origin and arise from a common primordium, which may be either paired or unpaired at the beginning (Raven, 1966). In the few Ampullariids, in which the development of the pericar- dium, heart and kidney was examined in detail, it has been asserted that these organs arise from 2 mesodermal rudiments. Both Fernando (1931) and Ranjah (1942), working on Ampullaria gigas and Pila globosa respectively, have correctly described 2 rudimentary aggregates of mesoderm cells, like those described here for Marisa, differentiating in the early embryo on either side of the endodermal sac. However, those 2 masses were then said to grow equally up to a cer- tain stage, then the right mass grew larger. Both masses acquired cavities, thus being transformed into 2 coelomic vesicles referred to as the “right and left rudimen- tary pericardia. The smaller, left, vesicle was stated to shift to the right, coming to lie just beside or below the right vesicle. The 2 vesicles communicated later with each other to form a single sac, within which the heart subsequently developed. In contrast, the present study revealed that only the right mesodermal mass grows and develops into the pericardium, heart and kidney; the left one diminishes quick- ly in size and finally disintegrates into mesenchyme. Marisa thus conforms in this respect with such prosobranchs as Calyp- traea (Salensky, 1872), Bithynia (Erlanger, 1891), Littorina (Delsman, 1914), Patella (Smith, 1935) and Pomatias (Creek, 1951); and with such pulmonates as Arion (Heyder, 1909), Limax (Hoffmann, 1922), Ariophanta (Balsubramaniam, 1953) and Achatina (Ghose, 1963). Fernando (1931) and Ranjah (1942) described 2 rudimentary kidneys develop- ing as 2 evaginations from the so-called “right and left rudimentary pericardia,” before the latter united into а single pericardial sac. Both authors also agreed that the right rudimentary kidney developed into the post-torsional left definitive kidney. But, while Fernando stated that the left rudimentary kidney dis- appeared at an early stage, Ranjah asserted that it persisted, to become later incor- porated in the gonoduct. Semper (1862), however, had described but а single kidney rudiment in Ampullaria polita, and Scott (1934) similarly made no mention of EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 189 a left rudimentary kidney in A. canaliculata. The present observations indicate that the kidney of Marisa is unpaired from the beginning. The kidney rudiment is con- stricted off the common primordium of the pericardium, heart and kidney formed on the right side of the early embryo. No trace of a corresponding left rudimentary kidney was recognized throughout development. Fernando (1931) and Ranjah (1942) moreover spoke of a reno-pericardial “pore” by which the cavity of the kidney communicated with that of the pericardi- um in the ampullariids they examined. They made no mention of а гепо- pericardial tube forming that connection, as did Burne (1898) for Ampullaria urceus, Sachwatkin (1920) for A. gigas, and An- drews (1965) for Pomacea canaliculata. In Marisa, the kidney communicates with the pericardial sac through a distinct reno- pericardial tube which differentiates from the same kidney rudiment and later is enclosed in the cavity of the definitive kidney. Ranjah (1942) not only reported 2 rudimentary kidneys, but also described 2 rudimentary ureters for Pila globosa; the right rudiment developing into the definitive ureter, while the left one con- tributed to the formation of the gonoduct. Fernando (1931) described only a right rudimentary ureter in Ampullaria gigas. The present findings, although agreeing with those of Fernando in as much as they show that the ureter of Marisa is single from the start, conflict with the reports made by both Fernando and Ranjah as regards the details of formation and development of these rudimentary organs. Fernando considered the rudimentary ureter to have developed, in Ampullaria, as a constricted portion of the mantle cavi- ty, and Ranjah described the 2 rudimen- tary ureters of Pila globosa as arising from the mantle cavity by evagination. It is clear from the present report, however, that in Marisa the rudiment of the ureter and renal vestibule arises as an invagina- tion of the ectoderm on the right side of the embryo, long before the mantle cavity has started differentiating. What was con- sidered as the mantle cavity by Fernando and Ranjah corresponds to the renal vestibule here described for the Ist time. The vestibule starts to develop in Marisa as early as Stage IV and becomes later engulfed in the mantle cavity. No trace of a rudimentary gonad, such as that described by Ranjah (1942) for Pila, was recognized in the embryo of Marisa. The gonad as well as the gonoduct have a largely post-embryonic development in Marisa, as in Ampullaria gigas (Fernando, 1931). The present observations also conflict with those of Ranjah (1942) as regards the development of the heart rudiment. Accor- ding to that author, the heart of Pila arises as a single tubular invagination from the wall of the united rudimentary pericardia. That invagination deepens gradually until it meets the opposite wall and perforates it; the heart is then divided by a constric- tion into an auricle and ventricle. But, in Marisa, the rudimentary auricle and ven- tricle are separate at the beginning. They arise as 2 invaginations from 2 nearly op- posite sides of the rudimentary pericardial sac and communicate with each other later. This is somewhat similar to what ob- tains in Achatina (Ghose, 1963). Another characteristic of the Am- pullariidae—the feature from which this family has derived its name—is the posses- sion of a thick-walled,capacious and highly expandable aortic ampulla found on the anterior aorta, almost immediately after it leaves the main aortic trunk. This ampulla is believed to accommodate the blood which may be forced out of the highly vascularized mantle skirt during retraction of the snail into the shell (Andrews, 1965). Morphologists have generally agreed that the aortic ampulla lies within the pericar- dial cavity, directly below the heart (Troschel, 1845; Bouvier, 1888; Prashad, 1925: Scott, 1934; Andrews, 1965). The present investigation, however, has shown that the aortic ampulla lies outside the pericardium from the start. It develops as a haemocoelic sinus below the pericardial sac. Later it is pressed against the floor of 190 DEMIAN AND YOUSIF the pericardial sac until it becomes deeply lodged in it, bulging into the pericardial cavity. The pericardial floor, however, is so thin that upon dissection the ampulla appears to be contained within the pericar- dial cavity. ACKNOWLEDGEMENTS The authors gratefully acknowledge the valuable contribution of Dr. K. Mansour, Emeritus Professor of Zoology, Faculty of Science, Ain Shams University, Cairo, in the supervision of the present work. Thanks are also due to Dr. B. Hubendick, Director of the Natural History Museum in Gothenberg, Sweden, for his continuous interest and support. REFERENCES ANDREWS, E.B., 1965, The functional anatomy of the mantle cavity, kidney and blood system of some pilid gastropods (Prosobranchia). J. Zool., 146: 70-94. BALSUBRAMANIAM, Т.5., 1953, Develop- ment of Ariophanta bristrialis Beck. J. An- namalai Univ., 18:147-154. BOUVIER, E.-L., tion des Ampullaires. Mém. Soc. philomat., Cent. Vol.: 63-85. BURNE, R.H., 1898, A reno-pericardial pore in Ampullaria urceus Müller. Proc. malacol. Soc. Lond., 3: 49-52. CREEK, G.A., 1951, The reproductive system and embryology of the snail Pomatias elegans (Müller). Proc. zool. Soc. Lond., 121: 599-640. DELSMAN, Н.С., 1914, Entwicklungs- geschichte von Littorina obtusata. Tijdschr. ned. dierk. Ver., 13: 170-340. DEMIAN, E.S., 1954, On the macroscopic anatomy of Lanistes carinatus Oliver. M.Sc. Thesis, Ain Shams Univ., Cairo (Published in part). DEMIAN, E.S. & YOUSIF, F., 1973a, Em- bryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). 1. General outlines of development. Malacologia, 12: 123-150. DEMIAN, E.S. & YOUSIF, F., 1973b, Em- bryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). II. Development of the alimentary system. Malacologia, 12: 151-174. 1888, Etude sur | organisa- | ERLANGER, В. von, 1891, Zur Entwicklung von Bithynia tentaculata. Zool. Anz., 14: 385- 388. ERLANGER, R. von, 1892, On the paired nephridia of prosobranchs, the homologies of the only remaining nephridium of most prosobranchs, and the relations of the nephridia to the gonad and genital duct. Quart. J. microsc. Sci., 33: 587-623. FERNANDO, W., 1931, The development of the kidney in Ampullaria (Pila) gigas. Proc. zool. Soc. Lond., 62: 745-750. FRETTER, V. & GRAHAM, A., 1962, British prosobranch molluscs, their functional anatomy and ecology. Ray Soc., Lond., 755 p. GHOSE, K.C., 1963, Morphogenesis of the pericardium and heart, kidney and ureter, and gonad and gonoduct in the giant land snail, Achatina fulica Bowdich. Proc. 3001. Soc. Ind., 16: 201-214. HAGLER, K., 1963, Anatomie von Pachylabra (Ampullaria) cinerea Reeve. Part I. Acta zool., 4: 313-410. HEYDER, P., 1909, Zur Entwicklung der Lungenhöhle bei Arion. Nebst Bemerkungen über die Entwicklung der Urniere und Niere, des Pericards und Herzens. Zt. wiss. Zool., 93: 90-156. HOFFMANN, H., 1922, Über die Entwick- lung des Geschlechtsorgane bei Limax max- imus L. Zt. wiss. Zool., 119: 493-538. JOURDAIN, S., 1879, Sur l’appareil respiratoire des Ampullaires. C. r. Acad. Sci. Paris, 88: 981-983. MICHELSON, E.H., 1956, Studies on the biology of the genus Ceratodes (Mollusca: Pilidae). Doctoral Dissertation, Harvard Univ. (Published in part). MICHELSON, E.H., 1961, On the generic limits in the family Pilidae (Prosobranchia: Mollusca). Breviora, Mus. comp. Zool., Har- vard Coll., 133: 1-10. PERRIER, R., 1889, Recherches sur l'anatomie et l'histologie du rein des gastéropodes prosobranches. Ann. Sci. natur., Zool., 8: 61- 315. PRASHAD, B., 1925, Anatomy of the common Indian apple-snail, Pila globosa. Mem. In- dian Mus., 8: 91-152. RANJAH, A.R., 1942, The embryology of the Indian apple-snail, Pila globosa (Swainson) (Mollusca, Gastropoda). Rec. Indian Mus., 44: 217-322. RAVEN, С.Р., 1966, Morphogenesis: The analysis of molluscan development. Pergamon Press, 2nd Ed., 365 р. EMBRYOLOGY OF MARISA. II. CIRCULATORY AND RENAL SYSTEMS 191 SABATIEER nA, 1879 Sur d'appareil respiratoire des Ampullaires. С. r. Acad. Sci. Paris, 88: 1325-1327. SACHWATKIN, V., 1920, Das Urogenital- system von Ampullaria gigas Spix. Acta zool., 1: 67-130. SALENSKY, W., 1872, Beiträge zur Entwick- lungsgeschichte der Prosobranchier. Zt. wiss. Zool., 22: 428-454. SCOTT, M.LH., 1934, Sobre el desarrollo em- brionario de Ampullaria canaliculata. Rev. Mus. La Plata, 34: 373-385. SCOTT, М.1.Н., 1957, Estudio morfologico у taxonomico de los ampullaridos de la Republica Argentina. Rev. Mus. Argent. Cienc. natur. (Zool.), 3: 233-333. SEMPER, C., 1862, Entwicklungsgeschichte der Ampullaria polita Deshayes. Naturkund. Verh. provinc. Kunsten. Wetensch., Utrecht, 1: 1-20. SMITH, F.G.W., 1935, The development of Patella vulgata. Phil. Trans. Roy. Soc. Lond., В, 225: 95-125. STARMUHLNER, F., 1969, Die Gastropoden der madagassischen Binnengewässer. Malacologia, 8: 1-434. TROSCHEL, F.H., 1845, Anatomie von Am- pullaria urceus und über die Gattung Lanistes Montf. Arch. Naturges., 11: 197- 216. ZUSAMMENFASSUNG EMBRYONALE ENTWICKLUNG UND ORGANOGENESE IN DER SCHNECKE MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). Ш. ENTWICKLUNG DES KREISLAUF-AUD NIERENSYSTEMS E. S. Demian und F. Yousif Perikard, Herz und Niere von Marisa cornuarietis entwickeln sich aus einer einzigen mesodermalen Anlage, die schon früh (Stadium II) auf der rechten Seite des Embryos erkennbar ist. Dieses gemeinsame Rudiment bildet durch Spaltung seiner Zellen einen zentralen Hohlraum, das Coelom, und teilt sich dann durch Abschnürung in einen vorderen Herzbeutel und in eine hintere Niere. Die entsprechende linke Anlage verschwindet bald, indem sie sich in Mesenchymzellen auflöst. Die beiden Anlagen verschmelzen also nicht zu einem einzigen Sack, wie für einige Ampullariiden angegeben. Auch Vor- und Herzkammer entwickeln sich nicht aus einem einzigen Schlauch, der sich später in der Mitte abschnürt, sondern aus 2 getrennten Einstülpungen an entgegengesetzten Seiten des rudimentären Herzbeutels. Diese treten erst später (Stadium VI) in Verbindung und bilden ein schlauchförmiges Herz, das anfänglich fast quer liegt. Durch die Drehung des Eingeweidesacks verlagert sich das Perikard nach links, so dass Vorkammer vor Herzkammer zu liegen kommt. Blutlakunen und Blutgefässe entstehen unabhängig vom Perikard und Herzen aus un- regelmässigen Räumen im Mesenchym des Blastocoels. Sie sind grösstenteils schon während der embryonalen Entwicklung gut ausgebildet; der Anschluss ans Herz jedoch erfolgt erst spät. Es zeigt sich, dass die Aortenampulle unterhalb des Perikards als Sinus in Hoemocoel entsteht und auch später nicht innerhalb des Herzbeutels liegt, sondern in einer tief ins Perikard hineinragenden Einsackung des dünnen Perikardbodens. Der vordere Teil der Urniere verwandelt sich in einen kurzen bewimperten Renoperikardialgang. Der resliche Teil, zuerst schlauchförmig, dann sackförmig, bildet die Niere, in deren Dach sich ein starkes Netzwerk von Blutgefässen entwickelt. Drehung des Eingeweidesackes verlagert die Niere dorsolateral nach links. Der Ureter, ein ebenfalls exkretorisches Organ, das früher für eine zweite Niere gehalten wurde, ist ektodermalen Ursprungs, und bildet sich aus einer schlauchförmigen Einstülpung an der rechten Seite des Embryos. Die Verbindung mit der mesodermalen Niere wird erst später, im IV. Stadium, hergestellt. Der proximale Teil des Ureters besteht aus einem trichterförmigen, hier zum ersten Mal beschriebenen Vestibül. An den Ureterwänden bilden sich stark vaskularisierte innere Querfalten aus, die der Ausscheidung dienen. Durch die Torsion kommt der Ureter vor der Niere zu liegen. 192 DEMIAN AND YOUSIF Beide Organe befinden sich nun im Mantelhöhlendach; Vestibül und Aussenmündung liegen tief in der Mantelhöhle. Dadurch, dass erwiesen wurde, dass die Niere homolog mit der topographisch links gelegenen Niere der Archaeogastropoden ist und dass der Ureter nicht mit deren rechter Niere homolog ist, sondern mit dem Ureter anderer Mesogastropoden, trägt diese Unterschung zur Klärung der in den Ampullariiden strittigen Homologien dieser Organe bei. А.С. RESUME DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGENESE CHEZ MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). Ш. DEVELOPPEMENT DES APPAREILS CIRCULATOIRE ET EXCRETEUR Е. 5. Demian et Е. Yousif Le péricarde, le coeur et le rein de Marisa cornuarietis apparaissent á partir d'un seul feuillet mésodermique commun qui est différencié trés tot (Stade II) sur le cóté droit de l'embryon. Cette ébauche commune développe une cavité centrale, le coelome, par clivage de ses cellules puis se devise а la suite d'une constriction en un péricarde antérieur et un rein postérieur. Une ébauche correspondante du cóté gauche disparait tót en se transformant en mésenchyme. Ainsi les deux ébauches ne fusionnent pas pour former un sac unique, comme cela a été décrit pour certains Ampullariidés. L oreillette et le ventricule ne se développent pas comme un unique tube qui plus tard subirait une constriction médiane, mais comme deux invaginations séparées provenant des deux cótés opposés du sac péricardique initial. Elles entrent en communication plus tard (Stade VI), formant un coeur tubulaire qui, initialement, est placé presque transver- salement. Une torsion ultérieure déplace le péricarde vers le cóté dorso-latéral gauche et méne l'oreillette en face du ventricule. Des sinus hémocoeliens et des vaisseaux sanguins se développent indépendamment du péricarde et du coeur, а partir de lacunes du mésenchyme dans le blastocoele. La plupart de ceux-ci s élaborent pendant la vie embryonnaire et se mettent en relation avec le coeur au stade final. On a montré que Гатроше aortique se développe comme un sinus hémocoelique placé sous le péricarde, qui plus tard, ne se situe pas dans le sac péricar- dique mais se loge dans un profond renflement interne du plancher de ce sac. La partie antérieure du rein rudimentaire se transforme en un court tube réno- péricardique cilié. Le reste forme le rein qui, d'abord tubulaire, puis sacculaire, développe un épais plexus de vaisseaux sanguins dorsalement. La torsion déplace le rein dorsolatéralement sur la gauche. L uretére, organe excréteur entierement fonctionnel, précédemment considéré comme étant un autre rein, est d’origine ectodermique et apparaît sous forme d'une invagination tubulaire sur le seul côté droit de l'embryon. Il communique plus tard avec le rein mésodermique (Stade IV); sa partie proximale forme un vestibule rénal en forme d'en- tonnoir, pour la premiere fois décrit ici. Les parois de l'uretére développent des replis in- ternes transversaux qui se vascularisent abondamment. L'uretére se déplace en face du rein pendant la torsion, venant se placer dans la partie dorsale de la cavité palléale, tandis que le pore excréteur et le vestibule rénal sont profondément enfermés dans la cavité palléale. En démontrant que le rein est homologue du rein gauche topographique des Archaeogastropodes et que l'uretére n'est pas l'homologue de leur rein droit mais de l'uretére des autres Mésagastropodes, cette étude contribue à clarifier les homologies controversées de ces organes chez les Ampullariidae. ASE. EMBRYOLOGY OF MARISA. Ш. CIRCULATORY AND RENAL SYSTEMS 193 RESUMEN DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). III. DESARROLLO DE LOS SISTEMAS CIRCULATORIO Y RENAL E. S. Demian y F. Yousif El pericardio, corazón y riñón de Marisa cornuarietis nacen de una masa de células mesodermales, simple, que se diferencian temprano (II estado) sobre el lado derecho del embrión. Este rudimento común desarrolla una cavidad central, el celoma, por el desdoblamiento de sus células, dividiéndose después por constricción en un saco pericar- dial anterior y un riñón posterior. Un rudimiento izquierdo, correspondiente, desaparece enseguida, desintegrándose en mesenquima. De tal manera, los dos rudimentos no se fusionan para formar un saco único, como se habia registrado para algunos ampularidos. La aurícula y ventrículo no se desarrollan como un tubo único para contraerse en el medio, sino como 2 invaginaciones separadas de 2 lados opuestos del saco pericardial rudimentario. Después se intercomunican (VI estado) para formar un corazón tubular el cual, al principio, descansa casi transversalmente. La torsión luego lleva el pericardio al lado dorso-lateral y trae la auricula frente al ventrículo. Senos homocélicos y vasos sanguíneos desarrollanse independientemente del pericar- dio y corazón, de los espacios irregulares de la mesenquima dentro del blastocelo. Muchos de estos quedan bien establecidos durante la vida embrionaria, conectandos al corazón en un estado posterior. La ampolla aórtica ha mostrado la formación de un seno homocélico debajo del pericardio, pero no se ubica más tarde dentro del saco pericardial, sino en una profunda comba hacia adentro del techo del saco. La parte anterior del riñón rudimentario se transforma en un tubo reno-pericardial, corto y ciliado. El resto forma el riñón, el cual siendo primero tubular y después sacular, produce en su techo una gruesa red vasos sanguíneos. La torsión lleva el riñón dorso- lateralmente a la izquierda. La uretra, un órgano excretor funcional completo, (se habia considerado previamente como otro riñón), es de orígen ectodermico y se forma por una invaginación tubular sólo en el lado derecho del embrión. Más tarde se comunica con el riñón mesodermal (IV es- tado); su parte proximal forma un vestibulo renal como un embudo, que se describe aquí por primera vez. Las paredes de la uretra desarrollan pliegues internos transversales, los cuales se vascularizan en manera abundante. La uretra se muda frente al riñón durante la torsión, viniendo a colocarse en el techo de la cavidad paleal, mientras que la abertura de excresión y el vestibulo renal quedan profundamente envueltos en la cavidad del manto. Al demonstrar que el riñón es homólogo con el, topograficamente, riñón izquierdo de los Archaeogastropoda, y que la uretra no es homóloga con el riñón derecho sino con la uretra de otros Mesogastropoda, este estudio contribuye a la clarificación en la controver- sia sobre homologías de tales órganos en los Ampullariidae. J.J.P. 194 DEMIAN AND YOUSIF АБСТРАКТ ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIDAE) Ш. РАЗВИТИЕ ЦИРКУЛЯЦИОННОЙ И ПОЧЕЧНОЙ СИСТЕМ 9. ДИМЬЯН И Ф. KCH Перикардий, сердце и почки у Marisa cornuarietis происходитя от одного общего мезодермального образования, которое диференцируется довольно рано (на П стадии) на правой стороне эмбриона. Этот общий рудимент образует центральную полость, целом, путем расщепления его клеток, а затем разделяется путем стягивания их и образования переднего перикардиального мешка и задней почки. Соответственно, левый рудимент вскоре исчезает, перерождаясь в мезенхиму. Таким образом, в данном случае 2 рудимента не сливаются, чтобы образовать единый мешок, как это наблюдалось раньше у некоторых Ampullariidae. Предсердие и желудочек не представляют собой единой трубки, которая позже образует перетяжку посредине, HO образована двумя отдельными инвагинациями e двух противоположных сторон рудиментарного перикардиального мешка. Позже они образуют внутренние коммуникации (на У1 стадии) и сердечную трубку, первоначально расположенную почти поперечно. Наступающая позднее торсия смещает перикардиум налево и дорзо-латерально, предсердие оказывается перед желудочком. Синусы гемоцёля и кровеносные сосуды развиваются независимо от перикардия и сердца от неправильно-расположенных лакун внутри бластоцёля. Большая их часть хорошо развивается втечение эмбрионального периода жизни, соединяясь с сердцем на поздних стадиях развития. Было показано, что ампула аорты развивается как синус гемоцёля, под перикардием; позже он уже находится не внутри перикардиального мешка, а помещается в глубокой вдавленности, имеющейся в тонкой стенке этого мешка. Передняя часть рудиментарных почек трансформируется в короткую реснитчатую почечно-перикардиальную трубку. Остальная часть - сначала - трубчатая, затем мешковидная, образует почки, которые развивают на своей стенке толстое сплетение кровеносных сосудов. Торсионный процесс сдвигает почки дорзо - латерально и налево. Уретра - это полноценно-функционирующий выделительный орган прежде считавшаяся другой почкой, имеет эктодермальное происхождение и возникает с правой стороны эмбриона, ввиде трубчатой инвагинации. Позже она связывается с мезодермальной почкой (стадия 1У); её проксимальная часть образует воронковидную почечную вестибулу, впервые описанную в настоящей статье. Стенки уретры образуют поперечные внутренние складки, пронизанные большим количеством кровеносных сосудов. Торсионный процесс сдвигает ‘уретру кпереди от почки так, что она лежит в стенке мантийной полости, в то время как экскреторное отверстие и почечная воронка оказываются глубоко погруженными в мантийную полость. В статье показано, что в данном случае почка по местоположению гомологична левой почке Archaeogastropoda, но что ypeTpa не является гомологом их правой почки, а соответствует уретре других Mesogastropoda. Изложенные в статье материалы выясняют противоречивость суждений об этих органах у Ampullariidae. Z.A.F. MALACOLOGIA, 1973, 12(2): 195-211 EMBRYONIC DEVELOPMENT AND ORGANOGENESIS IN THE SNAIL MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). IV. DEVELOPMENT OF THE SHELL GLAND, MANTLE AND RESPIRATORY ORGANS! Emile 5. Demian? and Fouad Yousif? ABSTRACT A “rudimentary shell gland” starts differentiating at the aboral end of the early em- bryo as a median thickened ectodermal plate. It invaginates to form a cup-shaped hollow, shifts to the left and secretes a delicate cuticular larval shell. Its central part then bulges up and its epithelium flattens. Together with the larval shell, it spreads circularly over the visceral sac rudiment, extending beyond it. Ultimately it forms the outer epithelium of the visceral mass and mantle. A peripheral epithelial rim remains thicken- ed, and will form the definitive shell gland. The larval shell persists as a layer of the adult shell. Contrary to earlier reports on related ampullariids, the mantle cavity develops relative- ly late, only after the onset of torsion. Starting as a depression or groove on the right dorso-lateral wall of the visceral sac rudiment, it gradually transforms into a deep cavity as it becomes overgrown by the mantle. The ectoderm, engulfed by that cavity, forms its internal lining and the inner mantle epithelium. During torsion the mantle opening shifts to face forwards. The ctenidium was shown to be ontogenetically older than the mantle cavity. Its rudi- ment starts differentiating early as a thickened ectodermal plate in the right wall of the visceral sac rudiment. It secondarily passes into the mantle cavity during torsion when it shifts to the left side, extending forwards as the mantle grows anteriorly. Transverse epithelial folds develop on it to later form the ctenidial lamellae. The lung, a structure peculiar, within the prosobranchs, to the Ampullariidae, starts developing shortly before hatching as a broad invagination in the roofing epithelium of the mantle cavity, between the ctenidium and osphradium. The epithelial rim edging the invagination grows centrad from the periphery to form the floor of the lung cavity, leav- ing open a narrow slit which persists as the pneumostome. The lung grows enormously after hatching, displacing the ctenidium to the right side. These findings indicate that the lung is a new acquisition in the Ampullariidae. It is not a modified 2nd ctenidium and does not seem to have any direct ancestral relationship with the lung of pulmonates. The accessory breathing organs, i.e., the pallial fold or “epitaenia” and the 2 nuchal lobes (siphons) also develop late, as folds of the epithelium in the floor of the mantle cavi- ty. They attain their definitive shapes and positions after hatching. INTRODUCTION The present investigation is the 4th in a series of embryological studies carried out on Marisa cornuarietis (L.), a freshwater ampullariid gastropod of potential impor- tance in the biological control of schistosome-transmitting snails. The Ist part of the series (Demian & Yousif, 1973a) included a description of the early cleavage, gastrulation and the general outlines of the process of em- bryonic development. Twelve embryonic stages were distinguished. The 2nd part (Demian & Yousif, 1973b) covered the em- 1 This investigation was supported in part by research grants (Al 04906 and Al 07696) from the National Institute of Allergy and Infectious Diseases, U.S. Public Health Service. 2 Department of Zoology, Faculty of Science, Ain Shams University, Cairo. 3 Laboratory of Bilharziasis Research, National Research Centre, Cairo. (195) 196 DEMIAN AND YOUSIF bryogenesis of the alimentary system, and the 3rd part (Demian & Yousif, 1973c) that of the circulatory and renal systems. In the present report, a detailed descrip- tion is given of the origin and embryonic development of the shell gland, mantle, mantle cavity and respiratory organs. Fin- dings are compared with earlier informa- tion on other Ampullariidae. The gross and microscopic anatomy of the mantle and respiratory organs of adult Marisa cor- nuarietis have been described in previous publications (Demian, 1965; Lutfy & De- mian, 1965) which may be consulted for details of structure and function of these organs. The present observations were made on the same material and sets of serial sec- tions that furnished the basis for all other parts of the series. The material and techniques employed have already been described in the Ist part of the series, to which reference should also be made for the age, dimensions and diagnostic features of the different embryonic stages which are frequently referred to below. KEY TO LETTERING ON FIGURES! 1 auricle afferent ctenidial vein ANP anal cell-plate СИ. ciliated ridge CN ctenidium DGP posterior lobe of digestive gland E eye ECV — efferent ctenidial vein EN endoderm EPT _ pallial fold or “epitaenia” ET ectoderm Е foot СВ goblet cell GZS sorting area of gizzard Н head I intestine K kidney I lung or pulmonary sac LGS left gastric streak LNL | left nuchal lobe LPPG left pleuro-pedal ganglionic mass LS larval stomach MS mesoderm or mesenchyme cells MT mantle МТС mantle cavity MTE mantle edge OS osphradium В pericardium PG pericardial cavity PDP _ pedal cell-plate PO pulmonary opening EN prototroch RGS right gastric streak ENL right nuchal lobe ENV renal vestibule RT rectum SD stomodaeum SH shell (protoconch) SHG shell gland SHGR rudimentary shell gland SPG supraintestinal ganglion STC statocyst TN tentacle l ureter V ventricle VS visceral sac 1. Shell gland and mantle A “rudimentary shell gland’ (SHGR, Fig. 1A,B), which is in fact the common rudiment of the mantle and the shell gland, differentiates early in the ectoderm (ET, Fig. 1B) at the aboral or “posterior” side of the embryo in Stage II. It appears as a thickened median circular plate of a single layer of tall columnar cells with sub- basal ovoid nuclei and a densely granular cytoplasm. This rudimentary structure considerably enlarges in the following stage and simultaneously invaginates, for- ming a cup-shaped median depression (SHGR, Fig. 2A,B) about 60 u in diameter and 40 u deep. As the invaginated rudiment con- tinues to enlarge in subsequent stages, it gradually shifts to the left until it comes to lie left of the median line in Stage V (SHGR, Fig. 3A). Meanwhile, its cells (SHGR, Fig. ЗВ) have produced a thin cuticular secretion of uniform thickness, the larval shell or protoconch (SH), which lines the whole invaginated rudiment. The epithelium around the opening of the in- vagination forms a slightly projecting fold ЗАП drawings are of Marisa cornuarietis (L.). The general views are reconstructions of the shell gland, mantle and respiratory organs made from serial transverse and sagittal sections. EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 197 that will develop into the free mantle edge (MTE) of the adult. As development proceeds, the т- vaginated rudiment further enlarges. Its central part bulges up, gradually rising out of the opening of the invagination. The rudiment thus acquires a cap-like form in Stage VI (Fig. 4A). The cells at the periphery remain tall, forming a circular marginal thickening (SH +, Fig. 4B) which eventually will develop into the definitive shell gland. The epithelium in the central part of the bulge, on the other hand, grows thinner. The mantle first appears at the onset of torsion (Stage VII) as a consequence of the rapid growth of the epithelium of the cap. This epithelium further thins as it grows and spreads over the left half of the vis- ceral mass (VS, Fig. 5A) in Stage VIII. Its flattened cells (Fig. 5B) harbour ellip- tical nuclei in their thickest central por- tions. This epithelium continues to grow until it covers the whole visceral sac; it then extends beyond the sac to form the outer epithelium of the mantle (MT, Figs. 6C, 8B) which has now become con- spicuous. The thin cuticular secretion elaborated by this epithelium simultaneously spreads on the outer sur- face of the visceral sac and mantle forming a cup-shaped thin larval shell (SH, Figs. 5A,B; 6A-C; 7; 8A,B) that reflects the shape of these organs. As these developments take place, the thickened margin (SHG, Fig. 4A,B) of the original rudiment, which represents the actual anlage for the definitive shell gland, further thickens and enlarges (Fig. 5A,B). The circular ectodermal fold, which will form the future mantle edge (MTE), projects around the rudiment of the shell gland (SHG), the 2 being separated by a conspicuous mantle groove. In subsequent stages, the shell gland (SHG, Figs. 6A,B; 7) and the mantle edge (MTE) are gradually carried forward, as a result of the forward prolongation of the mantle (MT), until they come to occupy their definitive positions around the head in Stage XI (Fig. SA). The shell gland at that stage consists of narrow columnar cells with ovoid nuclei and a highly chromophilic cytoplasm. Mesenchyme cells aggregate below its cells, and unicellular glands make their appearance among them shortly before hatching. The larval shell remains part of the adult shell. Secretions added to it from the shell gland and the outer epithelium of the mantle contribute later to the formation and growth of the definitive shell. 2. Mantle cavity The mantle cavity also develops relatively late in Marisa cornuarietis, i.e., only after torsion has begun (Stage VII). When the visceral sac starts rotating anti- clockwise as a result of torsion, a con- spicuous depression or groove shows on its right dorso-lateral side marking the begin- ning of formation of the mantle cavity (MTC, Fig. 5A,B). This groove gradually deepens as it becomes overgrown in sub- sequent stages by the developing mantle, being finally transformed into a deep cavi- ty whose wide external opening 15 рег- manently retained and serves as the man- tle opening. During torsion, as mentioned above, the ectoderm, which in Stage VIII is on the left side of the visceral sac rudiment (VS, Fig. 5A) and which is originally derived from the epithelium of the “rudimentary shell gland,” grows rapidly so as to cover the whole visceral sac rudiment (VS, Fig. 6A,B) and to project as a thick lobe (MT) over and a little beyond the mantle cavity in Stage IX (MTC, Figs. 5A,B; 6A-C). While the visceral sac bulges out on the left side, the ectoderm, which was situated on the right side of the visceral sac rudi- ment up to Stage VIII, caves in, coming to lie inside the mantle cavity and now for- ming its inner lining as well as the inner epithelium of the mantle growing over it. Certain structures, such as the rudimen- tary ctenidium (CN, Figs. 3A,B; 4A,B), which has already started differentiating in that ectoderm in earlier stages, are similarly engulfed in the developing man- tle cavity (Figs. 5B, 6B). The mantle (MT, Figs. 6A,C; 7) gradually prolongs anteriorly during sub- 198 DEMIAN AND YOUSIF FIG. 1. A, Embryo in Stage И showing the rudimentary shell gland, left lateral view. B, Part of a sagittal section of the embryo (same stage), passing through the rudimentary shell gland. A, Embryo in Stage III, left lateral view. B, Part of a sagittal section of the embryo (same stage), passing through the rudimentary shell gland. FIG. 3. A, Embryo in Stage У, dorsal view. B, Transverse section through visceral sac of embryo, same stage; plane of section in- dicated by stippled line in A. FIG. bo EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 199 es | 0.1mm FIG. 4. A, Embryo in Stage VI, dorsal view. B, Transverse section through visceral sac of embryo, same stage; plane of section in- dicated by stippled line in A. FIG. 5. A, Embryo in Stage VIII, dorsal view. В, Transverse section through visceral sac of embryo, same stage; plane of section in- dicated by stippled line in A. 200 DEMIAN AND YOUSIF sequent development, arching over the head vesicle, until it attains its definitive shape and position in Stage XI (MT, Fig. ЗА, В). By this same process, the mantle cavity (MTC, Figs. 6A-C; 8B) has grown conspicuously larger and deeper. Its wide external opening, originally facing to the right (Fig. 5A), shifts during torsion so as to face forwards (Stage X, Fig. 7), and on account of the simultaneous growth of the mantle and mantle cavity it lies close behind the head in Stage XI (Fig. 8A). 3. Ctenidium Marisa, like all other ampullariids, possesses a single monopectinate ctenidium. In the adult the organ consists, on the average, of 350 thin flattened triangular lamellae hanging from the man- tle roof with their apices pointing into the mantle cavity. The 2 free lateral edges of each lamella are unequal in length, the right or afferent edge being shorter than the left or efferent edge (Demian, 1965). The rudiment of the ctenidium (CN, Fig. 3A.B) first differentiates in Stage У as a thickened oval ectodermal plate on the right side of the visceral sac rudiment (VS, Fig. 3A). This plate measures about 40 u across. Its cells (CN, Fig. 3B) are tall, columnar and have a densely granular cytoplasm and ovoid sub-basal nuclei relatively rich in chromatin material. They proliferate rapidly, giving rise to a mul- titude of elliptical, polygonal and irregular cells which aggregate below the ctenidial rudiment (CN, Fig. 4B). When torsion begins, the rudimentary ctenidium, along with the ectoderm covering the right side of the visceral sac rudiment, is gradually drawn inside the developing mantle cavity. In Stage IX, the whole rudiment (CN, Fig. 6A,B) has been enclosed within the mantle cavity (MTC), i.e., it now lies on the inner epithelium of the mantle (MT, Fig. 6C) just behind the mantle opening. It has also elongated, shifted a little to the left, and has acquired the shape of a J, with the longer and broader right limb projecting ahead of the left limb (CN, Fig. 6B). Meanwhile, transverse epithelial folds, which will later form ctenidial leaflets or lamellae, started developing at the broader anterior end of the organ. Two or 3 of these rudimentary ctenidial lamellae are conspicuous in Stage IX, where the organ measures about 0.2 mm in length. As the mantle stretches forward in Stage X, the ctenidium (CN, Fig. 7) further elongates and shows new transverse epithelial folds behind the older ones, with a total of 7 ctenidial lamellae at that stage. Each rudimentary lamella is a double- walled flattened fold with an epithelial covering of cuboid cells that have a vacuolated cytoplasm and relatively large spherical nuclei. Mesenchyme cells from the segmentation cavity migrate inside these lamellae, leaving irregular haemocoelic lacunae in between them. In Stage XI, the ctenidium (CN, Fig. ЗА, В) shifts further forward, coming to lie in front of the heart (A,V) and kidney (K). It is now about 0.35 mm long and extends obliquely along the roof of the mantle cavity, parallel with the ureter (U, Fig. SA). The afferent and efferent ctenidial veins (ACV, ECV) become conspicuous along the 2 lateral edges of the organ. Twelve ctenidial lamellae are developed at this stage and project considerably into the mantle cavity (MTC, Fig. 8B). Transverse sections of these lamellae show that each has developed a narrow ciliated ridge on its anterior and posterior surfaces, running near to and parallel with its left or efferent edge. As development proceeds through Stage XII, the ctenidium further lengthens and now projects far in front of the anterior tip of the ureter. It is about 0.7 mm long at this stage and carries 20 ctenidial lamellae. The largest of these lie near the anterior end of the organ, their sizes decreasing gradually towards both ends. The epithelial cells covering the lamellae have already started differentiating (Fig. 9). Numerous basophilic granules accumulate within their apical ends and a few goblet cells (GB) differentiate between them, es- pecially near the bases of the lamellae. The cells in the ciliated ridges (CIL) carry long cilia and have a vacuolated cytoplasm. The EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 201 FIG. 6. A,B, Embryo in Stage IX, in right lateral (A) and dorsal (B) views, showing the mantle (MT) enclosing the developing mantle cavity (MTC). The ctenidial lamellae are shown in transparency as dark bands in B. C, Transverse section through visceral sac of embryo, same stage; plane of section in- dicated by stippled line in B. 202 DEMIAN AND YOUSIF FIG. 7. Embryo in Stage X, dorsal view. FIG. 8. A, Embryo in Stage XI, dorsal view. B, Transverse section of the embryo, same stage; plane of section indicated by stippled line in A. FIG. 9. Transverse section of a ctenidial lamella from the embryo in Stage ХИ passing parallel to the afferent edge and showing ciliated ridges on efferent edge. EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 203 narrow inner space found within each lamella is filled with mesenchyme cells (MS) of various forms and encloses irregular haemocoelic sinuses. At the time of hatching, the greater por- tion of the ctenidium still lies on the left side of the mantle roof. After hatching, the organ is displaced to the right side as a result of the enormous development of the lung on the left side. New ctenidial lamellae are continuously added at the posterior end of the organ. Thus there are 30, 50 and 75 lamellae, respectively, in snails 1, 3 and 5 weeks old (CN, Figs. 11- SI) 4. Lung or pulmonary sac Although essentially aquatic and breathing with a ctenidium, the Am- pullariidae have also developed a lung by means of which they use atmospheric air, apparently an adaption to life in habitats with foul water conditions and periodic droughts. Adult Marisa cornuarietis possesses a more or less rectangular, spacious, pouch-like lung or pulmonary sac hanging from the roof of the mantle cavity on the left side. The roof of this sac is formed by the thin mantle. Its floor is thick, highly vascularized and perforated near its left anterior corner by a small ovoid pulmonary opening ог pneumostome (Demian, 1965). The lung, as the ctenidium, is ectoder- mal in origin, but develops much later. The lung rudiment (Г, Fig. 7) starts differentiating in Stage X as a small oval disc of cuboid to flattened cells in the epithelium lining the roof of the mantle cavity, between the ctenidium (CN) and osphradium (OS). This rudimentary disc becomes invaginated in Stage XI (L, Fig. 8A,B); the invagination then enlarges, without any further differentiation, until the embryo hatches. The epithelium around the edge of the invagination thus forms a thick projecting continuous fold, which gradually grows over the concavity and towards the center, thus separating the lung cavity from the mantle cavity. The floor of the lung rudiment does not close entirely; a narrow slit-like opening is spared out and persists as the pneumostome in the adult. In a snail 1 week old (about 2 mm diameter) the lung (L, Fig. 11) shows as an elongated dorso-ventrally compressed sac, 0.7 mm in length and 0.1 mm in maximum width, with a slit-like pneumostome (PO), about 0.6 mm long. Thereafter the lung gradually increases in size, displacing the ctenidium to the right side. It attains a length of about 1 mm and a width of 0.4 mm in snails 3 weeks old (L, Fig. 12), and measures 1.7 by 1.4 mm in snails 5 weeks old (L, Fig. 13); the pneumostome (PO) has widened and assumed a triangular outline. The in- crease in floor area thereafter is more pronounced to the right of and behind the pneumostome, which therefore retains a position near the anterior left corner of the pulmonary sac. 5. Pallial.fold and nuchal lobes The chief accessory respiratory organs in the Ampullariidae are the pallial fold, or “epitaenia of Ihering (1887), and the 2, right and left, nuchal (neck) lobes or siphons. In adult Marisa (Demian, 1965), the epitaenia is a prominent ciliated longitudinal fold running along the entire length of the floor of the mantle cavity un- derneath the strip of the roof separating the ctenidium from the lung. It plays a major role in creating the respiratory water current that flows inside the mantle cavity and bathes the ctenidium, and in shutting off the cavity around the ctenidium during aerial respiration. It also separates from the rest of the mantle cavity a narrow channel on the right side of the mantle floor, along which excretory and waste products are passed out with the exhalant stream. The nuchal lobes are 2 highly muscular, flattened, flaps which project anteriorly from the floor of the mantle cavity, one on either side of the head. Unlike aquatic pulmonates, ampullariids are unable to bring the pulmonary opening directly to the water surface. Thus during pulmonary respiration, their pneumostome is moved forward only a lit- 204 DEMIAN AND YOUSIF FIG. 10. Part of a transverse section of the embryo in Stage XII, passing through the epitaenia. FIGS. 11-13. Mantle cavity and respiratory organs of juvenile snails 1 week (11), 3 weeks (12) and 5 weeks (13) after hatching. The shell is removed and the mantle is cut along the right edge of the ctenidium and reflected to the left so as to expose the mantle cavity. EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 205 tle and apposed to the base of the left nuchal lobe which rolls itself into a tube or siphon that reaches to the surface film. At- mospheric air passes in and out of the lung cavity through that siphon. The right nuchal lobe aids in aquatic respiration by forming a shallow gutter that directs the exhalant water current from the mantle cavity away from the head. The epitaenia first appears in Stage XI of the embryo as a small epithelial fold which projects transversely on the floor of the mantle cavity. Its epithelium consists of columnar to cuboid cells with relatively large ovoid nuclei. It gradually increases in length and height in subsequent stages, while 2 types of cells (EPT, Fig. 10) become differentiated in its epithelium. The majority of the cells are ciliated, columnar, with highly acidophilic granular cytoplasm and central or apical ovoid nuclei. The 2nd type consists of non- ciliated narrow columnar cells with less acidophilic cytoplasm and small elliptical nuclei located at various levels within these cells. The epitaenia elongates after hatching (EPT, Figs. 11-13), but does not assume its definitive form and its complete course along the floor of the mantle cavity until 4- 5 weeks after hatching. ; The left and right nuchal lobes are first seen in Stage XII as 2 small ectodermal folds on either side of the head. These 2 folds (LNL, RNL, Fig. 11) grow forward and expand laterally after hatching, reaching from behind the 2 eyes to the free mantle edge, while 2 types of cells differentiate in their epithelial covering. Some cells are ciliated and have a marked- ly acidophilic cytoplasm, while others are glandular and goblet-like. The histology of the fully-developed ctenidium, lung, epitaenia and nuchal lobes has been described in a previous publication (Lutfy € Demian, 1965). DISCUSSION A so-called “rudimentary shell gland,” more or less similar to that here described for Marisa cornuarietis, seems to be com- mon to all gastropods and to develop similarly into the shell gland of the adult and the outer covering epithelia of the visceral mass and the mantle (Ghose, 1963; Raven, 1966). The present account of the early differentiation and course of development of the “rudimentary shell gland” in Marisa generally agrees with observations made by some earlier authors on the correspond- ing structure in other ampullariids, i.e., in Ampullaria depressa by Brooks & McGlone (1908), in A. gigas by Fernando (1931), in A. canaliculata by Scott (1934) and in Pila globosa by Ranjah (1942). There is considerable disagreement, however, as regards the development of the mantle cavity and the method by which the rudimentary shell gland con- tributes to the formation of the mantle. According to both Fernando (1931) and Ranjah (1942), the mantle cavity develops as a mid-ventral invagination of the ec- toderm of the visceral sac rudiment at a very early embryonic stage. The invagina- tion grows into a tubular structure from which the ureter takes origin on the right side. This tube, the rudimentary mantle cavity, is shifted to the right side of the visceral sac during torsion, is constricted off from the ureter, and is finally moved to the dorsal side by the end of torsion. The sequence of events during torsion, as out- lined by those 2 authors, is not clear. Brooks € McGlone (1908) and Scott (1934), on the other hand, made no men- tion of such an invaginated mantle cavity rudiment in the early embryos of the am- pullariids they examined, and did not see a mantle cavity before the beginning of tor- sion. The present study revealed that, in Marisa, the mantle cavity does not arise at an early stage but only at a relatively late stage, after the onset of torsion. It does not start as a ventral tubular invagination, but as a depression or groove on the right dorso-lateral side of the visceral sac rudi- ment, as a consequence of torsion. This depression becomes later overgrown by the mantle, by which process it is transformed into a deep mantle cavity. Marisa is not unique in this respect. The 206 DEMIAN AND YOUSIF mantle is known to start in various other gastropods as a groove or a pair of grooves in the wall of the visceral sac rudiment, and to become secondarily overgrown by the mantle, as described for Paludina (Drummond, 1903), Haliotis (Crofts, 1938) and Pomatias (Creek, 1951) among the Prosobranchia; and for Planorbis (Rabl, 1879), Arion (Heyder, 1909), Agriolimax (Carrick, 1939), Ariophanta (Balsubramaniam, 1952) and Achatina (Chose, 1963) among the pulmonates. The conflict between the present obser- vations and those made by Fernando (1931) and Ranjah (1942) is doubtlessly due to a misinterpretation: from their il- lustrations and descriptions it is clear that they must have taken the rudiment of the ureter and renal vestibule, such as here observed in Marisa, for a rudimentary mantle cavity. The former rudiment arises as a tubular ectodermal invagination in the early embryo, its opening shifts to the right during torsion and is then drawn into the mantle cavity (Demian & Yousif, 1973с). Earlier authors dealing with the development of the ctenidium in the Am- pullariidae generally agreed that this organ started to differentiate at a late em- bryonic stage from a thickening in the ec- toderm lining the mantle cavity. Brooks & McGlone (1908) and Scott (1934), in the embryos of the Ampullaria spp. they in- vestigated, did not recognize the ctenidium until the mantle cavity was developed. Fernando (1931) asserted, for A. gigas, that the organ did not start differentiating until torsion was com- pleted, and Ranjah (1942) reported that in Pila it developed at a late stage, com- parable to our embryonic Stage VIII. The descriptions given by those earlier authors suggest that they probably overlooked the early anlage of the ctenidium and failed to distinguish the organ until it had developed a few ctenidial lamellae. That Fernando (1931), Scott (1934) and Ranjah (1942) observed and figured a number of well-defined lamellae on the rudimentary ctenidium, right after the completion of torsion, im- plies that the rudiment must have started differentiating a few stages earlier. Ranjah (1942) did describe a rudimentary thicken- ing in the right wall of the visceral sac of the early embryo of Pila, but apparently mistook it for the rudiment of the visceral ganglion; the thickening, however, evi- dently corresponds to the rudiment of the ctenidium here described in Marisa. The present investigation has clearly shown that the ctenidium, in Marisa, is on- togenetically older than the mantle cavity. Its early rudiment starts differentiating on the right wall of the visceral sac rudiment before either torsion begins or the mantle cavity forms. It later passes inside the mantle cavity, and ctenidial lamellae begin to develop on it. In some other prosobranchs such as Crepidula, Fulgur and Fasciolaria (Raven, 1966), the ctenidium similarly differentiates at a very early embryonic stage and is secondarily taken into the mantle cavity. It may be worthy of note that the ctenidium of Marisa, which originates on the right side of the embryo and corre- sponds morphologically to the right cteni- dium of the Archaeogastropoda, comes lie on the left side of the advanced embryo after torsion, and that, as a result of the development of the voluminous lung on the left side after hatching, it then again becomes displaced to the right side. The Ampullariidae are the only prosobranchs which have a well- developed lung in addition to the ctenidium. Such a peculiar development has raised much speculation and several important questions which have long been discussed and disputed by general morphologists and systematists. Among these questions are: How has this lung appeared? Is it a modified ctenidium or a new acquisition? Has it any ancestral connection with the lung of pulmonates? Brooks € McGlone (1908) were probably the first to advance some answers, basing themselves on an em- bryological study of the respiratory organs in Ampullaria depressa. They reported that the ctenidium, osphradium and lung developed simultaneously or nearly so EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 207 from the inner epithelium of the mantle, the ctenidium and osphradium developing as 2 parallel ridges on that epithelium, and the lung arising as an infolding of the epithelium between them. They conclud- ed therefrom that, in Ampullaria, the ctenidium, osphradium and lung con- stituted a series of homologous structures, specialized in differing directions, and that the lung might be regarded as represen- ting one or more modified gill lamellae. Prashad (1925), who agreed to that view, further suggested that the lung might be a modified part of a 2nd ctenidium which, in response to a need for aerial respiration, has been developed in close association with the Ist ctenidium. Ranjah (1942), ша study of the embryonic development of Pila, confirmed that the lung arose as an infolding of the mantle epithelium, almost simultaneously with the ctenidium and os- phradium. However, Brooks & McGlone as well as Ranjah described only the early rudiments of the ampullariid lung, and did not follow up the full development of the organ as was done in the present study. Evidence derived from the present in- vestigation indicates that in Marisa: 1. The lung does not arise simultaneous- ly with the ctenidium and osphradium as claimed by Brooks & McGlone (1908) and Ranjah (1942) for other ampullariids. It starts to differentiate much later than the ctenidium, and develops principally after hatching. 2. The lung is not a modified 2nd ctenidium as suggested by Prashad (1925) for Pila, but a new structure, developing as a modification of the mantle epithelium. The ctenidium arises from a single ec- todermal rudiment which starts differen- tiating on the right wall of the visceral sac rudiment before the mantle or mantle cavity have developed, and no trace of a 2nd ctenidial rudiment is observable at that time, or later. Moreover, there is no reason to believe that the lung represents one or more modified gill lamellae derived from the Ist ctenidium, as suggested by Brooks & McGlone (1908). 3. The probability of an ancestral con- nection between the lung of the Am- pullariidae and that of pulmonates suspected by some authors is remote, be- cause the lung, as observed in Marisa, is derived in a way that is basically different from that most commonly met with in the pulmonates. The pulmonate lung usually arises, prior to and independent of the mantle cavity, as an ectodermal invagina- tion on the ventral or right posterior wall of the visceral sac rudiment in the early embryo. It becomes secondarily engulfed into the mantle cavity to become a non- separable part of it, the edges of the 2 cavities growing together so that they ul- timately open to the exterior by a common opening, the pneumostome, as has been described for Helix (Fol, 1880), Limax (Meisenheimer, 1898), Arion (Heyder, 1909), and Achatina (Ghose, 1963). The pallial fold and the 2 nuchal lobes, in Marisa, were shown, through this study, to be pallial structures developed as folds of the epithelium lining the mantle cavity. ACKNOWLEDGEMENTS The authors gratefully acknowledge the valuable contribution of Dr. K. Mansour, Emeritus Professor of Zoology, Faculty of Science, Ain Shams University, Cairo, in the supervision of the present work. Thanks are also due to Dr. B. Hubendick, Director of the Natural History Museum in Gothenberg, Sweden, for his continuous interest and support. REFERENCES BALSUBRAMANIAM, T.S., 1952, Develop- ment of Ariophanta bristrialis Beck. J. An- namalai Univ., 17: 94-100. BROOKS, W.K. & McGLONE, B., 1908, The origin of the lung in Ampullaria. Carnegie Inst. Publ., 102: 95-104. CARRICK, R., 1939, The life history ‚and development of Agriolimax agrestis L., the grey field slug. Trans. Roy. Soc. Edinb., 59: 963-597. CREEK, G.A., 1951, The reproductive system and embryology of the snail Pomatias elegans (Müller). Proc. Zool. Soc. Lond., 121: 599-640. CROFTS, R.R., 1938, The development of Haliotis tuberculata, with special reference 208 to organogenesis during torsion. Phil. Trans. Roy. Soc. Lond., B, 228: 219-268. DEMIAN, E.S., 1965, The respiratory system and the mechanism of respiration in Marisa cornuarietis (L.). Ark. Zool., Ser. 2, 17: 539- 560. DEMIAN, E.S. € YOUSIF, F., 1973a, Em- bryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). I. General outlines of development. Malacologia, 12: 123-150. DEMIAN, E.S. € YOUSIF, F., 1973b, Em- bryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). II. Development of the alimentary system. Malacologia, 12: 151-174. DEMIAN, E.S. € YOUSIF, F., 1973c, Em- bryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). III. Development of the alimentary system. Malacologia, 12: 175-194. DRUMMOND, LM., 1903, Notes on the development of Paludina vivipara with special reference to the urino-genital organs and theories of gastropod torsion. Quart. J. microsc. Sci., 46: 97-143. FERNANDO, W., 1931, The development of the kidney in Ampullaria (Pila) gigas. Proc! zool. Soc. Lond., 62: 745-750. FOL, H., 1880, Études sur le développement des mollusques. III. Sur le développement DEMIAN AND YOUSIF des gastéropodes pulmonés. Arch. Zool. exp. gén., 8: 103-232. GHOSE, K.C., 1963, Morphogenesis of the shell gland, lung, mantle and mantle cavity of the giant land snail Achatina fulica. Proc. malacol. Soc. Lond., 35: 119-126. HEYDER, P., 1909, Zur Entwicklung der Lun- genhóhole bei Arion. Nebst Bemerkungen über die Entwicklung der Urniere und Niere, des Pericards und Herzens. Zt. wiss. Zool., 93: 90-156. IHERING, H. von, 1887, Giebt es Or- thoneuren? Zt.wiss. Zool., 45: 499-531. LUTFY, В.С. & DEMIAN, E.S., 1965, The histology of the respiratory organs of Marisa cornuarietis (1). Ark. Zool., Ser. 2, 18: 51-71. NEISENHEIMER, J., 1898, Entwicklungs- geschichte von Limax maximus L. Zt. wiss. Zool., 63: 573-664. PRASHAD, B., 1925, Anatomy of the common Indian apple-snail, Pila globosa. Mem. In- dian Mus., 8: 91-152. RABL, C., 1879, Uber die Entwicklung der Tellerschnecke. Morph. Jb., 5: 562-660. RANJAH, A.R., 1942, The embryology of the Indian apple-snail, Pila globosa (Swainson) (Mollusca, Gastropoda). Rec. Indian Mus., 44: 217-322. RAVEN, D.P., 1966, Morphogenesis: The analysis of molluscan development. Pergamon Press, 2nd Ed., 365 р. SCOTT, M.LH., 1934, Sobre el desarrollo em- brionario de Ampullaria canaliculata. Rev. Mus. La Plata, 34: 373-385. ZUSAMMENFASSUNG EMBRYONALE ENTWICKLUNG UND ORGANOGENESE IN DER SCHNECKE MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). IV. ENTWICKLUNG DER SCHALENDRUSE, DES MANTELS UND DER ATMUNGSORGANE Е. S. Demian und Е. Yousif Die Schalendriisenanlage lässt sich schon früh am aboralen Ende des Embryos als eine mediane Ektodermalplatte unterscheiden. Diese vertieft sich becherartig, wandert nach links und sondert eine zarte, kutikulare, larvale Schale ab. Der mittlere Teil der Ver- tiefung wölbt sich dann empor, während seine Epithelzellen verflachen. Zusammen mit der Schale wächst dieses Epithel kreisförmig über den Proto-Eingeweidesack, und dann allein darüber hinaus, und bildet so schliesslich das äussere Epithel des Eingeweidesackes und des Mantels. Der wulstartige Epithelkranz am Mantelrand wird zur endgültigen Schalendrüse. Die Schale der Larve bleibt in einer Schicht der endgültigen Schale erhalten. Im Gegenstaz zu früheren Berichten über Ampullariiden, entsteht die Mantelhöhle erst spät, nach Drehung des Eingeweidesacks. Anfänglich eine Vertiefung oder Furche EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS 209 in der rechten dorsolateralen Wand des Proto-Eingeweidesackes, verwandelt sie sich allmählich, sährend sie vom Mantel überdeckt wird, in eine tiefe Höhle. Das einbezogene Ektoderm bildet ihre innere Auskleidung und das innere Mantelepithel. Die Kieme erwies sich als ontogenetisch älter als die Mantelhöhle. Die Kiemenanlage hebt sich schon früh, als verdickte Ektodermplatte, an der rechten Wand des Proto- Eingeweidesacks ab. Durch die Torsion gelangt die Urkieme sekundär in die Mantelhöhle. Sie verschiebt sich nach links und verlängert sich mit dem wachsenden Mantel nach vorn. Epitheliale Querfalten, die späteren Kiemenblättchen, werden angesetzt. Die Lunge ist ein unter den Prosobranchiern den Ampullariiden eigentümliches Organ, das sich erst kurz vor dem Ausschlüpfen als eine breite Einsenkung des Mantelhöhlendaches, zwischen Kieme und Osphradium, auszubilden beginnt. Der Epithelsaum um die Vertiefung wächst vom Rande her nach innen und bildet so den Boden der Lungenhöhle. Ein schmaler Spalt bleibt offen, der als Pneumostom erhalten bleibt. Nach dem Ausschlüpfen wächst die Lunge enorm und verlagert dadurch die Kieme nach rechts. Die Lunge der Ampullariiden ist demnach eine Neuentwicklung und keine modifizierte Kieme. Ein direkter stammesgeschichtlicher Zusammenhang mit der Pulmonatenlunge ist nicht ersichtlich. Die akzessorischen Atmungsorgane, d.h. die Pallialfalte (Epitaenia) und die 2 Nackenlappen (Siphos), werden als Falten des Mantelbodenepithels ebenfalls spät ausgebildet. Sie erlangen ihre endgültige Gestalt und Lage erst nach dem Ausschlüpfen. А.С. RESUME DEVELOPPEMENT EMBRYONNAIRE ET ORGANOGENESE CHEZ LE MOLLUSQUE MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). IV. DEVELOPPEMENT DE LA GLANDE COQUILLIERE, DU MANTEAU ET DES ORGANES RESPIRATOIRES E. S. Demian et F. Yousif Une glande coquilliere rudimentaire commence à se différencier au pôle aboral du jeune embryon sous forme d'un disque ectodermique épaissi en position médiane. I] s'in- vagine pour constituer une cavité en forme de coupe, s étend sur la gauche et sécréte une délicate coquille larvaire cuticulaire. Par la suite sa partie centrale s épaissit et son épithélium s aplanit. En même temps que la coquille larvaire, il s'étend circulairement par-dessus le rudiment de sac viscéral en le débordant et en s'étendant plus avant. A la fin, il forme les épithéliums externes de la masse viscérale et du manteau. Un bourrelet épithélial circulaire et périphérique demeure épaissi, c'est lui qui formera la glande coquilliére définitive. La coquille larvaire persiste dans une couche de la coquille adulte. Contrairement aux résultats des premiers travaux sur des Ampullariidés apparentés, la cavité palléale ne se développe que relativement tard, apres le choc de la torsion. Elle débute comme une dépression ou une gouttiére sur la paroi dorso-latérale droite de l'ébauche de sac viscéral, puis se transforme graduellement en une cavité profonde tandis que le manteau la déborde. L'ectoderme enfoncé dans cette cavité forme sa doublure in- térieure et l'épithélium interne du manteau. Il a été prouvé que la cténidie est ontologiquement plus ancienne que la cavité palléale. Son ébauche commence à se différencier primitivement comme un disque ec- todermique épaissi, sur la paroi droite de l’ébauche de sac viscéral. Secondairement, elle passe dans la cavité palléale pendant la torsion lorsqu elle se déplace sur le cóté gauche, s'étendant plus en avant quand le manteau s'accroît antérieurement. Des replis épithéliaux transversaux se développent sur elle pour former plus tard les lamelles cténidiales. Ге poumon qui, chez les Prosobranches, est une structure particuliére aux Ат- pullariidae, commence а se développer, peu avant l'éclosion, sous forme d'une large in- 210 DEMIAN AND YOUSIF vagination dans le toit de l'épithélium de la cavité palléale, entre la cténidie et losphradie. Le bourrelet épithélial bordant l'invagination s'accroît à partir de la périphérie pour former le plancher de la cavité pulmonaire, laissant ouverte une fissure étroite qui persistera en tant que pneumostome. Le poumon s accroit énormément aprés l'éclosion, déplaçant la cténidie sur le côté droit. Ces découvertes prouvent que le poumon est une nouvelle acquisition chez les Ampullariidae. Ce n'est pas une cténidie modifiée et il ne semble pas avoir la moindre parenté ancestrale avec le poumon des Pulmonés. Les organes palléaux accessoires de la respiration c’est-à-dire les ““epitaenia” et les 2 lobes nucaux (siphons), se développent aussi tardivement, sous forme de replis épithéliaux qui apparaissent sur le plancher de la cavité palléale. Ils atteignent leurs formes et leurs positions définitives aprés | éclosion. A.L. RESUMEN DESARROLLO EMBRIONARIO Y ORGANOGENESIS EN MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIIDAE). IV. DESARROLLO DE LA GLANDULA CONCHIFERA, MANTO Y ORGANOS RESPIRATORIOS E. S. Demian y F. Yousif Una gländula de la concha rudimentaria comienza por differenciarse en el polo aboral del temprano embriön, como una placa media, ectodermal, engrosada. Al envaginarse forma cavidad como una taza, se traslada a la izquierda y segrega una delicada conchilla larval cuticular. La parte central se comba hacia arriba y su epitelio se aplana. La glän- dula se extiende, junto con la concha larval, circularmente y sobrepasando el saco visceral rudimentario. Ultimamente se forman el epitelio externo de la masa visceral y el manto. Un anillo periferico epitelial permanece engrosado, y luego formarä la gländula definitiva. La conchilla larval persiste en una capa de la adulta. Contrariamente a lo que se habia indicado en otros informes sobre los ampularidos, la cavidad del manto se desarrolla relativamente tarde, después que la torsión ha comen- zado. Iniciándose como una hendidura en la pared derecha dorso-lateral del saco visceral rudimentario, gradualmente se transforma en una profunda cavidad al ser superada por el desarrollo del manto. El ectoderma engolfado dentro de la cavidad forma su forro in- terior y el epitelio del interior del manto. La ctenidia mostro ser de una edad ontogeneticamente mayor que la cavidad paleal. Su rudimento se diferencia temprano como una placa ectodermal engrosada en la pared derecha del saco visceral rudimentario. Secundariamente pasa dentro de la cavidad paleal durante la torsión, cuando se mueve al lado izquierdo, extendiéndose hacia adelante en medida que el manto crece anteriormente. El pliegue epitelial transversal desarrolla por encima, más tarde, las lamelas de la branquia. El pulmón—una estructura peculiar dentro de los Prosobranquios de los Am- pullariidae, comienza muy poco antes de la eclosión, como una invaginación ancha en el techo del epitelio de la cavidad paleal, entre las branquias y el osfradio. El anillo epitelial que rodea la invaginación crece de la periferia para formar el piso de la cavidad paleal o pulmón, dejando una estrecha ranura que persiste como el penumostoma. El pulmón crece enormemente después de la enclosión, desplazando la branquia hacia el lado derecho. Esto indica que el pulmón es una adquisición nueva entre los Ampullariidae, No es una branquia modificada y no parece tener ninguna relación ancetral directa con el pulmón de los pulmonados. Los órganos respiratorios accesorios, como el pliegue paleal (o “epitaenia”) y los dos lóbulos nucales (sifones), tambien se desarrollan tarde como pliegues del epitelio en el piso de la cavidad del manto. Estos alcanzan sus formas definitivas después de la eclosión. J.J.P. EMBRYOLOGY OF MARISA. IV. MANTLE AND RESPIRATORY ORGANS ДБСТРАКТ ЭМБРИОНАЛЬНОЕ РАЗВИТИЕ И ОРГАНОГЕНЕЗ У MARISA CORNUARIETIS (MESOGASTROPODA: AMPULLARIDAE) 1V. РАЗВИТИЕ РАКОВИННОЙ ЖЕЛЕЗЫ, МАНТИИ И ДЫХАТЕЛЬНЫХ ОРГАНОВ D. ДИМЬЯН И ©. ЮСИХФ Рудимент раковинной железы начинает дифференцироваться на ранней стадии развития эмбриона, на аборальной его стороне, как срединное утолщение эктодермальной пластинки. Она — вдавливается, образуя чашковидную впадину, сдвигается налево и выделяет нежную кутикулярную личиночную раковину. Ee центральная часть затем становится выпуклой, a эпителий уплощается. Вместе с личиночной раковиной она окружает рудимент висцерального мешка, разрастаясь над ним. Наконец, она образует эпителий висцеральной массы и мантии. Периферическая эпителиальная кайма остается утолщенной и впоследствии образует окончатальную раковинную железу. МЛичиночная раковина сохраняется и в раковине взрослого моллюска. В противоположность более ранним данным о развитии родственных форм Ampullariidae, было найдено, что мантийная полость у них развивается сравнительно поздно, после начала процесса торсии. Начинается это с образования вдавленности или желобка на правой дорзо- латеральной стенке рудимента висцерального мешка; постепенно он превращается в глубокую полость, когда она обрастает мантией. Эктодерма, вдающаяся в эту полость, образует её внутреннюю выстилку и внутренний эпителий мантии. В статье доказано, что ктенидии и онтогенетически старше, чем мантийная полость. Их рудимент начинает дифференцироваться рано, ввиде утолщения эктодермальной пластинки В правой стенке рудимента висцерального мешка. Вторично он входит в мантийную полость во время процесса торсии, когда он сдвигается на левую сторону, выдаваясъь вперед, во время роста мантии спереди. Ha нем развиваются поперечные эпителиальные складки, которые позже служат началом образования пластинок ктенидиев. Легкие, образование необычное для Prosobranchia Ampullariidae, начинают развиваться незадолго до вылупливания личинок, ввиде широкой инвагинации, выстилающего мантийную полость эпителия, между ктенидием и осфрадием. Эпителиальная кайма, опоясывающая эту инвагинацию, растет от центра к периферии, образуя выстилку легочной полости, оставляя открытой узкую щель, которая остается, образуя пневмотостом. Легкие растут очень сильно после выклевывания личинок, вытесняя ктенидии к правой стороне. Эта особенность указывает Ha TO, что легкие являются HOBHIM образованием У Ampullariidae. Это не модифицицированные ктенидии, и они, видимо, не имеют какого-либо прямого предкового родства с легкими Pulmonata. Добавочные дыхательные органы, т.е. мантийные складки или "эпитении" и 2 нукальных лопасти (сифоны) также развиваются позже, из складок эпителия, выстилающего мантийную полость. Они достигают свое го окончательного вида и расположения после выклева личинок. Z.A.F. 211 SS A БАРЫ ¡$ : a ATA A AA A TOITIURE En | Dr Ze ty | | er | р у А ie № | MTS р j A is EU de LU 06h», | УТКУ no р | arn % | 7 j vr a 0 в o р Ni “ pe % CE ie da — . Ed „> $ ' EN © ed . | iy | TIRE mts | ha De у | ms” fe 0 wate pone ive В y . | | yeso VEA | 7 у : a it ‘ Hi 0 A o u ; i à Pi i . Le o gr . ‘ Br HON m: it 11. Y o : у | от | "MIN a т 7 y «+ oa Es р р y 4 is m р +! р - р > 4 . 8 mu т Ge ГР » 9 À | Ñ A 5 i # | a hi n e 2 | "à à Ar = > | $ = . u IAN ce lo , ++ | ns Hilt eal = ‘op ‘7% Ú 34 ® ira nie Ae vt bs en poy e Mm y ean 7 5 Da 4 A one { уп AA © © ant ff Утв № | Pr . 7 re mt e ‘ м 0 A: te nada) Ves fu, ing a aye i tor. (20500 rr AS “ obs an" (De fo ¿Mis NN a dla N 49 no 40 N LOT LP EP F сами Dri heat | ete A mT LS u tot $ «Y Wet 5 wird к ino sa Il © ti A . ET ee E q 0 ДН PP pn 14d Lillo ea fies ыы we «ele | ua Aoi | Fe nie Gam, Вар И Be - e = o | | BZ = | Ya MALACOLOGIA, 1973, 12(2): 213-223 REGULATION OF APICAL CILIA DEVELOPMENT BY THE POLAR LOBE OF ILYANASSA (GASTROPODA: NASSARIIDAE)! James N. Cather Department of Zoology, The University of Michigan Ann Arbor, 48104, U.S.A. ABSTRACT Ilyanassa passes through a stage comparable to the trochophore within the egg cap- sule. The typical structures of the trochophore are reduced, but apical cilia appear on the apical cells la!!! - Id!!! and are therefore homologous with the apical tuft of the trochophore. Lateral tufts of cilia on la?! and |b?! are the only vestiges of the prototroch. Removal of the first or second polar lobe or the D quadrant macromere results in the development of cilia over most of the pretrochal region; thus cells which remain un- ciliated in the normal embryo develop cilia in operated embryos. It is proposed that the polar lobe normally inhibits ciliation in those cells whose prospective fate is to form un- ciliated cephalic plate cells. The regulation of apical cilia development in Ilyanassa is compared to that of other spiralians. Ciliation has been shown by others to occur in the absence of DNA-dependent RNA synthesis as well as in the absence of RNA-dependent protein synthesis. It appears that regulation might occur at a post-translational level in the apical cilia-polar lobe system and possibly at the time of the assembly of tubulin into cilia. INTRODUCTION The relationship of the polar lobe to the formation of the apical tuft was one of the first embryological phenomena т- vestigated experimentally. Wilson (1904a) found that the pretrochal region of the trochophore of the scaphopod mollusc Dentalium is covered with short vibratile cilia, while the apex bears a long non- vibratile ciliary tuft on a circumscribed apical thickening, the apical organ. Removal of the Ist polar lobe, the non- nucleate vegetal extrusion of the Ist cleavage, resulted in larvae lacking an apical tuft, probably the apical organ, and the post-trochal region. The vibratile cilia were unaffected by this and subsequent operations. After removal of the 2nd polar lobe, the apical tuft was formed normally but the post-trochal region was missing. Partial embryos which developed from isolated blastomeres, or combinations of blastomeres, only developed the apical tuft when the D quadrant, the recipient of the polar lobe material, was present. Wilson found that about half the Ist polar lobe was required for apical tuft formation while Geilenkirchen, Verdonk & Timmer- mans (1970) found that the apical tuft would form after removal of 60% but not 80% of the vegetal side of the Ist polar lobe. Verdonk, Geilenkirchen & Timmer- mans (1971) found that removal of 70% of the volume of the polar lobe from the vegetal pole of fertilized or unfertilized eggs had no detrimental effect on apical tuft formation. They then found the factor responsible for tuft formation to be localiz- ed in the animal half of the Ist polar lobe, in the vegetal half of the CD blastomere at the 2-cell stage, and in the animal portion of the D blastomere at the 4-cell stage. Verdonk (1968a) showed that centrifuga- Supported in part by Institutional Research Grant No. IN-40M to the University of Michigan from the American Cancer Society (213) 214 J. N. CATHER tion did not affect the development of the apical tuft in intact or operated eggs, thus indicating a cortical rather than a general cytoplasmic influence. Timmermans, Geilenkirchen & Verdonk (1970) originally proposed that DNA-containing granules in the vegetal cortex served as morphogenetic factors for the apical tuft; but the later study of Verdonk, Geilen- kirchen € Timmermans (1971) showed that removal of these granules has no effect on the apical tuft, although they might still serve as post-trochal morphogenetic determinants. The mussel, Mytilus, is much like Dentalium in that lobeless embryos or those lacking the D quadrant lack an apical tuft (Rattenbury & Berg, 1954). Removal of the 2nd polar lobe does not affect tuft formation. As in Ilyanassa there is a general appearance of ectodermization in lobeless embroyos but this is due to the reduction of endodermal volume rather than an actual enhance- ment of ectodermal development. Other species have not been as thoroughly investigated. In Patella, Wilson (1904b) found that the apical tuft would form in any Y embryo and is not dependent on the D quadrant. The polar lobe is not present in this species. In the annelid, Sabellaria, Novikoff (1938 a,b) found that the apical tuft formed only in the presence of the C macromere when the Ist polar lobe was present. Removal of the 2nd polar lobe had no effect on the tuft. Thus it appears the lobe has made its con- tribution to CD at the 2-cell stage just as in Dentalium, but the final site is in the C blastomere rather than the D blastomere. Pretrochal cilia in Sabellaria are depen- dent on the presence of A or B. In the fresh-water prosobranch, Bithynia, the apical cilia appear to be normal in AB or CD halves or C or D quarters but are ab- sent in total exogastrulae (Hess, 1971). In another annelid Nereis (Costello, 1945) the apical tuft is derived from Та! - 1d! as it is in Patella, while in Dentalium only Id! contributes to the apical tuft (Wilson, 1904b). The apical plate in Lym- naea (Verdonk, 1965) and Biomphalaria (Camey & Verdonk, 1970) has a similar cellular origin; in these cases the cell lineage has been worked out in detail. Cather (1971) reported that, in Ilyanassa, progeny from isolated la! - lc! had a single cluster of cilia while those of 1d! had 2 ciliary clusters suggesting an origin of the apical cilia similar to that of the tuft of Dentalium. Conklin (1897) found that a distinct apical sense organ was formed in Crepidula from the 4 apical cells la!!! - Id!!! and that in addition a few of their progeny proliferated into the head vesicle. Posterior to the apical organ is the head vesicle which is covered by the large ciliated cells of the posterior cell plate in the veliger. These cells are the progeny of the posterior turret cells Ic? and Id? and of the basal сей (1d!2!) and the middle cell (1d122) of the posterior arm of the molluscan cross. The term apical plate was used by Conklin to refer to the 7 large ciliated cells derived from the anterior arm of the cross which extend from the apical organ to the velum. Their progeny make up 13 cells in the young veliger. Verdonk (1965) in- cludes the 4 apical cells in the apical plate in Lymnaea thus including all of the large cells between the small-celled cephalic plates, which are the sites of origin of the tentacles, eyes and cerebral ganglia. Even though Ilyanassa is much more like Crepidula than like Lymnaea, 1 will use apical plate to include all the large cells between the cephalic plates including the apical organ, and restrict the use of apical organ to the apical cells at whatever stage they are considered. The apical plate is a structure of the veliger in Ilyanassa while the apical organ is a vestige of the trochophore which is subsequently morphologically if not functionally incor- porated into the apical plate of the veliger. The following observations were made and experiments were done to determine the character and mode of regulation of the apical cilia in Ilyanassa. METHODS The experiments were performed on eggs and embryos of the prosobranch gas- APICAL CILIA REGULATION IN ILYANASSA 215 tropod, Nassarius obsoletus Say, common- ly referred to as Ilyanassa by em- bryologists. Animals were obtained from the Marine Biological Laboratory, Woods Hole, Mass., U.S.A., and were raised in Instant Ocean (Aquarium Systems Inc.) at The University of Michigan. All embryos were maintained at 20 + 1°C. At this temperature full differentia- tion of the veliger requires about 3 weeks. The details of handling eggs and embryos and of performing operations are given by Clement (1952, 1962, 1971) and Cather (1967). Analysis of ciliary patterns was done with a Zeiss Nomarski Differential Interference Contrast Microscope on liv- ing embryos. These were then fixed in 10% formalin-sea water on the slide, photographed, and made into permanent preparations by mounting the unstained embryos in diaphane (Clement & Cather, 1957). Several staining procedures were tried to enhance visibility of both the cell boundaries and the ciliary patterns, but none of the stained specimens was com- parable in quality to the unstained em- bryos in diaphane. The latter though were less satisfactory for observation of ciliary patterns than living embryos. Fixation and staining often resulted in the loss of cilia from positions where they had been observed on living embryos. RESULTS In Ilyanassa and other neogastropods the stage comparable to the trochophore is passed within the egg capsule, and typical ciliation is markedly reduced. There is no apical tuft comparable to that of forms with free-living trochophores such as Den- talium, Patella, Sabellaria, and Mytilus. The apical tuft of Nereis is distinct but the cilia are short and more motile than in those species previously noted. Short motile cilia do appear on the 4 apical cells of Ilyanassa (la!!! - 1b!!!) about 36 hours after the Ist cleavage (Fig. 1). At this time the cells still occupy an apical position over the furrow between the macromeres. The cells are relatively large and temporarily flattened when compared to the surroun- ding micromeres at this stage. The apical cells are delimited from the surrounding cells by a slight groove visible in section. Since the 4 cells that become ciliated shortly after gastrulation are the same cells which form the apical tuft in other annelids and molluscs, these apical cilia of Ilyanassa are homologous with the apical tuft of the trochophore. The apical cells which are formed within 8 hours of the for- mation of the mesentoblast cell do not divide again, at least through the early veliger stage shown in Fig. 11. The apical cells remain distinct through the developmental period due to their prox- imity to the posterior turret cells 1c? and ld? which remain very large until the head vesicle of the veliger begins to form. The same ciliary pattern persists as the stomodeum is formed and the mesoblast bands continue their elaboration (Fig. 2). RESULTS Normal Post-Gastrula Ciliation Although only the 4 apical cells are in- itially ciliated 3 additional cells become ciliated by the 5th or 6th day of develop- ment to give the ciliated area a Y or cross shape, with the arms slightly off the sagit- tal and transverse planes of the em- bryo. Judging from Conklin's (1897) il- lustrations of the cell pattern around the apical cells in Crepidula, which is very similar to Ilyanassa, these later ciliated cells appear to be derivatives of the anterior arm of the cross, which form the apical plate cells in Crepidula. It has been possible to follow the formation and fate of 1b1112 in Ilyanassa, due to its size and posi- tion, until the time of ciliation. In the veliger of Ilyanassa, as in Crepidula, all of the cells of the apical plate and the posterior cell plate are ciliated. From the stage comparable to the trochophore until the early veliger there is a shift in the posi- tion of the apical cells from the original animal pole to an anterior position. By the 6th day the anterior wall of the stomodeum is ciliated (Fig. 3) and the lateral trochoblast derivatives la?! and 1b?! which have remained very large become ciliated (Fig. 4). The early differentiation 216 J. N. CATHER FIGS. 1-8. Drawings of normal (Figs. 1-4) and experimental (Figs. 5-8) embryos of Ilyanassa grown at 20°C. The animal pole is uppermost in each drawing. FIG. 1. 36-hr control embryo, lateral view. FIG. 2. 48-hr control embryo, lateral view. FIG. 3. 6-day control embryo, lateral view. FIG. 4. 6-day control embryo, front view. FIGS. 5-7 are from operated embryos at a stage of development comparable to Figs. 3 and 4. FIG. 5. 6-day embryo after Ist polar lobe removal. FIG. 6. 7-day embryo after 2nd polar lobe removal. FIG. 7. 6-day embryo after D macromere removal. FIG. 8. 9-day embryo after Ist polar lobe removal showing complete development of ciliation. x 125. FIGS. 9-14. Photomicrographs of normal and experimental embryos of Ilyanassa grown at 20°C. (All x 220.) FIG. 9. 4-day control embryo, lateral view. FIG. 10. 9-day embryo after Ist polar lobe removal. FIG. 11. 9-day control embryo, dorsolateral view. FIG. 12. 11-day 1/4 embryo. FIG. 13. 4-day control, front view. FIG. 14. 9-day embryo after removal of the 1st polar lobe. The animal pole is at upper left. Abbreviations Used: a = apical cilia of apical cells; ac = apical cilia of all first quartet micromeres; f = foot; h = head cilia of head vesicle and apical plate; p = prototroch vestige of la2!: 5 = stomodeum: sc = stomodeal cilia; sh = shell; у = velar lobe; ус = velar cilia. APICAL CILIA REGULATION IN ILYANASSA 218 |. Nt CATHER of these cells and the fact that they remain the only lateral ciliated cells for almost 1/3 of the developmental period, suggest that they represent vestiges of the prototroch. The other velar rudiments appear much later. The development of the velum and of the ciliated bands anterior and ventral to the shell gland and on the foot and mantle occur much later; they have not been well worked out, but as structures of the veliger they are beyond the stages to be con- sidered here. Ciliation in Lobeless Embryos The ciliary pattern was studied in 44 liv- ing embryos from which the first polar lobe had been removed. Lobeless embryos complete gastrulation slightly more rapid- ly than eel embryos, but no apical cilia develop until the embryos are ap- proximately 48 hours old, a lag of about 12 hours behind the controls. Ciliation usual- ly extends ventrally somewhat farther than the lateral trochoblast position in tontrol embryos. This is apparently due to the fact that the first quartet derivatives cover relatively more of the lobeless embryo than of the control. Most or all of the derivatives of the first quartet appeared to be ciliated (Figs. 5, 10, 14) in 39 embryos; 4 embryos had unciliated patches in the region of the first quartet derivatives and 1 embryo had a single broad band of cilia across its apex. There was little variation in the basic pattern of ciliation through the stage comparable to the trochophore, although it is known that some variation is present in later stages (Clement, 1952; Atkinson, 1971). The pattern of cellular distribution was also studied an ad- ditional 24 fixed lobeless embryos and it was found to be quite uniform through the stage comparable to the trochophore. Although a detailed cell lineage has not been carried out on lobeless embryos, some observations have been made which are important in the interpretation of the pattern of ciliation lobeless embryos. Clement (1952) has shown that the pattern of cleavage is modified lobeless ет- bryos, but Davidson et al. (1965) and Cather and Mirkes (Cather, 1971) have shown that the total cell number is not ap- preciably modified. The total number of Ist quartet derivatives, including those of the turret cells, increases from 38 to 52 in the trochophore stage in both normal and lobeless embryos. The turret cells remain large and distinctive in lobeless embryos just as in control embryos and clearly mark the equatorial boundaries of ciliation in the trochophore stage. The apical cells in delobed embryos are similar in size to those in normal embryos and are equally distinctive. Velar cilia develop at the same equatorial position and ventral to the turret cell derivatives but later than the apical cilia (Fig. 8). The early formation of the stomodeal in- vagination acentric to the vegetal pole in lobeless embryos may indicate an aspect of polarity which is not lobe dependent (see Clement, 1952; Atkinson, 1971). An analysis of 12 living embryos and an additional 16 fixed embryos with the 2nd polar lobe removed indicated that there are no appreciable differences in the ciliary patterns between embryos with the Ist or 2nd polar lobe removed (Fig. 6). In cases where portions of the pretrochal areas remain unciliated, following either operation, the ciliated area could be observed to shift toward 1 side (Fig. 6). Such a shift cannot be detected when all of the pretrochal region is ciliated, even if it takes place. This may represent the normal shifting of the apical plate to an anterior position, but there is no way to determine the anterior-posterior axis in lobeless em- bryos due to the absence of ‘landmarks.’ Deletion of the D Quadrant Macromere The CD macromere was deleted in 20 cases to form AB half embryos; D was deleted in 7 cases to form ABC embryos; ABD, ACD and BCD were deleted in 2 cases each to form C, B and A quarter em- bryos respectively (Fig. 12). Following these operations the pattern of ciliation was essentially the same as in lobeless em- bryos, so that a cap of ciliated cells more or less covered the upper % of the embryo. The velar cilia develop later from the ven- APICAL CILIA REGULATION IN ILYANASSA 219 trolateral area and may be interspersed with additional short cilia from cells which by their position are probably 2nd quartet derivatives. DISCUSSION In lobeless embryos of Ilyanassa the ciliary pattern of the stage comparable to the trochophore is considerably different from the pattern in spiralians previously studied, when comparing the tuft of the trochophore with the development of apical cilia. Removal of the Ist polar lobe does not result in the absence of apical cilia in Ilyanassa, but rather in the absence of morphogenetic regulation of apical cilia. The same results follow the removal of the 2nd polar lobe. Certain cells of the Ist quartet, normally unciliated in early development, now develop cilia. Some of the cells under consideration would be ex- pected to develop cilia much later, but others are the cells which normally give rise to the eyes and cerebral ganglia, which remain unciliated normally. Atkinson (1971) has pointed out the dif- ficulty of making comparisons between lobeless forms of species such as Ilyanassa, lacking a free-living trochophore, and those species with a free-living trochophore, such as Dentalium, Mytilus and Sabellaria. Both Clement (1952, 1962) and Atkinson (1971), who have done the most complete analyses of lobeless em- bryos, have focused on the completely differentiated form comparable to the veliger. Because of the excellence of these works it is possible to direct attention to the intermediate stages for a more com- plete analysis of the steps leading to differentiative changes. Atkinson found that the normal veliger of Ilyanassa was essentially the same as Crepidula as far as the apical plate and surrounding area is concerned. He further found that the pre-velar epidermis of lobeless larvae was often non-ciliated cuboidal epithelium, though such larvae often had an area of ciliated ectoderm, usually opposite the posterior protrusion. In this study, each of the 130 lobeless or D-less embryos examined in detail at a stage comparable to the trochophore had an apical area with motile cilia covering most of the pretrochal ectoderm. This observation supports the wisdom of Atkin- son s statement concerning the difficulty of attempting comparisons between different larvae following the same opera- tion, and also illustrates the importance of sequential developmental analysis. Investigations thus far have shown that the polar lobe may influence development sequentially through: 1) modification of cleavage pattern (Clement, 1952); 2) material contribution to structures in the D quadrant cell lineage (Clement, 1952, 1956, 1962); 3) induction of specific organs (Clement, 1952, 1956, 1962, 1967; and Cather, 1967); and 4) inhibition (Cather, 1967; Atkinson, 1971). Results of the pre- sent study appear to fall in the last category. Polar lobe derivatives somehow influence certain cells of the first quartet so that the potential to form cilia is not realized. Removal of the lobe, or of the early blastomeres into which it is incor- porated, evidently releases this inhibition so that not only the normally ciliated apical cells form cilia, but all the Ist quartet derivatives become ciliated. This is consistent with the view of Verdonk (1968b) on radialized embryos of Lym- naed. Alternative hypotheses—the stimulation of apical cell division to cover the apical ciliated region in lobeless embryos, or a precocious appearance of velar cilia—do not appear to be tenable. In the Ist case, the apical cells of lobeless embryos are ap- proximately the same size as in normal em- bryos, which indicates that there has not been a significant increase in progeny from these cells. Furthermore, the total number of cells derived from the Ist quartet is similar in delobed and control embryos. In the 2nd case, velar cilia develop ventrally and equatorially to, and include the turret cell derivatives. The velar cilia appear subsequently to the development of the rest of the apical ciliated region, which persists without be- ing involved in velar lobe formation in lobeless embryos. 220 J. ¿Ni CATHER The formation of cilia in lobeless em- bryos by cells which are unciliated in nor- mal embryos is particularly interesting in light of recent work indicating that cilia can form in the absence of DNA- dependent RNA synthesis in Ilyanassa (Collier, 1966; Feigenbaum & Goldberg, 1965; Mirkes, 1970) and in the sea urchin (Auclair & Siegel, 1966). It has also been shown (Iverson, 1971) that the sea urchin can regenerate cilia without RNA- dependent protein synthesis by utilizing an intracellular pool of tubulin, formed originally on maternally derived mRNA. Repeated deciliation and regeneration does require new synthesis. Amemiya (1971) further found that while isolated cells of the sea urchin cannot regenerate cilia, those in reaggregates under the same conditions can. He attributes this to inhibi- tion of the biosynthesis of precursor proteins or to an inhibition of the associa- tion of subunits in isolated cells. The in- vestigations cited above present evidence in favor of the later alternative, but in either case, the role of the cell surface as a regulatory agent is indicated. In Ilyanassa, an interesting and testable hypothesis, although still highly speculative, is that subunits for ciliary syn- thesis are present in ectodermal cells of at least the Ist quartet. However the associa- tion of such subunits is inhibited in all non-apical cells by the polar lobe. The cells of lobeless Ilyanassa embryos which are added to the ciliated apical group are cephalic plate cells which go through ap- parently the normal number of divisions prior to their abnormal ciliation. It is not known how tubulin utilization is regulated for cell division or ciliation, but it is interesting to consider how the ancestral apical tuft might be reduced in length to be the apical cilia in those forms with a reduced trochophore. Shell inhibition in the A, B and C quadrants (Cather, 1967) is similar to the ciliary inhibition in that only certain cells respond to the inhibition while others proceed to form shell and carry out their prospective fates. Multiple lobes of the velum and multiple stomodea in lobeless embryos of Ilyanassa (Atkinson, 1971) suggest another case of inhibitory in- fluence by the polar lobe in normal development. The regulatory mechanisms are un- known in all these cases but the regulation of ciliation may be most amenable to fruit- ful further investigation because of the re- cent advances in our knowledge of the biochemistry of cilia formation. 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H., 1970, Local accumulation of Feulgen- postive granules in the egg cortex of Dentalium dentale L. J. Embryol, exp. Morphol., 23: 245-252. VERDONK, N. H., 1965, Morphogenesis of the head region in Limnaea stagnalis L. Thesis, Rijkuniversiteit Utrecht, p 1-133. VERDONK, №. H., 1968a, The effect of remov- ing the polar lobe in centrifuged eggs of Dentalium. ]. Embryol. exp. Morphol., 19: 33-42. VERDONK, N. H., 1968b, The determination of bilateral symmetry in the head region of Limnaea stagnalis. Acta Embryol. Morphol. exp, LOS 201-227, VERDONK, N. H., GEILENKIRCHEN, W. L. M. & TIMMERMANS, L. P. M., 1971, The localization of morphogenetic factors in uncleaved eggs of Dentalium. J. Embryol. exp. Morphol., 25: 57-63. WILSON, E. B., 1904a, Experimental studies on germinal localization. I. The germ regions in the egg of Dentalium. J. exp. Zool., 1: 1- PR WILSON, E. B., 1904b, Experimental studies on germinal localization. II. Experiments on the cleavage-mosaic in Patella and Den- talium. J. exp. Zool., 1: 197-268. ZUSAMMENFASSUNG REGULIERUNG DER APIKALZILIENBILDUNG DURCH DEN POLLAPPEN BEI ILYANASSA (GASTROPODA: NASSARIIDAE) J.N. Cather Ilyanassa durchläuft in der Eikapsel ein Entwicklungsstadium, das der Trochophora vergleichbar ist. Die typischen Trochophora-Strukturen sind zuriickgebildet, doch bilden sich Apikalzilien auf den Apikalzellen la!!! bis 1411; sie sind daher mit dem apikalen Biischel der Trochophora homolog. Laterale Wimpernbiischel auf Та?! und 1b?! sind die einzigen Rudimente des Prototrochs. Entfernung des ersten oder zweiten Pollappens oder der Makromere des D- Quadranten führt zur Zilienentwicklung auf dem größten Teil der Prätrochalregion. So 222 J. N. CATHER entwickeln Zellen, die im normalen Embryo unbewimpert bleiben, bei operierten Em- bryonen Zilien. Der Pollappen inhibiert, wie zur Deutung vorgeschlagen wird, die Zilien- bildung in denjenigen Zellen, deren prospektive Bestimmung es ist, unbewimperte Scheitelplatten-Zellen zu bilden. Die Regulierung der Apikalzilienentwicklung bei Ilyanassa wird mit der anderer Spiralier verglichen. Andere Autoren konnten zeigen, daß Zilienbildung beim Fehlen DNS-abhängiger RNS-Synthese vorkommt wie auch beim Fehlen RNS-abhängiger Protein-Synthese. Es scheint, daß die Regulierung auf der Posttranslationsstufe im Apikalzilien-Pollappen- System stattfiden kann, möglicherweise zur Zeit der Ansammlung von Tubulin in den Zilien. C.M.-B. у RESUME REGULATION DU DEVELOPPEMENT DES CILS APICAUX PAR LE LOBE POLAIRE CHEZ ILYANASSA (GASTROPODA: NASSARIIDAE) J. N. Cather Ilyanassa atteint un stade comparable а la trochophore а l'intérieur de la capsule de l'oeuf. Les structures typiques de la trochophore sont réduites, mais cependant des cils apicaux apparaissent sur les cellules apicales la!!! - 1d!!! et sont homologues de la touffe apicale de la trochophore. Des touffes latérales de cils sur la?! et 1b?! sont les seuls vestiges de la prototroque. Si Гоп enléve le premier ou second lobe polaire ou le macromere D du stade 4, il en résulte le développement de cils sur la plus grande partie de la région prétrochale; ainsi les cellules qui demeurent non-ciliées sur l'embryon normal développent des cils sur les embryons opérés. On suppose que le lobe polaire inhibe normalement la ciliation dans ces cellules dont la destinée future est de former des cellules céphaliques de revêtement, non-ciliées. La régulation du développement des cils apicaux chez Ilyanassa a été comparée à celle des autres spiralias. D'autres auteurs ont montré que la ciliation se produit en l'absence de synthèse de RNA dépendante du DNA, aussi bien que de l'absence de synthèse de proteines dépen- dantes du RNA. Il semble que la régulation pourrait se manifester au niveau post- translationnel dans le système cils apicaux—lobe polaire et peut-être au moment de l’ajustage des tubules dans les cils. А.Г. RESUMEN REGULACION DEL DESARROLLO DE CILIAS APICALES POR EL LOBULO POLAR DE ILYANASSA (GASTROPODA: NASSARIIDAE) J. N. Cather Dentro de la cápsula ovigera, Пуапазза pasa por un estado comparable al de trocosfera. Las estructuras apicales de la trocosfera estan reducidas, pero las cilias estan presentes sobre las células apicales la!!! - Id!!! siendo asi homólogas a los penachos apicales trocosfóricos. Los únicos vestigios de la prototrocosfera son los penachos laterales de cilias en la?! y 1b21 Extirpación del primer o segundo lóbulo polar, o del cuadrante D macromero, resulta en el desarrollo de cilias; por esto, células que en un desarrollo normal permanecerían no ciliadas, tienen cilias en los embriones operados. Se sugiere que el lóbulo polar nor- APICAL CILIA REGULATION IN ILYANASSA 223 malmente inhibe la ciliación en aquellas células cuyo destino es formar placas celulares cefálicas no ciliadas. La regulación en el desarrollo de las cilias espirales en Ilyanassa es comparada con las de otros con desdoblamiento espiral. J.J.P. АБСТРАКТ РЕГУЛЯЦИЯ РАЗВИТИЯ АПИКАЛЬНЫХ РЕСНИЧЕК ПОЛЯРНОЙ ЛОПАСТЬК ILYANASSA ДЖ. КЭТЕР Пуапазза проходит через стадию развития, сравнимую с трохофорой, внутри яйцевой капсулы. Типичное строение трохофоры редуцировано, но апикальные реснички появляются на апикальных клетках la Wl - аш | и поэтому гомологичны апикальному пучку трохофоры. Латеральные пучки ресничек на la! и 162 являются единственными следами прототроха. Удаление первой или второй полярной лопасти или Д-квадранта макромеры имеет своим результатом развитие ресничек на большей части претрохальной области; таким образом у клеток нормального эмбриона, не имеющего ресничек, таковые развиваются у оперированного эмбриона. Предполагается, что полярная лопасть нормально не имеет ресничек на тех клетках, дальнейшее назначение которых состоит в образовании безресничных клеток цефалической пластинки. Регуляция развития апикальных ресничек у Пуапазза в статье сравнивается с другими спиральными формами. Ранее было показано, что образование ресничек встречается при отсутствии DNA - зависимого компонента при синтезе RNA, как и в случае отсутствия ВМА - зависимого компонента протеинового синтеза. По-видимому, эти регуляции может встречаться на пост-трансляционном уровне в системе "апикальные реснички - полярная лопасть" и, возможно, во время накопления тубулина в ресничках. Z.A.F. р № eae ee D = см Сару AR TA PP Иа, | e | : ALAN 1:06 (te? = mil ni Ai Br “live Aina o de tory ld и» 8:1 +- qu ret dr a tel ù $ a mb Re j un i 4 НА TETE scan Y N, ® | р | a в pl + | y | IN DE | $ | ö u = u a = Ут у = o 00D s 2 A | CD) р Че! 2% e U ge e sl - р fl | ES) О В e 5 у р AY р | | q A) ч i и 4 ) 0 МАР ote ait LL él le mx ae ten u as | at, = 0. 2.22820, Y » We eri om ete | 7 O wu br a | + u ax (ut a = ara DR o a A | AUS u ne = +... | | | = IN ee Я ab u MALACOLOGIA, 1973, 12(2): 225-245 MORPHOGENESE, DE „ГА, CHARNIERE. CHEZ, 5 1ESPECES DE VENERIDAE! Marcel L. M. Le Pennec Laboratoire de Zoologie, Université de Bretagne Occidentale 29 N. Brest, France RESUME L'élevage au laboratoire de 5 représentants des Veneridae des côtes de Bretagne a fourni des renseignements sur la morphogenése des charnieres. Le stade de la métamorphose a été dépassé pour toutes les espéces. L'observation journalière des со- quilles larvaires a permis de suivre en détail l’évolution de la charnière: d’abord les crénelures de la prodissoconque, puis la formation des lames primitives chez la dis- soconque, enfin la régression des crénelures. Parallélement nous avons noté la formation et la position du ligament. Les résultats sont traduits sous forme d'une clé de détermina- tion pour les 5 espéces de Veneridae. Le genre Venerupis est caractérisé, des la fin de la premiere semaine, par des crénelures bien formées et dénombrables alors qu elles restent indistinctes chez le genre Venus. A l'intérieur du genre Venerupis la variation du nombre des crénelures permet de différencier les espéces : de 8 4 10 pour Venerupis pullastra, généralement 12 pour Venerupis aurea. A la fin de la deuxiéme semaine des formations latérales apparaissent chez Venus fasciata. Les stries trés marquées de la coquille de Venus striatula aident а reconnaítre cette espéce. Aucun caractére morphologique par- ticulier n'a pu être retenu pour Venus verrucosa. Il ressort de cette étude que l'examen de la charniére des coquilles larvaires est un des critéres les plus sûrs pour établir l'identité des larves de bivalves récoltées dans le plancton. Cependant la détermination des larves, au moyen de cette méthode, reste impossible avant la constitution des crénelures qui а lieu ä la fin de la premiere semaine. INTRODUCTION L'élevage au laboratoire permet d’obtenir les différents stades larvaires de la plupart des mollusques et le probléme de la récolte et de la détermination est ain- si résolu. Il est désormais possible de suivre la morphogenese de la coquille larvaire et de déterminer les critéres qui aideront а résoudre le probléme de la détermination spécifique des larves de bivalves du planc- ton, récolté en mer. Au cours d'une étude précédente (Le Pennec, 1970; Le Pennec € Lucas, 1970) nous avons retenu 5 critéres qui sont: les dimensions de la larve, la forme générale de la coquille, la proéminence de ГитБо, les détails de la charniére et la position du ligament. L'examen de la charniére et la position du ligament nécessitent l'ouverture de la coquille larvaire, mais les résultats obtenus montrent que ce sont les 2 meilleurs critéres pour la reconnaissance spécifique des larves. Ils font l'objet de ce present travail. Depuis Bernard, en 1895, peu d auteurs ont étudié les charniéres de mollusques. Werner (1939), Sullivan (1948), et Rees (1950) ont suggéré que Гехатеп des char- niéres serait un bon critere pour l'iden- tification des larves dans le plancton. Leurs observations, bien que super- ficielles et effectuées sur des échantillons récoltés en mer, leur ont permis d'établir une classification simplifiée des larves de bivalves. ! Etude réalisée dans le cadre des contrats 70/170 et 71/292 passés entre le Professeur Lucas et le C.N.E.X.O. (225) 226 M. L. M. LE PENNEC L'obtention des différents stades lar- vaires en laboratoire permet de suivre de maniére certaine l’évolution d'une char- nière de la prodissoconque jusqu à l'adulte. Partant de ces données nouvelles, Chanley (1965, 1969) decrit la morphologie de nombreuses larves de bi- valves et différencie les especes prin- cipalement d’apres la structure de leur charniére (crénelures et dents juvéniles). Malheureusement on ne trouve dans ses publications aucun schéma (ou photo) montrant une évolution complète de la charnière larvaire et post-larvaire. La premiére classification des bivalves basée sur la charnière, et la systématisa- tion de la plupart des types (Cryptodontes, Taxodontes, Hétérodontes, etc.) sont dues au paléontologiste Neumayr (1891). De plus, la division des bivalves en famille et en genre est fondée en grande partie sur le caractére des dents et du ligament. Bernard (1895) a proposé de traduire la disposition respective des dents et des fossettes par des formules cardinales. Les dents se forment aux dépens de lames primitives. Des chiffres romains indiquent le rang de la lame primitive à laquelle elles appartiennent. Si cette lame se divise, on utilise la notation en chiffre arabe 2a, 2b: 3a, 3b, etc. Les chiffres sont impairs pour la valve droite, pairs pour la valve gauche. Chez les Hétérodontes, auxquels appar- tiennent les Veneridae, les dents sont dis- semblables avec généralement 3 cardinales semblant rayonner des umbos et divergeant plus ou moins vers le bord in- férieur du plateau cardinal. La prodissoconque a une charniére rec- tiligne dépourvue de dent. Les 2 valves sont maintenues jointes le long du cété rec- tiligne grace au périostracum qui se con- tinue d'une valve sur l’autre. Au bout de quelques heures le plateau cardinal s épaissit et la prodissoconque présente des dents qui apparaissent com- me des crénelures encore peu marquées. Cette charniére embryonnaire est appelée provinculum (Bernard, 1895). Les crenelures grandissent à mesure que s épaissit le plateau qui les porte. Elles sont paralléles entre elles et perpendiculaires a la ligne dorsale. Puis les crénelures pren- nent une direction moins rigoureusement parallele, ce qui est en relation avec le fait que le bord cardinal extérieur prend une direction plus arquée sous la poussée de l'umbo. D'une maniére générale, c'est à peu pres pendant le stade de transition entre la prodissoconque et la dissoconque que les premiéres dents apparaissent chez les Hétérodontes. Aprés la métamorphose les crénelures larvaires disparaissent а mesure que se développent les dents définitives. Dans la présente étude la morphogenése de la charniére a été étudiée sur 5 espéces de Veneridae vivant sur les cótes de Bretagne; ce sont: Venus striatula, Venus verrucosa, Venus fasciata, Venerupis pullastra et Venerupis aurea. METHODES Au cours de l’année 1969, plusieurs es- peces de bivalves ont été élevées au laboratoire de Zoologie de la Faculté des Sciences de Brest (France). Les tech- niques utilisées dérivent de celles que Loosanoff € Davis (1963) ont mis au point des 1946 au laboratoire de Milford (U.S.A.). La ponte des géniteurs est provoquée par stimulation thermique: variations de la température de l’eau et quelque fois émersion. Les larves, obtenues aprés fécondation artificielle, sont élevées dans des cuves en plastique contenant 20 a 30 litres d eau de mer. La stérilisation de Геаи se fait au moyen d'un appareil Millipore dont les filtres retiennent а leur surface toutes les particules excédant 0,22 u. L'eau des cuves est renouvelée journellement jusqu'à ce que les larves atteignent une longueur de 300 и environ. La nourriture des larves est composée de Phytoflagellées: Monochrysis lutheri et Isochrysis galbana, et de Diatomées dont Chaetoceros calcitrans. L'étude des charnières nécessite une manipulation délicate qui consiste à ouvrir les jeunes coquilles. Celles-ci sont mises dans l'eau de Javel concentrée (hypo- chlorite de sodium) pendant 2 à 5 minutes, CHARNIERES CHEZ VENERIDAE LARVAIRES 227 ouvertes sous la binoculaire à l'aide de deux fines aiguilles puis rincées à l'eau dis- tillée et mises dans l'alcool glycériné pour observation au microscope. L'alcool glycériné (50% alcool-50% glycérine) permet de garder les valves orientées perpendiculairement au champ de vision du microscope et facilite l'étude des char- niéres. Les valves sont ensuite mesurées au micrometre oculaire, photographiées et les dessins des charniéres sont réalisés d’apres les agrandissements photographiques. RESULTATS 1. Charniere de Venus striatula La prodissoconque de 3 jours, 103u x 87u, a une charniére droite, non fonc- tionnelle, mesurant 64a. Le plateau car- dinal prend naissance le long du bord dor- sal de la coquille mais il est interrompu a l'endroit où se formera le ligament. La prodissoconque de 7 jours (Fig. 1) a un plateau cardinal épaissi. Les crénelures larvaires se forment et sont visibles sur une coquille de 142u x 118u. Le ligament ap- paraît dans le prolongement du plateau cardinal au cours de la deuxième semaine. Au stade qui précéde la métamorphose, la coquille de 220u x 205u (Fig. 1) présente des crénelures larvaires trés visibles, mais non différenciées entre elles. Le ligament est en forme de demi-cercle, du cóté du bord postérieur de la coquille. La dissoconque donne naissance a la premiere dent juvénile. Elle nait sous forme dun bourgeon émergeant du bord de la coquille. La premiére dent apparait sur la valve droite et sur la valve gauche de facon simultanée. Chez une coquille de 292 u x 261 u (Fig. 1) la valve droite présente une lame primitive, I, trés allongée occupant une partie du bord antérodorsal et se con- tinuant jusqu'au milieu du plateau car- dinal. Sur la valve gauche la lame primitive, II, occupe seulement la partie dorsale du bord antérieur de la coquille. Au bout de 40 jours la coquille de 348 u x 316 и (Fig. 2) posséde encore des crénelures larvaires qui s estompent peu a peu. Une dépression médiane apparait sur la lame primitive de la valve droite délimi- tant 2 dents dans un plan inférieur, 1, et supérieur, III. La lame primitive, II, de la valve gauche s est allongée jusqu au liga- ment qui prend une position oblique par rapport au plateau cardinal. A 42 jours la coquille mesure 355 и x 320 и (Fig. 2), la lame primitive de la valve gauche s est recourbée sur elle-méme et $ est aplatie а son sommet. Sur la valve droite la deuxième lame, III, s'allonge. Les crenelures larvaires sont presque т- distinctes. Le ligament devient opisthodete. Au 50e jour la coquille mesure 442 u x 395 u. La valve droite possede une dent juvénile, I, et une lame située au-dessus et qui se divise en 2 dents 3a et 3b. Le sommet de la lame primitive, II, de la valve gauche s est élargi et se scinde en deux parties 2a, 2b, dans за portion médiane. Une deuxieme dent juvénile, IV, nait au centre du plateau cardinal et croit perpendiculairement а ce dernier. Les crénelures larvaires ne sont plus visibles. Le ligament est de plus en plus oblique. 2. Charniere de Venus verrucosa La prodissoconque de 3 jours, 110 их 85 и, a une charniére droite représentée par un plateau cardinal se formant le long du bord dorsal de la coquille. Les crénelures larvaires apparaissent chez la prodissoconque de 5 jours qui mesure 130 их 96 pu. Au 13e jour, la coquille mesure 174 u x 150 u (Fig. 4), les crénelures larvaires sont tres inégales et leur dénombrement est im- possible. Les crénelures larvaires grandis- sent au fur et à mesure que $ épaissit le plateau cardinal qui les porte. Le ligament devient visible lors de la deuxiéme semaine. I] apparait dans le prolongement des crénelures larvaires et a une forme en demi cercle. La premiére dent apparait durant le passage de la prodissoconque а la dissoconque, de facon simultanée pour les 2 valves. Sur une coquille de 21 jours mesurant 220 их 205 u les crénelures larvaires sont trés visibles, inégales et méme absentes en certains endroits; le ligament est bien formé et la premiére dent apparait comme 228 M. L. M. LE PENNEC un bombement intéressant le bord de la coquille. Au 30e jour la coquille mesure 253 их 240 и: la premiere lame s'étale de plus en plus dans la zone des crénelures larvaires (Fig. 4). Au 32e jour la valve droite montre deux lames primitives dis- posées l’une au-dessus de l'autre; il s’agit de la lame I et II. Le ligament prend une position oblique par rapport au plateau cardinal. Les crénelures larvaires disparais- и \ 126 X 95 E / | / \ au = 150 X 126 166 X 134 221 X 205 FIG. 1. Venus striatula—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére (longueur puis largeur) CHARNIERES CHEZ VENERIDAE LARVAIRES 229 sent peu а peu, la lame II de la valve gauche s est recourbée sur elle-méme et son sommet s épaissit. La coquille de 35 jours (Fig. 4) mesure 332 их 308 u. Les lames I et III de la valve droite se sont allongées. La lame II de la valve gauche présente un sommet trés élargi qui va se scinder en deux parties dans sa position médiane pour donner les dents 2b et 2a. Le ligament devient opisthodete. 3. Charniere de Venus fasciata Le plateau cardinal devient visible chez la prodissoconque de 3 jours, mesurant 110 их 88 y (Fig. 6). Les crénelures larvaires apparaissent sur la coquille de 134 u x 102 u. Le ligament se forme des le 7e jour. Au 17e jour la larve se métamorphose et mesure 190 их 158 u (Fig. 6). La premiere lame primitive apparait simultanément sur la valve droite et sur la valve gauche sous forme d'un mamelon intéressant le bord de la coquille auprés de la zone des crénelures larvaires. 348 X 316 Nous observons chez les dissoconques de У. fasciata la formation d'une lame sur le bord de la coquille, auprés du ligament. La dissoconque montre la premiére dent juvénile (Fig. 7). Cette dent s'allonge еп direction de la zone des crénelures lar- vaires. Sur la valve gauche la lame se recourbe sur elle-même et s'étire à son sommet suivant le modéle que nous avons vu chez Venus striatula et Venus verrucosa. Sur la valve droite la premiere dent commence а se différencier du bord de la coquille quand celle-ci mesure 280 u. Avant ce stade elle n'apparaît que sous forme d'un mamelon assez étiré le long du bord de la coquille. Le ligament, d'abord interne et dans le prolongement des crenelures larvaires, devient de plus en plus oblique 4 mesure que la dissoconque grandit. 4. Charniere de Venerupis pullastra Le faible nombre d'échantillons élevés au laboratoire ne nous a pas permis de suivre l’évolution de la charnière de façon a NN 2a VALVE GAUCHE FIG. 2. (longueur puis largeur). 442 X 395 VALVE DROITE Venus striatula—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére 230 MeL. М. LE PENNEC Valve ING Valve gauche и EN LE “à N droite FIG. 3. Venus striatula—1-Prodissoconque de 10 jours: 1404 x 120u-Naissance des crénelures. 2-25 jours: 240u x 220 и:итБо proéminent: crénelures difficilement dénombrables. 3-40 jours: 355 u x 316 u:valve gauche:la lame primitive II se forme valve droite:I et Ш présentes. 4-48 jours: 387 u x 340 u:valve gauche:la lame II donne 2a et 2b bourgeonnement de la lame IV sur le plateau cardinal. aussi nette que dans les cas précédents. d'évolution de la charniére se rapproche Cependant, les quelques observations que de celui de Venerupis aurea. nous avons faites au cours de la croissance Le plateau cardinal s épaissit au fur et à de la larve, montrent que la schéma mesure que grandit la prodissoconque. Les CHARNIERES CHEZ VENERIDAE LARVAIRES 231 plateau cardinal et sont facilement dénom- crénelures larvaires apparaissent au bout brables 2 jours aprés leur naissance (Fig. de 4 à 5 jours aprés la formation de la larve 9). Sur les exemplaires étudiés leur nombre D. Elles poussent perpendiculairement au 126 X 103 И 174 X 150 182 X 166 253 X 245 FIG. 4. Venus verrucosa—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiere (longueur puis largeur). 232 M. ТМ: LE PENNEC varie entre 8 et 10 et est donc inférieur à semaine, dans le prolongement des créne- celui de Venerupis aurea où généralement lures larvaires et dans le même plan que on compte 12. ces derniéres. Comme chez les espéces précédentes le Га premiére dent apparait lors de la ligament apparaît lors de la deuxiéme transformation de la prodissoconque en Valve Valve auc . 7 eue N droite gauche 4 I QA Y / N \ / O 1 FIG. 5. Venus verrucosa—1-13 jours: 1604x140u-Premieres crénelures larvaires. 2-21 jours: 2104x1904-Umbo bien formé. Crénelures non dénombrables. 3-60 jours: 330ux305u-Coexistence dents juvéniles et crénelures. Ligament conservé sur les 2 valves. 4-61 jours: 335ux310u-Dent juvénile de valve droite grandit et s aplatit; crénelures larvaires encore présentes. CHARNIERES CHEZ VENERIDAE LARVAIRES 233 dissoconque, au cours de la troisième sent comme des excroissances se differen- semaine, et de facon simultanée pour les 2 ciant des parois latérales de la coquille, valves. dans un plan inférieur а celui des créne- Les lames primitives, I de la valve lures larvaires (Fig. 9). droite, et II de la valve gauche, apparais- Au bout d 1 mois environ nous voyons 110 X 88 158 X 126 166 X 143 182 X 150 190 X 158 FIG. 6. Venus fasciata—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére (longueur puis largeur). 234 M. L. M. LE PENNEC 2 270 X 240 276Х 243 FIG. 7. Venus fasciata—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entière | 1 (longueur puis largeur). sur la valve gauche (Fig. 9) que les créne- lures larvaires sont encore présentes mais indifférenciées entre elles et tendent а se confondre dans la masse du plateau car- dinal. La lame II s est recourbée sur elle- méme en délimitant avec la paroi de la coquille un profond sillon oú vient prendre place la lame primitive I de la valve droite lors de la fermeture des 2 valves. Le sommet de la lame II s est allongé et on voit nettement qu une dépression se forme dans la partie médiane d'où la formation de 2 parties qui évolueront en dents car- dinales 2a et 2b. Au centre des crénelures larvaires on remarque un petit bourgeon qui est | ébauche de la dent cardinale IV. Le ligament est devenu oblique par rap- port au plan des crénelures larvaires et tente de gagner le bord extérieur de la co- quille pour devenir opisthodete. Sur la valve droite les crénelures lar- vaires sont indistinctes. La lame I est peu visible sur la photo 3 (Fig. 10). La lame Ш, située dans le plan des crénelures est bien formée, la pointe médiane donnera la dent cardinale 3b. Le ligament est oblique et situé sur le bord de la coquille. 5. Charniére de Venerupis aurea Les 2 valves de la prodissoconque de 24 heures sont maintenues jointes gráce au périostracum qui se continue d'une valve á l'autre. Peu а peu le plateau cardinal $ épaissit le long du bord dorsal de la co- quille et des crénelures larvaires apparais- sent au cours de la premiére semaine. Mais, alors que chez les 3 espéces du genre Venus les crénelures étaient indifféren- ciées, ici elles sont facilement dénom- brables 2 jours aprés leur formation (Fig. 11). On en compte généralement 12, de taille variable. Le ligament se forme lors de la deux- iéme semaine comme dans le cas des 4 es- peces précédentes. La naissance de la premiére dent a lieu chez la dissoconque de facon simultanée pour les 2 valves et suivant le schéma que nous connaissons (Fig. 11). Les crénelures larvaires sont encore trés visibles chez le juvénile (Fig. 11 et 12). Sur la valve gauche la lame II se recourbe et son sommet s élargit pour donner les 2 dents juvéniles 2a, 2b. Au centre de la zone des crénelures larvaires et done dans un plan supérieur а celui de la lame Il apparrait la CHARNIERES CHEZ VENERIDAE LARVAIRES 235 Valve Valve gauche Grouse o = FIG. 8. Venus fasciata—1-14 jours: 18lux150u-Crénelures présentes mais non dénombrables. 2-21 jours: 230ux197u-Ligament visible sur les 2 valves. 3-23 jours: 250ux220u-Naissance de la premiere lame primitive. 4- 41 jours: 276ux225u-Crénelures encore fonctionnelles. 5-45 jours: 290ux275u-Premiére dent bien visible. 236 M. L. M. lame IV. Sur la valve droite les 2 lames I et ПГ se sont formées dans 2 plans différents, la lame Ш, au niveau des crénelures lar- vaires, la lame I dans un plan inférieur. Ces 2 lames sont bientót séparées par un profond sillion. Le ligament est de plus en plus oblique par rapport au plateau cardinal et finit par gagner le bord antéro-supérieur de la co- quille. Les crénelures larvaires sont encore visibles sur la coquille de 790 u x 670 u. La dissoconque de 840 u x 750 и (Fig. 12) montre que sur la valve gauche la lame primitive IV pousse perpendiculairement au plateau cardinal en laissant une fossette entre elle et la dent 2b, ой vient se loger la dent 3b de la valve droite. Les dents 2a et 2b divergent dune de l'autre à partir dune partie commune qui tend a gagner l'umbo (coquille de 1150 их 1020 и). Dans la fossette ainsi formée par les dents 2a et 2b vient se loger la dent I de la valve droite. Sur la valve droite les dents 3a et 3b forment entre elles un angle presque droit et délimitent, avec la dent I, un profond sillon ой viennent prendre place les dents 2a et 2b de la valve gauche. Га coquille de 4,000 и nous montre l'allure presque définitive de la charniere. 200 X190 LE PENNEC Les dents semblent diverger a partir de l'umbo, vers la base du plateau cardinal en délimitant entre elles de profondes fossettes. Le ligament d'abord interne et situé dans le prolongement des crénelures lar- vaires a maintenant gagné le bord externe antéro-supérieur de la coquille; il est devenu opisthodete. CONCLUSION D'après les renseignements ainsi obtenus nous pouvons dresser une cl& de determination pour les 5 especes étudiées (Fig. 15). Il ressort de ce tableau une difference entre les crénelures de la char- niere du genre Venerupis et Venus qui permet de distinguer ces deux genres dés les premiers stades de vie larvaire. Chez Venerupis aurea et Venerupis pullastra les crenelures larvaires sont dénombrables peu de temps aprés leur for- mation et persistent longtemps aprés Гар- parition des premiéres dents juvéniles. On peut encore les observer sur une coquille ágée de 40 jours et mesurant 400 u en- viron. Il semble que chez Venerupis aurea le nombre des crenelures larvaires est FIG. 9. Venerupis pullastra—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille en- tiere (longueur puis largeur). CHARNIERES CHEZ VENERIDAE LARVAIRES 237 - Valve gauche Valve droite FIG. 10. Venerupis pullastra—1-10 jours: 180ux170u:Crénelures larvaires apparaissant nettement. 2-20 jours: 215ux205u:Bourgeonnement lames primitives I (V.d.) et II (V.g.): ébauches dents cardinales. Ligament visible. 3-27 jours: 364ux323u :Crénelures larvaires régressent cependant que dents cardinales se différencient. supérieur a celui de Venerupis pullastra (12 dans le premier cas pour 8 4 10 dans le second cas). Ce serait donc un caractére de différenciation de ces 2 expéces. Chez Venus striatula, Venus verrucosa et Venus fasciata les crénelures larvaires forment une zone indifférenciée, le long du plateau cardinal. Elles perdent trés vite leur identité lors de la formation des dents juvéniles. Enfin, chez Venus fasciata les dis- soconques possèdent des formations latérales qui les différencient de celles de Venus verrucosa et Venus striatula. Un caractère morphologique externe déja signalé par Rees en 1950 permet de separer Venus verrucosa et Venus striatula: cette derniere possede des stries de croissance très marquèes, des la deuxiéme semaine. On peut supposer que l'observation des charniéres de bivalves au microscope élec- M: L. М. LE PENNEC bo C2 00 118 X 95 141 X 125 237,X 229 323 X 308 379 X 340 426 X 402 L MN Els SEN FIG. 11. Venerupis aurea—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére (longueur puis largeur) CHARNIERES CHEZ VENERIDAE LARVAIRES 239 626 X 550 E 840X 750 1140 X1020 FIG. 12. Venerupis aurea—Pour chaque dessin sont indiquées les dimensions en microns, de la coquille entiére (longueur puis largeur). 240 М. L. М. LE PENNEC tronique а balayage permettra de se faire une idée plus exacte sur la genése des dents (lieu de formation, formes, dimen- sions, nombre, etc. ). Les quelques résultats x x So que nous avons déjà obtenus confirment cette hypothese. Il sera alors possible, en combinant l'étude des charniéres au microscope op- Valve droite a. y FIG. 13. Venerupis aurea—1-5 jours: 120ux104u: Prodissoconque au stade de la charnière droite; les crénelures larvaires se forment. 2-14 jours: 197ux181a: Crénelures facilement dénombrables. Ligament bien conservé sur valve droite. 3-30 jours: 235ux218u: Formation premiere dent juvénile. 4-34 jours: 290ux260u: Crénelures lar- vaires et premiere dent juvénile. CHARNIERES CHEZ VENERIDAE LARVAIRES 241 tique et au microscope électronique а critéres les plus sûrs pour établir l'identité balayage, de conclure que examen des des larves de bivalves récoltées dans le charniéres des coquilles larvaires est un des plancton. Valve gauche FIG. 14. Venerupis aurea—5-40 jours: 370ux340u: Lame primitive 11 (У. gauche) III (У. droite). 6-60 jours: 500ux485u: Bourgeonnement lame IV sur valve gauche. 7-64 jours: 840ux750u: Les dents juvéniles grandissent. 8-70 jours: 11404x10204: Charniére juvénile totalement transformée. Les dents prennent leur allure definitive. 242 М. L. М. LE PENNEC aprés la fécondation 36-48 heures 70-100 p Prodissoconque de Bivalves lére semaine at QC) ® Famille des Veneridae Un trait caractéristique : épaules dissymétriques Crénelures distinctes: Crénelures indistinctes : Cas général genre Venerupis genre Venus PA eS Généralement 12 crénelures De 8 а 10 crénelures Umbo proéminent : Forme globuleuse de a y e es : E | la coquille : Е Venerupis aurea Venus strtatula Venerupts pullastra : 7 Stries de croissance Venus verrucosa As . seme semaine 0-400 )-400 р 5 Présence de formations latérales: FL: Venus fasciata -Persistance des crénelures larvaires aprés la formation des lames primitives : genre Venerupis. -Disparition des crénelures larvaires lors de la formation des lames primitives : genre Venus. FIG.15. Clé de determination pour 5 especes de Veneridae. CHARNIERES CHEZ VENERIDAE LARVAIRES REFERENCES BIBLIOGRAPHIQUES BERNARD, F., 1895-97, Sur le développe- ment et la morphologie de la coquille chez les lamellibranches. Bull. Soc. géol. France, Ser. 3, 23 (1895): 104-154; 24 (1896): 54-82, 412-449; 25 (1897): 559-566. CHANLEY, Р. E., 1965, Larval development of the large blood clam, Noetia ponderosa (Say). Proc. natn. Shellfish. Assoc., 56: 53-58. CHANLEY, P. E., 1969, Larval development of the coquina clam, Donax variabilis Say, with a discussion of the structure of the lar- val hinge in the Tellinacea. Bull. mar. Sci., 19: 214-224. LE PENNEC, M., 1970, Elevages au laboratoire de Mollusques Bivalves: Morphogenese de la coquille des Veneridae. These de Зе cycle: 1-95. LE PENNEC, M. € A. LUCAS, 1970, Com- parative growth and morphology of some 243 Venerid larvae (Bivalvia, Veneridae). Malacol. Rev., 3: 175-183. LOOSANOEE V. lL.) & He С. DAVIS; 1963, Rearing of bivalve mollusks. In: Advances in Marine Biology. F. S. Russell, Ed., Academic Press, Inc., London, 1: 1-136. NEUMAYR, 1891, Beitrage zur liner morphologischen Eintheilung dee Bivalven. Densk. К. К. Akad. Wiss. Wien, math. nat. cl., 58: 701-801. REES, С. B., 1950, The identification and classification of lamellibranch larvae. Hull Bull. mar. Ecol., 3: 73-104. SULLIVAN, C. B., 1948, Bivalve larvae of Malpeque Bay, Р.Е.1. Bull. Fish. Res. Bd. Canada, 77: 1-36. WERNER, B., 1939, Uber die Entwicklung und Artum terscheidung von Muschellarven des Nordseeplanktons, unter besonderer Berücksichtigung der Schalenentwicklung. Zool.-Jahrb. Abt. Anat., 116(1): 1-54. ABSTRACT MORPHOGENESIS OF THE HINGE IN 5 SPECIES OF VENERID BIVALVES M. L. M. Le Pennec Laboratory culture of 5 species of Veneridae from the coast of Brittany has provided data on the development of the hinges. Metamorphosis was accomplished by all species. Daily observations of larval shells allowed detailed observations of the growth of the hinge: first the notches of the prodissoconch, then formation of the first thin plates of the dissoconch, and finally the regression of the notches. We have also noted the formation and position of the ligament. The results have been used to construct a key for the iden- tification of the 5 species. The genus Venerupis is characterized, from the end of the first week, by obvious notches whereas these remain indistinct in the genus Venus. Within the genus Venerupis, variation in the number of notches allows one to distinguish the species: Venerupis pullastra has 8-10, Venerupis aurea generally 12. At the end of the second week lateral formations appear in Venus fasciata. The marked striations on the Venus striatula shell aid recognition of this species. No particular morphological character is applicable for Venus verrucosa. It seems from this study that larval hinge structure is a good criterion for identification of larval bivalves taken from the plankton. However, larval identification using this method is not possible before establishment of the hinge which occurs at the end of the first week. ZUSAMMENFASSUNG MORPHOGENESE DES SCHLOSSES BEI FUNF MUSCHELARTEN DER FAMILIE VENERIDAE M. L. M. Le Pennec Laborzuchten von 5 Veneriden von der Kiiste von Brittany haben Daten zur Schloßentwicklung erbracht. Die Metamorphose wurde von allen Arten vollständig 244 M. L. M. LE PENNEC durchlaufen. Tägliche Beobachtung der Larvengehäuse erlaubte, das Schloßwachstum eingehend zu verfolgen: zuerst die Einkerbung des Prodissokonchs, dann die Bildung der ersten dünnen Dissokonch-Platten, schließlich das Verschwinden der Kerben. Auch über Bildungsweise und Anlageort des Ligaments konnte Aufschluß gewonnen werden. Die Ergebnisse wurden dazu verwendet, einen Schlüssel zur Identifikation der 5 Arten aufzustellen. Die Gattung Venerupis ist vom Ende der 1. Woche an durch auffällige Kerben gekennzeichnet, die dagegen in der Gattung Venus undeutlich bleiben. Innerhalb der Gattung Venerupis erlaubt die Differenzierung der Kerbenzahl die Artunterscheidung: Venerupis pullastra hat 8-10, Venerupis aurea im allgemeinen 12. Am Ende der 2. Woche erscheinen laterale Bildungen bei Venus fasciata. Die kräftige Streifung auf der Schale von Venus striatula erleichtert das Erkennen dieser Spezies. Für Venus verrucosa gibt es kein verwendbares besonderes morphologisches Kennzeichen. Nach den vorliegenden Untersuchungen scheint der larvale Schloßbau ein geeignetes Merkmal zur Bestimmung von Muschellarven aus Planktonfängen darzustellen. Die Larvenbestimmung nach dieser Methode ist allerdings erst nach Anlage des Schlosses möglich, also vom Ende der ersten Lebenswoche an. C.M.-B. RESUMEN MORFOGENESIS DE LA CHARNELA EN CINCO ESPECIES DE BIVALVOS VENERIDOS M. L. M. Le Pennec El cultivo en laboratorio de cinco especies de Veneridae de la costa de Bretaña suministró datos sobre el desarollo de la charnela. Todas las especies tuvieron metamor- fosis. Se observó diariamente en detalle, el crecimiento de la charnela de las conchillas larvales: primero las muescas de la prodisoconcha, formación de las primeras delgadas placas de la disoconcha, y finalmente la regresión de las muescas. Se notó también la for- mación y posición del ligamento. Los resultados se utilizaron para construir una clave de identificación para las cinco especies. El género Venerupis se caracterizó, al finalizar la primera semana de desarrollo, por las muescas muy evidentes, mientras que estas permanecieron indistintas en el género Venus. Dentro de Venerupis, la variación en el número de muescas permite distinguir las especies: Venerupis pullastra con 8-10, Venerupis aurea generalmente con 12. Al ter- minar la segunda semana aparecieron, en Venus fasciata, formaciones laterales. Las mar- cadas estrias en la concha de Venus striatula contribuyen al reconociemto de esta especie. Ningún caracter morfologico particular es aplicable a Venus verrucosa. Este estudio parece desmonstrar que las estructuras larvales de las charnelas, otrecen un buen criterio para la identificación de bivalvos larvales tomados del plankton. Sin em- bargo, tal método de identificación larval no podria usarse antes del establecimiento de la charnela, el cual ocurre al final de la primera semana de desarrollo. J.J.P. CHARNIERES CHEZ VENERIDAE LARVAIRES ABCTPAKT МОРФОГЕНЕЗ ЗАМКА У 5 ВИДОВ МОЛЛЮСКОВ ИЗ CEM. VENERIDAE (BIVALVIA) М.Л. ЛЕ-ПЕННЕК В лабораторной культуре у 5 видов двустворчатых моллюсков Veneridae с берегов Британии были получены данные по развитию замка. У всех видов был прослежен метаморфоз. Ежедневные наблюдения развития личиночных раковин сопровождались детальными наблюдениями роста замка: сначала выемок продиссоконха, затем образования первой тонкой пластинки диссоконха и, наконец, - регрессии выемок продиссоконха. Отмечено также образование и расположение лигамента. Полученные результаты были использованы для ключа для определения 5 видов моллюсков. Род Venerupis характеризуется, начиная с конца первой недели жизни, наличием заметных выемок, которые у видов рода Venus неразвиты. Внутри рода Venerupis изменение количества выемок имеет видовое значение: y Venus pullastra ux 8-10, у Venerupis aurea обычно 12. В конце первой недели развития у Venus fasciata появляются слабые боковые выросты, а заметная исчерченность раковины y Venus striatula помогает определить этот вид. У Venus verrucosa нет никаких особых морфологических отличий. Из этих наблюденнй выяснилось, что структура личиночного замка является хорошим критерием для идентификации личиночных планктонных форм двустворчатых моллюсков. Однако, определение этим методом видов на личиночной стадии возможно лишь после образования замка, в конце первой недели жизни. Zi AT: 245 a Br — WED _ Fs yw ie Oly HAVAADEMUAIA MOST PRE ТАУ no . | N а’ ak } D в | Om zu = & | y on р ' Ú } = = 5 mt ый В LD) . u $ ' PA у 7 > т u Г "1" > $ MALACOLOGIA, 1973, 12(2): 247-263 EFFECT OF CARBONIC ANHYDRASE INHIBITION PENETRATION BY THE MURICID GASTROPOD UROSALPINX CINEREA ОМ SHELL Melbourne В. Carriker! and Howard H. Chauncey? ABSTRACT A study was made of the effect of a series of concentrations of DiamoxR(2-acetylamine- 1,3,4-thiadiazole-5-sulfonamide), a specific inhibitor of the enzyme carbonic anhydrase (CA), on the penetration of shell of the oyster Crassostrea virginica by the boring muricid gastropod Urosalpinx cinerea follyensis. Forty-five initially boring snails con- tinued boring and fed on oysters in Diamox solutions ranging in concentration from 5x- 10-4M to 1x10°2M. Forty-five initially nonboring snails identified, mounted, and began penetration in the same range of concentrations. Snails were able to complete boreholes and to feed in concentrations up to 5х10-3М. The total number of complete boreholes decreased by 2/3 while the total number of incomplete holes almost doubled with increasing concentrations of Diamox during the 6 day experiment. All 90 snails survived the 6 days, as well as an additional month in nor- mal running seawater where they bored and fed actively. Blots of secretion collected from active accessory boring organs (ABO) of live snails on a valve model, as well as secretion released by the ABO in the ABO pore, were positive for CA when tested by histochemical techniques. Treatment with Diamox inhibited the CA in both. Control halves of ABOs, excised from actively boring snails, etched polished shell, while increasing concentrations of Diamox applied to the experimental half of these ABOs, increasingly reduced etching. In the 5х10-3М and 1х10-2М solutions the etching was almost totally inhibited. A suspension of pure bovine erythrocyte CA in seawater produced no etching of shell. These experiments indicate that CA plays a vital role in shell dissolution during boring by this species of snail, but do not confirm its function as a direct demineralizing agent. INTRODUCTION The calcareous exoskeleton of bivalves such as Crassostrea virginica (Gmelin) and Mytilus edulis Linné can be penetrated by many marine invertebrate predators (Carriker & Smith, 1969). The penetrating behavior of one, Urosalpinx cinerea (Say), has been described (Carriker, 1969; Carriker & Van Zandt, 1972). The shell of the bivalve prey of Urosalpinx cinerea consists of calcium car- bonate in the form of calcite and aragonite crystals embedded in organic matrices (Travis & Gonsalves, 1969; Mutvei, 1969, 1970; Taylor, Kennedy & Hall, 1969). As currently understood, boring in- volves a chemical phase followed by a mechanical phase. During the chemical phase the accessory boring organ (ABO) is extended into the borehole and secretes a substance that dissolves a thin layer of the shell. In the mechanical phase the pro- boscis is extended into the borehole and the bottom is briefly rasped by the radula. The weakened shell removed by the radular cusps is then swallowed by the snail. By repeated alternation of chemical activity and mechanical rasping, the snail penetrates the shell of its prey, inserts its proboscis and initiates feeding on the soft tissues within. ISystematics-Ecology Program, Marine Biological Laboratory, Woods Hole, Massachusetts 02543, U.S.A.—Pre- sent address: College of Marine Studies, Field Station, University of Delaware, Lewes, Delaware 19958, U.S.A. 2Veterans Administration Center, Bay Pines, Florida 33504, U.S.A. (247) 248 CARRIKER AND CHAUNCEY Various hypotheses have been offered to explain the chemical phase of shell penetration. These include solubilization by acids, proteolytic enzymes, and chelating substances (Carriker, Scott & Martin, 1963; Carriker € Smith, 1969). The histochemical localization of cyto- chrome oxidase and succinic dehydro- genase in the secretory epithelium of the ABO has provided an indication that these cells can metabolize aerobically (Person et al., 1967). In addition these cells contain dense populations of mitochondria (Nylen, Provenza & Carriker, 1969), and the secre- tion in actively boring snails has a pH of approximately 3.8 (Carriker, Charlton & Van Zandt, 1967). Since carbonic anhydrase is involved in aerobic respira- tion and is responsible for the formation of hydrochloric acid in human gastric mucosa, we assumed that carbonic anhydrase should be present. Subsequently, Smarsh et al. (1969) demonstrated carbonic anhydrase activity in the microvillar zone of the ABO in both actively boring and inactive snails. Histo- chemical localization of carbonic anhydrase revealed that the secretory epithelium of the ABO exhibited very high activity, in contrast to tissues such as con- nective tissue of the ABO stalk, the buccal mucosa, and the esophagus. Only the car- tilages of the odontophore, the mantle, and certain muscle groups of the proboscis showed nearly comparable activity. The addition of DiamoxR (2-acetylamine-1,3,4- thiadiazole-5-sulfonamide) in concen- trations as low as 2x10-5M inhibited the carbonic anhydrase activity. In vitro chemical assay of carbonic anhydrase and total nonspecific esterase activities in homogenates of the ABO of Urosalpinx cinerea were carried out (Carriker et al., 1968). Samples from 60 nonboring, 75 boring, and 60 feeding snails were evaluated. Alpha naphthol acetate was used as substrate for non- specific esterase, and Diamox inhibition was used to reveal carbonic anhydrase ac- tivity. Specific enzyme reactivity was recorded in nanomoles/min/mg of pro- tein. Carbonic anhydrase activity was es- sentially identical for each of the 3 groups, being 0.88+0.11, 1.04+0.10, and 0.95+0.01, respectively. Preliminary results of differential centrifugation studies т- volving isolation of a 30,000 xg pellet, a 105,000 xg pellet, and the 105,000 xg supernatant fluid indicated that most of the carbonic anhydrase and nonspecific es- terase activities were present in the 105,- 000 xg supernatant fluid. The presence of carbonic anhydrase ac- tivity in the ABO suggested that this en- zyme might be a responsible factor in the production of certain substances used in the chemical phase of shell penetration by Urosalpinx cinerea. The purpose of this paper is to report the effect of Diamox, a specific inhibitor of carbonic anhydrase, on the penetration of shell by live boring U. cinerea; the presence of carbonic anhydrase in the ABO secretion after its normal release by the gland; the effect of Diamox on etching of polished shell by the excised ABO; and the action of pure car- bonic anhydrase on polished shell. The study, begun in the summer of 1967, was carried out at the Marine Biological Laboratory, Woods Hole (Carriker, 1967). MATERIALS AND METHODS The following experiment was con- ducted to determine the effect of a graded series of Diamox? concentrations on the capacity of living snails (Urosalpinx cinerea follyensis Baker) to identify, mount, bore, and feed on _ oysters (Crassostrea virginica(Gmelin)).The snails were collected in Wachapreague, Virginia. They had been maintained in our laboratory for several weeks in running seawater, and fed local oysters. Ninety snails, 28-40 mm in shell height, and 15 clean oysters, 6-8 ст long, were divided into 5 groups containing 18 snails and 3 oysters each. Each group contained 9 bor- ing snails, 3 per oyster, and 9 nonboring snails, in a continuously aerated clean glass dish 20 ст in diameter (Figs. 1, 2). 3 Diamox supplied by Lederle Laboratories Division, American Cyamid Co., Pearl River, New Jersey. INHIBITION OF SHELL PENETRATION BY UROSALPINX 249 FIG. 1. Arrangement of 5 aerated covered dishes in running seawater of relatively constant temperature (about 20С) used in study of effect of graded series of concentrations of Diamox on the capacity of live Urosalpinx cinerea follyensis to identify, mount, bore, and feed on Crassostrea virginica. Each dish 20 cm in diameter. FIG. 2. Positions of marked Urosalpinx cinerea follyensis and Crassostrea virginica in one of the dishes photographed in Fig. 1. 250 CARRIKER AND CHAUNCEY To obtain boring snails, we placed oysters in the stock tank of snails 36 hours prior to the experiment. At the time of transfer all but 3 of the snails which had mounted and were boring were removed from each oyster. Nonboring snails were those which neither had been boring nor feeding, but were crawling on the sides of the stock tank. They were identified by a mark on the shell spire, and placed at ran- dom on the bottom of each bowl. The following concentrations of Diamox, in clear unfiltered seawater, were employed: 5х10-4М, 1х10- 3M, 5х10-3М, and 1х10-?М. The final pH of the sea- water solution was adjusted to 8.10+0.02 with 0.1N HCl. It was calculated that the resultant NaCl formed by HCl neutraliza- tion of the sodium hydroxide in the con- centrated Diamox solution did not significantly alter the salinity (from 320/00 to 330/00) of the test solutions. The sea- water control (pH 8.12) contained neither Diamox nor HCl. One liter of solution was placed in each of the 5 dishes. Aeration by bubbling was carefully controlled in each dish to maintain a uniform level of oxygen and permit normal oxidation of metabolites released by the oysters and snails. The dishes, loosely covered with glass plates to keep the snails from crawl- ing out, were immersed in a shallow tray of running seawater at approximately 20°C (Fig. 1). Throughout the day, and oc- casionally in the early evening, fluorescent light illuminated the experiment. On day 3 the solutions were replaced us- ing clean dishes. The experiment was ter- minated after 6 days. A daily record of the number of nonboring and boring snails on each oyster, and whether the oysters were closed or pumping, was maintained. At the termination of the experiment the snails from each dish were placed in separate perforated plastic cages containing fresh oysters. Similarly, the nonpenetrated oysters, as well as the penetrated but still viable oysters, were placed in perforated cages. The cages were immersed in run- ning seawater. This was done to determine the rate of recovery and ability of the snails to bore after the Diamox treatment. The live oysters were continuously observed to note their recovery, or expiration due to penetration injury. The series of Diamox concentrations used was based on the concentration re- quired to inhibit reactivity of carbonic anhydrase in frozen sections of snail tissue for a minimum of 3 hours (Smarsh et al., 1969). In preliminary tests in nonaerated seawater we noted that boring was prac- tically nonexistent, even in the seawater control, while a final Diamox concentra- tion of 5x10 2M, first inactivated and then proved lethal to both snails and oysters. It was also observed that if filtered (Millipore) seawater was used none of the nonboring snails mounted or bored oysters. For these reasons unfiltered aerated seawater was used. The presence of carbonic anhydrase in the ABO secretion, after its release from the gland, was investigated both with specimens of secretion collected using a valve model and with frozen sections of snail pedal tissue. For the collection of specimens of secre- tion, we allowed a snail to penetrate ap- proximately halfway through the shell of an oyster. Then the opposing oyster valve and the flesh were removed underwater. Next the valve and snail were inverted and supported in running seawater under a binocular microscope (Carriker € Van Zandt, 1972). When the snail penetrated the upturned inner surface of the valve and the borehole was of sufficient diameter to allow the ABO to extrude, but was not wide enough to accommodate the full proboscis, we elevated the valve model until its inner face was above the water. Seawater remaining around the borehole was thoroughly removed Бу blotting. Under these conditions the snail main- tained the ABO in the borehole and con- tinued to secrete fluid. A small wedge of cellulose acetate Millipore filter paper (Зи pore size) was placed on the crown of the exposed ABO to absorb the thin layer of secretion. The filter paper was then air dried at room temperature for 20 min. Representative specimens were taken from several snails. The sections of filter paper, INHIBITION OF SHELL PENETRATION BY UROSALPINX 251 unfixed, but air dried, were then processed for carbonic anhydrase activity (Smarsh et al., 1969). For the demonstration of carbonic anhydrase in the ABO pore, we removed a cube of pedal tissue surrounding the with- drawn ABO after the shell was cracked and the foot amputated. Unfixed frozen sec- tions of the cube, cut 9-12u thick in a cryostat, were placed on filter paper and tested for carbonic anhydrase by a modification of Häuslers (1958) tech- nique (Smarsh et al., 1969). Sections from several snails were examined. Inhibition by Diamox, in a concentration of 2x10-5M, was used as a confirmatory test for the presence of carbonic anhydrase, both for the secretion collected and the material within the ABO pore. To study the effect of Diamox on the etching capacity of excised ABOs, we em- ployed a device (Fig. 5) patterned after an earlier model (Carriker € Van Zandt, 1964). The ABO was excised from large, actively boring Urosalpinx cinerea in the manner described by Carriker et al. (1963). It was then placed in a drop of seawater on a teflon block, and cut into 2 equal parts. One half was placed in seawater while the other half was put in seawater-Diamox solution for either 5 or 10 min. The con- centrations of Diamox used were: 5x- 10-4M, 1х10-3М, 5х10-3М, and 1х10-2М. ABO halves were then transferred in а drop of seawater or Diamox solution to a small piece of plastic plankton cloth (pore size approximately 854) which was overly- ing the inner nacreous surface of a square of polished surf clam (Spisula solidissima) shell. The ABO sections were then covered with a disk of thin plastic membrane. A minute collar of lead weighted the edge of the membrane. This membrane kept the gland moist and pressed it gently against the underlying cloth screen which allowed the secretion expressed from the gland to contact the surface of the shell. The gland-shell preparation was held in a moist chamber at room temperature for 21 hrs. During this time pressure from the taut plastic membrane and relaxation of the half gland caused it to spread to about twice its original diameter (0.5 to 0.8 mm). At the end of the incubation period, the half ABO was flushed from the shell with seawater, and the shell surface quickly rinsed with distilled water and rapidly dried with a stream of air. The etched sur- face was then coated in vacuum with gold and subsequently examined as well as photographed with the light microscope and with a scanning electron microscope (JEOLCO JSM-U3). The action of pure carbonic anhydrase on polished shell was demonstrated as follows: one end of a 6 mm section of intra- medic polyethylene tubing with an inter- nal diameter of 6 mm was fastened to the surface of a polished shell with a thin layer of Dow Corning high vacuum grease. Ten sections were thus secured to squares of polished shell. Care was taken to insure that the shell surface within the diameter of the tube was free of grease. Three drops of filtered fresh seawater were pipetted into 5 tube sections as controls, while 3 drops of a freshly prepared seawater solu- tion of carbonic anhydrase, from bovine erythrocytes (Mann Biochemicals) con- taining 1 mg/ml (pH 8.15), were added to each of the remaining tube sections. The outer end of each section was then covered with a disk of plastic membrane to control evaporation. After incubation at room temperature for 18.5 hrs., the tube sections were remov- ed and the shell surface was rapidly wash- ed with distilled water. The surface was then immediately dried with a stream of air and examined with direct as well as polarized incident light at 200 and 400 magnifications. RESULTS Effect of Diamox on boring. None of the snails, or oysters which escaped pene- tration, died during the 6 day experiment. Daily checks of the oysters showed that some were open in all solutions of Diamox. Two oysters which gaped after being bored, 1 in the seawater control and 1 in the 1x10°3M Diamox, were completely de- fleshed by feeding snails. The number of initially boring snails bo 52 which remained on oysters, as well as the number of initially nonboring snails which mounted oysters and remained mounted, decreased with time (Table 1). The 6-day cumulative number of initially boring snails on oysters did not vary in accordance with different Diamox concentrations in each of the 5 containers. In contrast the cumulative number of initially nonboring snails decreased slightly with increasing concentrations of Diamox. The total number of boreholes, both in- complete and complete, on the valves of the 3 oysters in each dish was 14+2. While the total number of boreholes per dish was not significantly different, the ratio of completed to incompleted boreholes in the control versus the Diamox solutions was quite different. Whereas the seawater con- trol and the 5x10°*M and 1х19-3М Diamox solutions had an equal or greater number of complete holes than incomplete holes, the 5х10-3М and the 1x10-2M solutions of Diamox had 2x and 4x as many incomplete holes as complete holes, respectively. The data indicate that an average of 78% of the initially boring snails in the 4 TABLE 1. CARRIKER AND CHAUNCEY Diamox solutions continued boring, while 67% of the initially boring snails in the seawater control dish remained boring. On the other hand, only 47% of the initially nonboring snails in the Diamox solutions mounted and remained mounted, while 67% of the initially nonboring snails in the seawater control were mounted. The 90 snails employed in the experi- ment all survived for the next month, dur- ing which they bored and fed actively on small oysters, mussels, and surf clams. Viability and recovery of oysters in each of the concentrations of Diamox in sea- water were as follows: 5x10~4M. Out of 3 oysters, 2 had 3 com- plete boreholes and 1 had 2 complete holes. All 3 oysters were alive at the ter- mination of the study, but died within 7 days after being placed in running sea- water. 1x10°3M. One of the 3 oysters con- tained 4 complete boreholes and was con- sumed during the experimental period. The 2nd oyster, with 1 complete hole, died 2 days after isolation in running seawater, while the remaining oyster, which had 2 holes, died after 30 days. Effect of Diamox solution on shell penetration by live Urosalpinx cinerea. Three oysters and 18 snails per dish, initially 9 boring snails (on oysters) and 9 nonboring snails. Cumu- Ps No. snails on lative No. boreholes in oyster shells Diamox Initial к É ers LES Cis ; be oysters per day по. snails after 6 days concentration activity Е E of snails Sen я а 1 2 3 4 5 6 ters in Incomplete Complete Total 6 days Seawater Boring Во. 6 "107225 36 1 9 16 Nonboring Tt MG) ES A Wat) att! 36 0.0005M Boring eh. OS tor le) 46 4 5 12 Nonboring COTTON об 37 0.001 M Boring Ta” a ee Oe a? 37 7 7 14 Nonboring NIDO AI 5 ИЗ 29 0.005 M Boring OIE SS IH 46 10 5 15 Nonboring Bea On Ar 24 0.01M Boring rl 515 40 11 3 14 Nonboring 6 1 1 7 29 13 Total Boring 40’ 40°86 °86 31722 Nonboring 29 25 24 19 18 24 a a - р 3 Indicates number from maximum of 9. b One of the oysters gaping, snails feeding on it; flesh removed by following day. INHIBITION OF SHELL PENETRATION BY UROSALPINX 253 wedge C/7 FIG. 3. Sketch of a blot of secretion from the accessory boring organ of Urosalpinx cinerea follyensis on a wedge of Millipore paper demonstrating reactivity of carbonic anhydrase (CA), black granules, by Hiusler’s test. Diameter of blot about 1.5 mm. ИВО SIRUS 120) ИВО stalk ProPOoIIUM ABO pore CA FIG. 4. Diagram of a frozen median sagittal section of the accessory boring organ of a male Urosalpinx cinerea follyensis, cut from a cube of pedal tissue, demonstrating reactivity of carbonic anhydrase (CA), black granules, in secretion released by the accessory boring organ into the pore and outside the foot onto the supporting paper. Háusler's test. Accessory boring organ about 1 mm wide. 5x10 3M. One oyster which contained only 1 newly completed borehole survived beyond the 30 day holding period. Of the 2 other oysters, with 2 holes each, 1 sur- vived for 7 days while the other died 14 days after isolation. 1x10°2M. Only 2 oysters contained com- plete boreholes, and 1 had 2 newly com- pleted holes. This latter oyster and the one which was not penetrated survived throughout the 30 day recovery period. The remaining oyster, with 1 complete hole, died 3 days after termination of the test period. Seawater control. The 3 oysters in this container each had 3 complete boreholes. Two oysters died during the experimental period, and the 3rd died 3 days after isola- tion. Release of carbonic anhydrase in ABO secretion. The specimens of ABO secre- tion collected with Millipore paper and in- cubated in Háusler's substrate were all distinctly positive. The dried secretion which initially was a light watery-cream color exhibited a vivid black granular deposit (Fig. 3). Treatment of represen- tative specimens with 2x10 5M Diamox completely inhibited activity. The material present in the ABO vestibule and pore also showed a positive carbonic anhydrase reaction. Black 254 CARRIKER AND CHAUNCEY granules were conspicuously present within the vestibule, adjacent to the secretory eqithelium of the ABO, and on the paper outside the pore (Fig. 4). Activi- ty was inhibited by 2х10-5М Diamox. Effect of Diamox on etching by excised ABOs. The ABO halves excised from ac- tively boring snails and tested in seawater etched the polished surface of shell from Spisula solidissima (Figs. 6, 7). The degree of etching varied from very deep to a trace (Table 2). The same variability of etching by whole excised ABOs, from both boring and nonboring snails, was observed previously (Carriker et al., 1963). Thus the variability observed in the experiment was not attributed to dissecting the glands. In 5x10°-4M Diamox the half ABOs etched slightly more conspicuously than in the seawater controls, while in the 1x10°3M Diamox etching activity was reduced ap- proximately by half. In the 5х10-3М and 1x10°2M Diamox solutions only a faint trace of etching was evident. Action of pure carbonic anhydrase on polished shell. No etching of the shell sur- face was visible either with the seawater or the carbonic anhydrase solution at magnifications up to 400X. DISCUSSION The current investigation revealed that initially boring Urosalpinx cinerea were able to continue boring and feed on oysters in concentrations of Diamox ranging from 5x10-4M to 1x10°2M, while initially in- active snails, to a lesser degree, were able to identify, mount, bore, and feed on oysters in all but the highest Diamox con- centration. In addition, the number of complete boreholes decreased, while the number of incomplete holes increased, with increasing concentrations of Diamox. However, the cumulative number of bore- holes, complete as well as incomplete, was quite constant for the seawater control and 4 Diamox solutions. The observation that initially inactive snails mounted and bored oysters would seem to indicate that the oysters were ac- tive, at least for a time, since snails usually will not mount and bore closed oysters (Carriker & Van Zandt, 1972). The aban- donment of oysters by a few of the initially boring snails, after transfer to the dishes, was probably due to the mechanical dis- turbance. Certain of the initially inactive snails never mounted oysters. This is often the case with inactive or nonboring snails, probably because they are not hungry. Furthermore, oysters with almost no food, as was the case in the containers, soon become less attractive to resting snails. This may also explain, in part, why few snails mounted oysters after the experi- ment was in progress. The occasional movement of snails on and off oysters accounted for the apparent disparity between the total number (complete plus incomplete) of holes in oyster valves in each container and the total number of mounted snails (initially active plus initially inactive) on oysters in the same dish on any given day. The fact that most initially inactive snails which had mounted oysters crawled off by the BG RY OF 2218 collar membrane seawaler FIG. 5. Diagram of the cross section of a square of polished shell of Spisula solidissima and accessories used to test etching (dissolution) by an excised half accessory boring organ of Urosalpinx cinerea follyensis. Long dimen- sion of shell, 20 mm. Half accessory boring organ spread to about 2 mm. 255 INHIBITION OF SHELL PENETRATION BY UROSALPINX т ++++ ZI F ++++ Il т ++++ OI т +++++ 6 a +++++ 8 0 = L ++ ++++ 9 ++ ++++ с + ++ р ++++ +++ 8 ++++ +++ 7 ++++ +++ | W100 19JEMPIS N£00'0 19JEMB9S W000 JOVLMLIS WS000'0 19]PMBOS OAV ‘ON SUOHNIOS XOUIBI( ит pue [043402 19JBMBIS ur SOGY JPY Aq Buryoja JO ээл8эр pur хоше JO иоцезиэриоо) ‘sIY [5 10} эт]елэ4шэ} WOO! ye [Joys UO poyeqnoul uy) ‘шит ОТ 10} UOTNIOS XOUIBI( ur pod элэм SOGY JPY [в}иэцилэах ‘++ +++ d99p Алэл ‘+ +++ 4ээр ‘+++ эзвлэрош ‘+ + 3431 ‘+ 1481] Алэл “F 99.1 ‘0 9UOU :SOGY J[ey Aq Buryoja Jo asuey “SOU V Fey pastoxa Aq |Jays paystpod Jo 3uryoja uo чоци[оз хошес( JO 99 YA A'IAVL 256 CARRIKER AND CHAUNCEY FIG. 6. Pattern of dissolution of polished shell of Spisula solidissima produced by half an excised accessory bor- ing organ of Urosalpinx cinerea follyensis. Darkest areas represent deepest etching. Maximum dimension of etching, 3 mm. Light micrograph. 2nd day in the highest concentration of Diamox suggests that at least the higher concentrations may have caused snails to abandon oysters and their boreholes. This may have been responsible for the inverse trend in the number of complete to incom- plete boreholes associated with increasing concentrations of Diamox. Nothing, however, is known of the effect of Diamox on the overall physiology of snails. If Diamox had inhibited hole bor- ing by seriously affecting the snails, they might not have bored at all in concen- trations of 5x10-3M and above—which was not the case. An explanation for the inverse trend in the number of completed boreholes is suggested by the results of the experiments with the pure secretion and the excised ABOs where it was shown that the secre- tion from normally functioning ABOs as well as excised ABOs contained carbonic anhydrase and etched shell. Diamox in- hibited carbonic anhydrase activity in the released secretion, and also inhibited etching of polished shell by excised half ABOs even though a purified solution of bovine erythrocyte carbonic anhydrase itself did not affect the shell. It has been reported that shell penetra- tion by Urosalpinx cinerea consists of rasp- ing on the chemically weakened shell at the bottom of the incomplete borehole, followed by passage of the middle portion of the propodium across the bottom of the hole and insertion of the ABO for further chemical dissolution (Carriker € Van Zandt, 1972). During rasping, seawater passes around the proboscis and enters the borehole. The propodium, however, presses the seawater out of the hole prior to insertion of the ABO. The effectiveness of the propodium appears to vary among snails and some seawater may remain in the incomplete borehole. Any residual Diamox solution in the hole could inhibit the shell dissolving properties of the released secretion and/or be absorbed into the ABO to inhibit reactivity of carbonic anhydrase in the secretory epithelium. In either case, the result would be a decelera- tion of shell penetration, the rate of boring decreasing with the extent of exclusion of seawater-Diamox by the propodium, and with increasing concentrations of Diamox. Thus behavioral elimination of seawater from the borehole by the propodium might be responsible, at least in part, for the decrease in the number of complete boreholes and the increase in the number of incomplete holes, as well as the varia- tion in the time of completion of holes in a FIG. 7. Scanning electron micrographs of the pattern of dissolution of the surface of polished shell of Spisula solidissima etched by the secretion of half an accessory boring organ of Urosalpinx cinerea follyensis. Shell sur- face was coated with gold in vacuum prior to examination in the scanning electron microscope. 10,000X. Top. Normal polished surface of the shell. The diagonal scratch line was cut by grit on the wet silicon carbide paper during polishing of the surface. The minute nodular structures are part of the morphology of the shell. INHIBITION OF SHELL PENETRATION BY UROSALPINX 257 , ь ® are WERT Las > > a or y AS EWR hat na Middle. Moderately etched surface. The secretion dissolved the outside of most of the nodules bringing them into strong relief, and more deeply etched clusters of them leaving deep interstices. The slightly darker central portion of the micrograph represents minimal dissolution. Bottom. Example of the most deeply etched shell surface. The nodular units are still distinctive, irregular clusters of them exaggerated by deep dissolution resulting in a complex spongelike appearance. 258 CARRIKER AND CHAUNCEY given concentration of Diamox seen with increasing concentrations of Diamox. The presence of carbonic anhydrase in bivalve mantles has been demonstrated previously (Maetz, 1946; Freeman & Wilbur, 1948; Stolkowski, 1951). Wilbur & Jodrey (1955) indicated that Diamox in- terferes with calcium translocation in the oyster. In studies of the electric potential in clam mantle, Istin & Kirschner (1968) presented a model equation which incor- porates observed potential differences and calcium movement across membranes. They indicated that when the СО? tension is increased and the pH is thus decreased, the concentration of ionized calcium is in- creased. These authors noted that the in- crease in transmantle potential differences associated with rising concentrations of СО? was lowered by the addition of Diamox. Since carbonic anhydrase is necessary for the hydration of COz, they believe that this enzyme plays an impor- tant role in transmembrane calcium flux. In view of the presence of enzymes in- volved in aerobic metabolism in the ABO (Person et al., 1967), it is possible that metabolic COz production by this gland may regulate its ability ultimately to solubilize calcareous substrates. Some controversy still exists regarding the use of the inhibitory action of low con- centrations of Diamox (1x10~>M) in histo- chemical techniques for confirmation of the presence of carbonic anhydrase (Muther. 1972). However, recent studies dealing with carbonic anhydrase, the sul- fonamides, and calcium flux have in- dicated that 1x10-5M acetozolamide and 1x10-$M methazolamide will inhibit para- thyroid hormone-induced resorption of bone in organ culture (Minkin & Jennings, 1972). Studies of this nature thus tend to confirm the validity of the histochemical localization of carbonic anhydrase and provide an in vitro mammalian counter- part to our findings in the marine environ- ment. The importance of carbonic anhydrase in controlling the calcium con- tent of body fluids and tissues continues to be investigated (Chauncey & Weiss, 1958; Kenny, 1972; Nielsen & Frieden, 1972). It has been demonstrated (Dugal, 1939) that aerobic conditions are requisite for the deposition of shell calcium by mantle. We have observed that Urosalpinx cinerea is capable of active penetration of shell only under aerobic conditions. If we hypothesize that the ABO epithelium acts by producing a secretion which contains water, carbonic anhydrase, and CO», this secretion would be acidic and have the capacity to solubilize calcium carbonate. That the secretion is acidic has already been demonstrated (Carriker et al., 1967). However, Pigman, Feagin & Walker (1970) have indicated that the bicarbonate-carbonate system, and specifically bicarbonate ions, can be re- sponsible for decalcification even at pH values above neutrality. This might ex- plain the ability of excised ABOs to etch polished shell at alkaline pH values (Carriker et al., 1963, 1967). CONCLUSIONS The present study is part of a continuing effort to describe the mechanism of shell penetration by boring gastropods and other shell penetrating organisms, and the role of this mechanism in the behavioral ecology of these species. By histochemical techniques we found high carbonic anhydrase reactivity in the ABO of Urosalpinx cinerea. Differential ultra- centrifugation of an homogenate of excis- ed ABOs indicated that the major portion of the carbonic anhydrase was in soluble form. We previously observed that an acetone-insoluble cation-binding granular material was present in the ABO microvilli which may function to chelate the calcium of the shell into a water-soluble complex for rapid removal. This hypothesis was strengthened by our observation in the ABO of microbodies which contain soluble calcium (Smarsh et al., 1969). Our observations that hole boring decreased in increasing concentrations of Diamox are corroborated by Chétail and associates in the French muricid snail Thais lapillus. Chetail & Binot (1967) and Chetail & Fournié (1969) found carbonic anhydrase in both active and inactive INHIBITION OF SHELL PENETRATION BY UROSALPINX 259 ABOs of this snail, and later demonstrated an increase of calcium ions in the ABO during active shell penetration (Chétail & Fournié, 1970). They demonstrated, by a manometric method, using ABO homo- genates of T. lapillus, that although car- bonic anhydrase is always present in both boring and inactive glands, it is present in variable amounts. Tests of fluid outside of whole ABOs by the same method in a sub- strate made isotonic with mannitol were negative, which was taken to indicate that carbonic anhydrase was found only intra- cellularly. In experiments with live snails held in closed seawater aquaria, in con- centrations of Diamox ranging from 1x- 10-3М to 7x10°3M, for 4 weeks, they found that at low concentrations the num- ber of complete holes drilled decreased or disappeared while the number of in- complete holes increased. At 5x10~3M and above, full inhibition of boring took place (Rossenberg, Chétail & Fournié, 1968; Chétail & Fournié, 1969). In another ex- periment, where they bubbled a mixture of 5% СО? and 95% Oz through the sea- water the rate of boring increased two fold. This reinforced their conclusion that car- bonic anhydrase in the ABO of T. lapillus “is responsible for dissolution of СаСОз” (Chétail & Fournié, 1969). We demonstrated greater reactivity in both active and inactive ABOs of Urosalpinx cinerea than in adjacent secre- tory tissues (Smarsh et al., 1969), and in this paper we report the presence of car- bonic anhydrase in the released secretion of the ABO and inhibition by Diamox of shell dissolution by live snails and excised ABOs. These results support our earlier suggestion of a vital role of this enzyme in shell dissolution during boring by this snail and provide support for Chétail et al.’s (1969) statement of a similar role for the enzyme in shell boring Thais lapillus. It appears unlikely, however, that the car- bonic anhydrase functions as a direct demineralizing agent. Carbonic anhydrase has been im- plicated in dissolution of shell by 2 different genera of boring gastropods and by a species of burrowing barnacle (Tur- quier, 1968). Whether carbonic anhydrase is involved in the dissolution of calcareous substrata by the many other calcibio- cavites already known (Carriker & Smith, 1969) remains to be determined. Because of its ravage, especially of young oysters, Urosalpinx cinerea has been of concern to oyster farmers in the United States for at least the last 100 years. These snails apparently became а serious problem concurrently with the develop- ment of widespread transplantation and cultivation of oysters (Carriker, 1955). Plantings in other parts of the world are plagued by other species. U. cinerea has so far resisted efforts to control it. Recogni- tion of the importance of carbonic anhydrase and the oxidative enzymes in shell boring may lead to methods of con- trolling this and other predatory muricid gastropods. ACKNOWLEDGEMENTS Anne Smarsh conducted the histo- chemical phase of the study and tested the ABO secretion blots for CA. Dirk Van Zandt assisted in the overall study, and took the light photomicrographs. The scanning electron microscopy was done in collaboration with Dr. Virginia Peters. The live Urosalpinx cinerea follyensis were supplied by Michael Castagna. We are grateful to these persons for their generous belp, and to Dr. Philip Person for sug- gestions and review of the manuscript. The research was supported by Public Health Service Research Grant DE 01870 from the National Institute of Dental Re- search and by the Veterans Administra- tion. LITERATURE CITED CARRIKER, M. R., 1955, Critical review of biology and control of oyster drills Urosalpinx and Eupleura. Fish & Wildlife Service, Special Sci. Rept.: Fish., No. 148, 150 p. CARRIKER, M. R., 1967, Research and research training on the biology of the whole organism. Systematics-Ecology Program, Fifth Annual Report on Progress, Marine Biological Laboratory, Woods Hole, Mass., p 46-49. 260 CARRIKER AND CHAUNCEY CARRIKER, M. R., 1969, Excavation of boreholes by the gastropod, Urosalpinx: an analysis by light and scanning electron microscopy. Amer. Zool., 9: 917-933. CARRIKER, М. R., SCOTT, D. R. & MARTIN, G. N., 1963, Demineralization mechanisms of boring gastropods, p 55-89, in Mechanisms of Hard Tissue Destruction, В. Е. Sognnaes, Ed., Publ. No. 75, Amer. Assoc. Adv. Sci., Washington, D.C., 764 p. CARRIKER, M. R. & VAN ZANDT, D., 1964, Use of polished mollusk shell for testing demineralization activity of accessory boring organ of muricid boring gastropods. Biol. Bull., 127: 365. CARRIKER, М. R., CHARLTON, С. € VAN ZANDT, D., 1967, Gastropod Urosalpinx: pH of accessory boring organ while boring. Science. 158: 920-922. CARRIKER, M. R., PERSON, P., SMARSH, Al, “LIPSON, S: & “GCHAUNCEY, HE: IE, 1968, Role of carbonic anhydrase in decalcification by Urosalpinx cinerea follyen- sis (oyster drill). Internat. Assoc. Dental Res. Program & Abstracts, 1968, Abstr. No. 604, p 188. CARRIKER, M. R. & SMITH, E. H., 1969, Comparative calcibiocavitology: summary and conclusions. Amer. Zool., 9: 1011-1020. CARRIKER, M. R. & VAN ZANDT, D., 1972, Predatory behavior of a shell-boring muricid gastropod, p 157-244, in Behavior of Marine Animals: Current Perspectives in Research, Vol. 1: Invertebrates, H. E. Winn & B. L. Olla, Ed., Plenum Press, New York, 244 p. CHAUNCEY, H. H. & WEISS, P. A., 1958, Composition of human saliva. Parotid gland secretion: flow rate, pH and inorganic com- position after oral administration of a car- bonic anhydrase inhibitor. Arch. Int. Phar- macodyn., 113: 377-383. CHETAIL, M. & BINOT, D., 1967, Mise en evidence et rôle de l anhydrase carbonique dans Vorgane accessoire de perforation de Purpura lapillus L. (Gastéropode, Pro- sobranche). C. r. Acad. Sci. Paris, 264: 946- 948. CHETAIL, M. € FOURNIE, J., 1969, Shell- boring mechanism of the gastropod Purpura (Thais) lapillus: a physiological demonstra- tion of the role of carbonic anhydrase in the dissolution of CaCOs. Amer. Zool., 9: 983- 990. CHETALL,. MM: € FOURNTE, J. 1970, Mécanisme de pertoration chez Thais lapillus L. (Gastéropode Prosobranche, Muricidé): mise en évidence d'une entrée d'ions calcium durant l'activité de l'organe de perforation. С. =. Acad. Sci! Paris, 971: 118-121. DUGAL, L. Р., 1939, The use of the calcareous shell to buffer the product of anaerobic glycolysis in Venus mercenaria. J. cell. comp. Physiol., 13: 235-251. FREEMAN, J. А. & WILBUR, К. M., 1948, Carbonic anhydrase in molluses. Biol. Bull., 94: 55-59. HAUSLER, С., 1958, Zur Technik und Spezifität des histochemischen Carbo- anhydrasenachweiss im Modellversuch und in Gewebsschnitten von Rattennieren. Histochemie, 1: 29-47. ISTIN, M. & KIRSCHNER, L. B., 1968, On the origin of the bioelectrical potential generated by the freshwater clam mantle. J. gen. Physiol., 51: 478-495. KENNY, A. D., 1972, Effect of dietary acetazolamide on plasma electrolytes, bone mass, and renal mineral contents in rats. Proc. Soc. exptl, Biol. Med., 140: 135-139. MAETZ, J., 1946, L'Activité anhydrasique de quelques tissus d’invertebres. Bull. Inst. Oceanogr., 899: 1-20. MINKIN, C. € JENNINGS, J. M., 1972, Car- bonic anhydrase and bone remodeling: sul- fonamide inhibition of bone resorption in organ culture. Science, 176: 1031-1033. MUTHER, T. F., 1972, A critical evaluation of the histochemical methods for carbonic anhydrase. J. Histochem. Cytochem., 20: 319-330. MUTVEI, H., 1969, On the micro- and ul- trastructure of the conchiolin in the nacreous layer of some recent and fossil molluscs. Stockholm Contr. Geol., 20: 1-17. MUTVEI, H., 1970, Ultrastructure of the mineral and organic components of molluscan nacreous layers. Biomineraliza- tion Res. Rept., 2: 48-72. NIELSEN, S. A. & FRIEDEN, E., 1972, Car- bonic anhydrase activity in molluses. Comp. Biochem. Physiol., 41B: 461-468. NYLEN, М. U., РВОУЕМАА , DE CARRIKER, М. R., 1969, Fine structure of the accessory boring organ of the gastropod, Urosalpinx. Amer. Zool., 9: 935-965. PIGMAN, W., FEAGIN, Е. & WALKER, A., 1970, The effect of carbonic acid on dental enamel. Internat. Assoc. Dental Res. Program & Abstracts, 1970, Abstr. No. 449, р 161. PERSON, Р., SMARSH, A., LIPSON, 5. J. & CARRIKER, M. R., 1967, Enzymes of the accessory boring organ of the muricid gas- tropod Urosalpinx cinerea follyensis. 1. INHIBITION OF SHELL PENETRATION BY UROSALPINX 261 Aerobic and related oxidative systems. Biol. Bull., 133: 401-410. ROSENBERG, А, CHETAIE, М... & FOURNIE, J., 1968, Intervention de l'anhydrase carbonique dans le mécanisme de perforation des valves de Lamellibranches par Purpura (Thais) lapillus L. (Gastéropode Prosobranche Muricidae). Cr. Acad. Sci. Paris, 266: 944-947. ОМАНА, (CEPATUINIC E Ya erie She CARRIKER; М: В; & PERSON, P.;' 1969; Carbonic anhydrase in the accessory boring organ of the gastropod, Urosalpinx. Amer. Zool., 9: 967-982. STOLKOWSKI, J., 1951, Essai sur le déter- minisme des formes minéralogiques du calcaire chez les étre vivants (calcaires co- quilliers). Ann. Inst. Oceanogr., 26: 1-113. TAYLOR} 0. (KENNEDY, №. Jo& HALL; A., 1969, The shell structure and mineralogy of the Bivalvia. Nuculacea-Trigonacea. Bull. British Mus. (Nat. Hist.), Zool. Suppl., 3: 1- 125. TRAVIS, D. F. & GONSALVES, M., 1969, Comparative ultrastructure and organization of the prismatic region of two bivalves and its possible relation to the chemical mechanism in boring. Amer. Zool., 9: 635-661. TURQUIER, Y., 1968, Recherches sur la biologie des Cirripédes Acrothoraciques. 1. L’ anhydrase carbonique et le méchanisme de perforation du substrat par Trypetesa nassarioides Turquier. Arch. Zool. exp. gen., 109: 113-122. WILBUR, K. M. & JODREY, L. H., 1955, The inhibition of shell formation by carbonic anhydrase inhibitors. Biol. Bull., 108: 359- 365. ZUSAMMENFASSUNG DIE AUSWIRKUNG EINER CARBOANHYDRASE-HEMMUNG AUF DIE SCHALENBOHRFAHIGKEIT DER MURICIDE UROSALPINX CINEREA M. R. Carriker und H. H. Chauncey Uber die Auswirkung einer Reihe von Konzentrationen von Diamox (2-Acetylamin- 1,3,4-thiadiazol-5-sulfonamid), eines spezifischen Hemmers des Enzyms Car- boanhydrase (CA), auf die Bohrleistung der bohrenden Muricide Urosalpinx cinerea follyensis an der Schale der Auster Crassostrea virginica wurde eine Untersuchung ausgeführt. 45 zu Versuchsbeginn bohrende Schnecken bohrten und frassen an Austern weiter, wenn sie in Diamox-Lósungen von Konzentrationen zwischen 5x107*M und 1х10-2М verbracht wurden. 45 zu Versuchsbeginn nicht bohrende Schnecken erkannten die Beutetiere in demselben Bereich von Konzentrationen, krochen auf sie hinauf und bohrten sie an. Die Schnecken waren in der Lage, in Konzentrationen bis hinauf zu 5x10°3M Löcher fertigzubohren und Austern anzufressen. Während des sechstägigen Experiments nahm die Gesamtzahl fertiger Bohrlöcher mit steigender Diamox-Konzentration um 2/3 ab, während die Gesamtzahl nicht vol- lendeter Löcher sich verdoppelte. Alle 90 Schnecken überlebten die 6 Tage sowie auch einen weiteren Monat in normalem fliessenden Meerwasser unter emsigem Bohren und Fressen. Sekret, das von tätigen accessorischen Bohrorganen (ABO) lebender Schnecken auf einem Schalenmodell abgetupft wurde, wie auch solches, das aus dem ABO-Porus austrat, reagierte in histochemischen Tests positiv auf CA. Diamox-Behandlung in- hibierte die CA in beiden Sekreten. Aus aktiv bohrenden Schnecken excisierte Kontrollhäften von ABOs ätzten polierte Schalen an, wogegen auf die halbierten Versuchs-ABOs einwirkende steigende Diamox- Konzentrationen die Atzwirkung zunehmend verringerten. In den Konzentrationen von 5х10-3М und 1x10°2M war die Ätzfähigkeit fast völlig inhibiert. Eine Suspension von reiner Schafserythrocyten-CA in Meerwasser führte nicht zur Schalenanätzung. Diese Versuche zeigen an, dass CA eine wesentliche Rolle beim Schalenauflösen während der Bohrtätigkeit dieser Schneckenart spielt; sie bestätigen auf der anderen Seite nicht ihre Funktion als direktes demineralisierendes Agens. C.M.-B. 262 CARRIKER AND CHAUNCEY RESUME EFFET DE L INHIBITION DE L'ANHYDRASE CARBONIQUE SUR LA PERFORATION DE COQUILLE PAR LE MUREX UROSALPINX CINEREA M. R. Carriker et H. H. Chauncey Une étude a été faite sur une série de concentrations de Diamox (2-acétylamine-1,3,4- thiadiazole-5-sulfonamide), qui est un inhibiteur de Гепхуте anhydrase carbonique (AC), sur la perforation de la coquille de l'huítre Crassostrea virginica par le bigorneau perceur Urosalpinx cinerea follyensis. Cinquante cing individus qui étaient initialement en train de perforer ont continué а perforer et а se nourrir sur des huitres dans des solu- tions de Diamox se situant а des concentrations comprises entre 5x10~4M et 1x10°?M. Quarante cing individus qui ne perforaient pas initialement, sont montés sur les huitres et ont commencé а percer aux concentrations précédentes. Les murex se sont montrés capables de terminer leur trou de perforation et de se nourrir jusqu à des concentrations de 5х10-3М. Le nombre total de perforations completes décroit des 2/3 tandis que le nombre total de perforations incomplétes double presque а mesure que Гоп augmente les concentra- tions de Diamox, pendant les 6 jours d’experimentation. Tous les 90 murex ont survécu les 6 jours, ainsi d'ailleurs que le mois suivant ou ils étaient dans une eau de mer courante normale ou ils pouvaient perforer et se nourrir activement. Les extraits de sécrétion récoltés а partir d'organes accessoires de perforation (O.A.P.) en activité, sur des individus vivants sur un modele de valve, ainsi que les produits de sécrétion libérés par ГО.А.Р. au niveau du pore de ГО.А.Р., se sont montrés positifs pour ГАС lorsqu'ils ont été testés par des techniques histochimiques. Le traitement par Diamox a inhibé ГАС dans les 2 cas. Des moitiés d'O.A.P. utilisées comme témoins, excisés sur les murex en activité de per- foration, ont érodé des coquilles polies, tandis que des concentrations croissantes de Diamox appliquées aux moitiés expérimentales de ces O.A.P., ont progressivement réduit leur capacité d’eroder. Dans des solutions de 5х10-3М et 1х10-?М, I abrasion était presqu entiérement inhibée. Une suspension en eau de mer d'AC pure d érythrocyte de bovin п’а provoqué aucune abrasion de coquille. Ces expériences indiquent que ГАС joue un róle vital dans la dissolution de la coquille pendant la perforation chez cette espéce, mais ne confirment pas ses fonctions comme agent direct de déminéralisation. А. Lb. RESUMEN EFECTO INHIBITORIO SOBRE LA ANHIDRASA CARBONICA EN LA PERFORACION DE OSTRAS POR EL GASTROPODO MURICIDO UROSALPINX CINEREA M. R. Carriker y H. H. Chauncey Se estudiaron los efectos de una serie de concentraciones de Diamox (2-acetilamina- 1,3.4-thiadiazol-5-sulfonamida), como un inhibidor especifico de la enzima carbónica anhidrasa (CA), sobre la penetración en la concha de la ostra Crassostrea virginica por el gastrópodo muricido perforador Urosalpinx cinerea follyensis. 45 caracoles que ya habian iniciado la perforación, continuaron la acción y se nutrieron en las ostras, en soluciones de Diamox de 5х10-4М a 1x10-2M. Otros 45 que no habian iniciado la perforación la comenzaron en las mismas soluciones. Los caracoles fueron capaces de completar la horadación de las ostras en concentraciones de 5x1072M. El número total de orificios completos en las ostras decreció dos tercios, mientras que el número de los incompletos se duplicó en concentraciones mayores de Diamox durante INHIBITION OF SHELL PENETRATION BY UROSALPINX los 6 dias de experimentación. Los 90 caracoles sobrevivieron los 6 dias, y aún hasta un mes más en agua de mar corriente normal, en la cual perforaron y se alimentaron ac- tivamente. Residuos de secreción tomados de los órganos perforadores activos accesorios (ABO) en caracoles vivos sobre una valva modelo, así como secreciones emitidas por el ABO en el poro ABO, fueron positivas para CA cuando se probaron con técnicas histoquímicas. Tratamiento con Diamox produjo inhibición de CA en ambos. Mitades controladas de ABO, sacadas de caracoles perforadores activos, mordieron conchas pulidas, mientras el aumento de concentraciones de Diamox, aplicadas a la mitad experimental de estos ABO, redujeron esa acción proporcionalmente. En las soluciones 5х10-3М y 1x10°2M el mordiente fué, casi totalmente, inhibido. Una suspen- sión de eritrocitos CA bovinos puros, pero en agua de mar no produjeron efecto mor- diente en las conchas. Estos experimentos indican que CA desempena un rol vital en la acción disolvente durante la perforación de la concha por esta especie de caracol, pero no confirma su fun- ción como un agente desmineralizador directo. LIE 263 г: У | AA | 4 р ‚ bad PICAS PR лаки СО оля! 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Y - ! | Neal y lo | “au | dde 13 a e: OA ne de en ne o Ч ША Re Nr Do Vies). o г. eu I» EL Lee. Does À a A Fer эми Bun и не A MALACOLOGIA, 1973, 12(2): 265-281 SOME ASPECTS OF THE BIOLOGY AND FUNCTIONAL MORPHOLOGY OF THE ORGANS OF FEEDING AND DIGESTION OF LIMNOPERNA FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA) Brian Morton Department of Zoology, The University of Hong Kong ABSTRACT Limnoperna fortunei (Dunker) has recently been introduced into the fresh water supp- ly system of Hong Kong. The initial occurrence of the mollusc can be related to the com- mencement of supplies of water to Hong Kong from the East river in China. It is suggested that Limnoperna could emulate the rapid expansion of range experienced by Dreissena polymorpha in Europe and Corbicula manillensis in N. America. For this reason pertinent aspects of the functional morphology and biology of Limnoperna have been investigated. Comparisons have been made with other mytilids, and with Dreissena which Limnoperna superficially resembles. The possibility of a phylogenetic affinity between these 2 animals is discounted; the similarities being due to convergent evolution and the adoption of similar habits. The evolution of the heteromyarian condition in the Mytilacea and Dreissenacea, followed by the subsequent evolution of osmoregulating powers, has enabled Limnoperna and Dreissena to successfully invade the hard surfaces of fresh-water systems. In this habitat there is no competition from the specialised infaunal bivalves characteristically found in fresh waters. The colonisation of this habitat has conflicted in Dreissena, and may possibly conflict in the case of Limnoperna, with the interests of man in the supply of fresh water. INTRODUCTION In recent years the attention of water supply engineers and biologists in Europe and North America has been drawn to the problems of fouling caused by fresh-water bivalve molluscs. In the 19th century and in this century Dreissena polymorpha has expanded its range from an initial restricted area focused on the Caspian Sea to one encom- passing much of the European continent. It has been suggested that much of the ap- parent success of this animal is attributable to the construction of waterways, thereby facilitating the artificial expansion of range. This is certainly the reason for the expansion of range that Dreissena under- took in Great Britain in the 19th century (Kerney & Morton, 1970). Dreissena also possesses a byssus and is thus adapted to the colonisation of solid surfaces (such as are found in the pipes and conduits of water supply systems) hitherto inaccessible to the typically infaunal bivalve con- stituents of fresh-water faunas (Morton, 1969а), e.g., the Unionacea and Cor- biculacea. This has led to a situation in which many European countries, in- cluding Great Britain, spend time, money and effort in controlling Dreissena (Mor- ton, 1969c). Corbicula manillensis has recently been introduced into North American waterways and has caused similar problems of fouling (Sinclair, 1964). First observed in 1938 in Washington this species has since expanded its range to en- compass all of the major North American river basins (Sinclair, 197la, b). The fouling problems caused by Corbicula are somewhat different from those caused by Dreissena in that Corbicula is essentially an infaunal species and thus, although it does clog pipes and condensers, also causes additional problems when occurring in sands dredged for ultimate use in the manufacture of concrete. Like Dreissena the rapid expansion of range experienced by Corbicula may be attributable to man’s (265) 266 В. MORTON development of artificial waterways for water supply purposes. In Asia, the original home of Corbicula manillensis, there are few instances of molluscs causing problems with regard to water supply, largely one would suspect because in many cases water supply systems themselves are not as extensive or as refined as they are in Europe and North America. The mytilid Limnoperna fortunei (Dunker) occurs in the rivers of Asia but has aroused little interest. There is a dearth of information on this animal, most records being found in obscure and an- cient journals. Limnoperna is of interest, however, from a number of viewpoints. In the first instance it is, for a mytilid, living in a unique habitat. Secondly, Limnoperna possesses a striking superficial similarity to Dreissena and, in view of the recent sub- mission by Purchon & Brown (1969) of a common ancestry between the Mytilacea and Dreissenacea, it is considered that Limnoperna may test the validity of this concept. Finally, and most importantly, Limnoperna was, prior to 1968 unknown in Hong Kong. Its appearance in part of the water supply complex of Hong Kong may be a re-enactment of the pattern of colonisation typical of Corbicula and Dreissena (i.e., via man-made systems). Thus Limnoperna might Бе potentially detrimental to water supply in Hong Kong in particular and Asia in general. There is thus a need to set any further studies on Limnoperna upon а firm footing. This study was undertaken to fulfill, in part, this need. MATERIALS AND METHODS A large number of specimens of Lim- noperna fortunei were obtained from a channel used for conveying water to Tai Lam Chung reservoir, Hong Kong. Further samples were subsequently ob- tained from Plover Cove reservoir. Material to be sectioned was fixed in alcoholic Bouin Duboscq and ultimately stained in either Heidenhain s haematoxylin, Masson s trichrome ог Mallory 's triple stain. Where necessary, decalcification of the shell was achieved by immersion, subsequent to fixation and prior to sectioning, in R.D.O.! rapid bone decalcifier for a period of 4 hours. The ciliary currents elucidated in this work were demonstrated by the application of either suspended carmine or milk. NOMENCLATURE Volsella fortunei (Dunker 1857) is in all probability synonymous with Modiola lacustris (von Martens 1875) and Modiola fortunei (Reeve 1858). It is probably also synonymous. with Dreissena siamensis (Morelet 1866). The generic name Lim- noperna Rochebrune 1888 was erected to distinguish this apparently monotypic genus from the other mytilids. The elucidation of these differences is one of the aims of this paper. DISTRIBUTION AND HABITS Prior to 1968 Limnoperna was not found in Hong Kong. Its subsequent discovery in 1968 in certain major tunnels, culverts and pipelines of Hong Kong's water supply system would seem to suggest accidental and artificial introduction. The ap- proximate timing of its appearance coin- cides with the supply to Hong Kong in 1967 of water derived from the East river in China. Limnoperna has been reported from the Pearl river estuary (Miller € McClure, 1931), of which the Shum Chun river of Hong Kong is a component, and it is thus possible, though unlikely, that in- troduction was via this path. The sudden occurrence, however, in pipelines of the water supply system strongly suggests that the former possibility was the primary (and maintained) source of infection. No information is available to indicate if this animal is a nuisance in China, although Limnoperna has been reported as ос- curring in Tung-Ting lake, which connects up with the Yangtsekiang river, in Hunan Province (Tchang, Li € Liu, 1965). Whatever its origin, however, Lim- ‘Supplier; Du Page Kinetic Laboratories, Inc., Р.О. Box 416, Downers Grove, Illinois 60515, U.S.A. BIOLOGY AND FEEDING OF LIMNOPERNA noperna is now firmly established in the rapidly expanding and _ increasingly sophisticated water supply system of Hong Kong. The pattern of colonisation reflects that of Corbicula and Dreissena, but of course on a much smaller scale. It is now a significant and established member of the epifauna of the Plover Cove reservoir and its associated pipelines. Limnoperna is very like Dreissena (Morton, 1969c) in that when living in relatively slow flowing waters it characteristically occurs in clumps or “nodules” of individuals living bound upon the dead shells of their predecessors by a very stout byssus. In very fast flowing waters, such as are found in pipelines or culverts, Limnoperna inhabits crevices and pits, although from these foci succeeding generations can spread out to cover more and more of the exposed sur- face of the pipe. Its byssus makes it extremely difficult to dislodge in such situations. ADEE TATIONS USED IN, THE FIGURES is Auricle AA Anterior adductor muscle or scar ABR Anterior byssal retractor muscle or scar B B type sorting area BG Byssus gland BS Branchial septum BY Byssus CS Crystalline style DD Digestive diverticula DDD(1)-(5) Ducts of the digestive diverticula DH Dorsal hood DHT Dorsal hood tract DS Dorsal septum ES Exhalant siphon Е Foot ЕС Food sorting caecum GS Gastric shield ID Inner demibranch IG Intestinal groove IP Inflected periostracum IS Inhalant siphon E Ligament BP Left pouch LT Left duct tract M Mouth 267 MG Mid gut MM Mantle margin MT Minor typhlosole O Oesophagus OD Outer demibranch OS Opening of food sorting caecum into stomach OV Ovary В Pericardium PA Posterior adductor muscle or scar PBR(1),(2) Posterior byssal retractors muscle or scar PL Pallial line POG Proximal oral groove PPR Posterior pedal retractor muscle or scar R Rectum £ RP Right labial palp RT Right duct tract (SA3) SA2 Sorting area SS Style sac E Major typhlosole RE Tongue of major typhlosole U Umbo V Ventricle VM Visceral mass ANATOMY The shell and ligament The equivalve, heteromyarian shell of Limnoperna fortunei is superficially very similar to that of Xenostrobus securis (Wilson, 1967) (Fig. 1, A & B). In par- ticular, in both species the shell is dark brown above the umbonal keel and a paler yellow-brown below. This is caused by the nacre of the interior of the shell being pur- ple above and white below the keel. The presence of a nacreous layer in Limnoper- na displaces this genus from all contact with the Dreissenacea (Taylor, Kennedy & Hall, 1972). The outer periostracal layer of the shell is smooth and shiny and where it curls in- wards at the shell margin is thick. The um- bones are very nearly terminal and the dorsal ligamental margin is straight or, at most, only slightly curved. The ventral margin of the shell is the most variable feature and in different specimens varied between the 2 extremes of being either straight or distinctly arcuate. There are no hinge teeth and no byssal notch. 268 B. MORTON FIG. 1. Limnoperna fortunei. Views of the exterior (A) of the left shell valve and interior (B) of the right shell valve. (For abbreviations see p 267). The overall dimensions of the shell are regular for the population sampled in this study as can be seen from Fig. 2 and by the ratio of width: height: length which is: 1: 1.18 + 0.18: 2.60 + 0.50. The ratios of shell width : length and shell height length have been calculated as being 0.38 + 0.06 and 0.45 + 0.06 respectively. The opisthodetic ligament of Limnoper- na consists of 2 layers with staining reac- tions similar to those of Mytilus edulis (Trueman, 1950; Beedham, 1958). The outer layer stains red and the inner layer bright blue with both Mallory's triple stain and Masson's trichrome. Other mytilids e.g., Modiolus, Lithophaga (Yonge, 1955), Septifer (Yonge & Campbell, 1968) and Fungiacava (Goreau, Goreau, Soot-Ryen & Yonge, 1969) possess a ligament with a similar structure. In all these forms, and in Limnoperna, the periostracum extends over the ligament, thereby adding another layer. Yonge & Campbell (1968) regard this ligamental structure as being typical of the Mytilacea. The results of this work on Limnoperna agree with this premise. The ligament of Dreissena polymorpha has a totally different structure (Yonge & Campbell, 1968); it is an uniquely complex opisthodetic ligament. SHELL LENGTH (mm) 2 6 10 14 SHELL WIDTH (mm) FIG. 2. Limnoperna fortunei. Width : length ratios of a large sample from Hong Kong. The mantle Mantle fusion occurs dorsally above the exhalant siphon and between the exhalant siphon and inhalant aperture. Mantle fu- sion is of the inner mantle folds only and thus of type A (Yonge, 1957). The periostracum that is secreted by the epithelia delimiting the periostracal groove is composed of 3 layers. The outer layer is thin (54), and stains very slightly BIOLOGY AND FEEDING OF LIMNOPERNA 269 grey with Heidenhain's haematoxylin but not at all with Mallory s or Masson s stains. The middle layer is 20-254 thick at its greatest depth and is composed of a yellow substance that is unaffected by the routine stains used in this study. This layer does not, as does its counterpart in Mytilus (Beedham, 1958), possess vacuoles. An in- ner laminated layer ultimately achieves a thickness of between 25 and 35 и and when first secreted stains red with both Mallory's and Masson’s stains. Toward the margin of the valve the outer laminations of this layer stain blue. Ultimately all the laminae stain blue. The structure of the periostracum and the epithelia that secrete the component zones bear a close similari- ty to those possessed by Mytilus (Beedham, 1958) but are very different from the Eulamellibranchia in general and Dreissena polymorpha in particular (Mor- ton, 1969a). The mantle distal to the man- tle margin contains, as in other mytilids, much of the gonadial tissue of the animal. This is not so in Dreissena. The siphons The exhalant siphon (Fig. 3, ES) of Lim- noperna is formed by fusion between the inner mantle folds only, this being type A (ii) (Yonge, 1957). The inhalant aperture is not separated from the pedal/byssal aper- ture by fusion of the opposite mantle lobes but is separated functionally by their ap- position. It can thus be referred to as a siphon, even though this is not strictly cor- rect. Such a situation is typical of the Mytilacea, e.g., Mytilus (White, 1937), Lithophaga (Yonge, 1955), Adula (=Botula) (Yonge, 1955; Fankboner, 1971) and Xenostrobus (Wilson, 1967). Neither the inhalant siphon nor the exhalant siphon bear tentacles or papillae (Fig. 3, A). Externally each mantle lobe is patterned with a brown stripe; these fuse dorsally to the exhalant siphon to form a single stripe. А similar brown stripe patterns the internal surfaces of the mantle lobes forming the inhalant siphon, and there is a dorsal median stripe on the in- halant siphon at the point of fusion of the mantle lobes forming the exhalant siphon (Pig. oo Ay): A branchial septum (Fig. 4, BS) con- nects the ctenidia (ID, OD) to the mantle at the point of fusion of the mantle lobes separating the exhalant from the inhalant siphon. This septum effectively separates posteriorly the infra-branchial from the supra-branchial chamber. When the animal is actively filtering and the siphons are extended, the branchial septum is horizontal, but folds up when the siphons are withdrawn. In Adula (Fankboner, 1971) this septum apparently acts as a valve. The musculature The anterior adductor muscle (Fig. 4, AA) is small and is located on the antero- ventral floor of the shell valves. In this respect Limnoperna is very similar to Xenostrobus (Wilson, 1967) and Mytilus (White, 1937). The anterior byssal retrac- tor muscle (ABR) has its origin on the antero-dorsal roof of the shell like X. securis and X. pulex (Wilson, 1967). The posterior adductor muscle (PA) is large and the posterior byssal retractor muscle (PBR) is divided into 2 component units as in X. inconstans (Wilson, 1967) and M. edulis (White, 1937). There is a small posterior pedal retractor muscle (PPR) that has its origin anterior to the posterior byssal retractors and not posterior as in Dreissena (Yonge € Campbell, 1968). The ciliary currents of the mantle, visceral mass and foot The ciliary currents of the mantle (including the siphons), visceral mass and foot are all rejectory in nature and serve to keep the mantle cavity free of too large or unwanted particles. The ciliary currents of the visceral mass (Fig. 4, VM) and foot (F) pass particles posteriorly to be concentrated at the postero-ventral tip of the visceral mass. From this point they are presumably removed by (a) the ventrallv, or (b) the dorsally, directed ciliary tracts of the ascending lamella of the inner demibranch (ID) to be rejected respectively by the sor- ting mechanism of the ventral ctenidial marginal food groove or the dorsal food groove in the junction of the inner HIG.3: FIG. 4. В. MORTON B C Limnoperna fortunei. A posterior view of the animal showing (A) the patterning on the mantle and siphons and the shape of the shell. The inhalant a am (broken arrows), ех- halant stream (open arrows) and ciliary rejection currents (solid arrows) of an actively filter- ing animal (B) and a disturbed animal (C) are also shown. (For abbreviations see p 267). PBR (1) Limnoperna fortunei. The anatomy and the ciliary cleansing currents of the mantle, foot and visceral mass. The ciliary currents of the ascending lamella of the inner demibranch are also shown. The shell valve, mantle and ctenidium of the right side have been removed. (For ab- breviations see p 267). BIOLOGY AND FEEDING OF LIMNOPERNA 271 demibranch and visceral mass. In both cases (if they are too large) the particles ul- timately pass onto the mantle. Particles falling on to the mantle are passed posteriorly from the region of the mouth and labial palps (RP) to the in- halant siphon (IS). Pseudofaeces are not concentrated at the base of the inhalant siphon to be expelled by the rapid adduc- tion of the shell valves, as in the typical eulamellibranchs possessing a distinct siphon. Instead in Limnoperna the lobes of the inhalant siphon are highly mobile and bear on their inner surfaces strong ciliary tracts which pass the pseudofaeces dorsally towards the exhalant siphon (Fig. 3, В). When actively filtering, with the inhalant lobes fully expanded, water can pass into the mantle cavity. The ciliary currents can take the pseudofaeces towards the exhalant siphon against this stream. Rapid closure of the shell valves forces water out of both siphons, but particularly the exhalant siphon, thereby ejecting the pseudofaeces (and faeces). When the animal is disturbed, the shell valves only FIG. 5. Limnoperna fortunei. The labial palps and ctenidium of the right side showing the various ciliary currents. (For abbreviations see p 267). bo I bo partially open (Fig. 3, С), but open suf- ficiently to allow pseudofaeces to be similarly removed from the mantle cavity via a reduced inhalant aperture. The ctenidia and labial palps The ctenidia comprise 2 sub-equal demibranchs of which the outer demibranch is the longer. The ventral margin of the outer demibranch (Fig. 4, OD) was found to always lie tucked behind the incurving mantle margin (MM) with the associated periostracum (IP). The up- per margins of the ascending lamellae of the outer and inner demibranchs are at- tached to the mantle and the visceral mass respectively by ciliary fusions. The ctenidia are flat, homorhabdic and filibranchiate (eleutherorhabdie). Ctenidial cohesion is maintained by ciliary discs as in other mytilids. Like many other mytilids listed by Fankboner (1971), the outer demibranchs of Limnoperna for- tunei are some 5 or 6 filaments shorter at their anterior ends than the inner demibranchs. A similar arrangement exists in Dreissena (Morton, 1969a) and Petricola (Purchon, 1955). Fankboner (1971) states that “a functional advantage for this anatomical reduction is unclear.” For Limnoperna the advantage of this arrange- ment is clear in that it enables the ventral marginal food grooves of both demibranchs to be in contact with both labial palps thereby greatly increasing the efficiency of particle selection by the palps. In other genera this is apparently not so well developed. The ctenidial-labial palp junction of Limnoperna thus falls into Category I elucidated by Stasek (1963) and is thus typical of the Mytilacea in general. D. polymorpha, on the other hand, has a ctenidial-labial junction that is of Category Ш (Morton, 1969a). The ciliation of the ctenidial surfaces is of type В (1) (Atkins, 1937) (Fig. 5). Accep- tance tracts are situated on the ventral margins of both demibranchs, in the ctenidial axis and in the junctions of the ascending lamella of the inner and outer demibranchs with the visceral mass and mantle respectively. Only those particles arriving on the labial palps inside the ven- В. MORTON tral marginal food groove of the inner demibranchs pass into the proximal oral groove and directly to the mouth. Particles arriving at the anterior end of the ctenidium via (1) the crests of the ventral marginal food grooves of both inner and outer demibranchs, (2) inside the ventral food groove of the outer demibranch and (3) in all 3 dorsal food grooves are sub- jected, before ingestion, to the ciliary selection currents of the labial palps. The abrupt termination of the outer demibranch (Fig. 5), facilitating this un- usually complicated sorting process has not been observed in other bivalves, and is markedly different from that possessed by Dreissena (Morton, 1969a). Particles are probably removed from the ctenidial ter- mini by the unridged portion of the labial palps, the ciliary currents of which subse- quently pass the particles onto the sorting portion of the palps. This function is the attribute of the system of parallel ridges and grooves which pass selected particles of a suitable nature and size over the crests of the ridges toward the proximal oral groove for ultimate ingestion. Too large or unwanted particles are passed laterally toward the opposite free edge of the palp for rejection. Recirculatory currents also exist. Details of the palp ciliation need not be gone into here since they are essentially the same as those described by Fankboner (1971) for Adula and are typical of mytilids in general. The ciliary currents of the lips of the mouth (M) are rejectory in nature passing unwanted material back to the palps for rejection along the prescribed course. The alimentary system The oesophagus passes upwards from the mouth, which lies between the anterior byssal retractor muscles and is closely applied to the anterior adductor muscle. The ciliated oesophagus opens into the stomach which is located under the antero- dorsal margin of the shell and is sur- rounded by the dark digestive diverticula (Fig. 4, DD). From the posterior end of the stomach arises the combined style sac and mid-gut (MG) which passes backwards between the BIOLOGY AND FEEDING OF LIMNOPERNA 273 posterior byssal retractors (PBR (1), (2) ). Just dorsal to the posterior adductor (PA) the style sac terminates but the mid-gut loops forwards to pass back between the posterior byssal retractors. The mid-gut loops again on the right side of and just before the stomach and passes posteriorly to penetrate the ventricle of the heart (V) and terminate in the anus near to the exhalant siphon. The detailed structure of the style sac and mid-gut of Limnoperna is essentially the same as that described for Mytilus edulis by Giusti (1971). The stomach of Limnoperna (Fig. 6) is elongate and bears a close similarity to the stomachs of other mytilids,e.g., Lithophaga (Purchon, 1957), Mytilus edulis (Graham, 1949: Reid, 1965), Adula (Fankboner, 1971), Botula, Lithophaga and Perna (Dinamani, 1967) and thus belongs to type Ш and Section I of the stomach types elucidated by Purchon (1957) and Dinamani (1967) respectively. An attempt has been made in this description of the stomach of Limnoperna to combine the nomenclatural systems of Purchon (1957) and Reid (1965). In Limnoperna, as in all bivalves, the floor of the stomach is dominated by the major typhlosole (T) and associated in- testinal groove (IG) which arise in the style sac (SS) and pass forwards to penetrate the food sorting caecum (FC). The major typhlosole does not divide as reported for Adula by Fankboner (1971). The minor typhlosole (MT) also arises in the style sac and passes, for a short distance, along the right side of the stomach. The crystalline style (CS) is secreted in the style sac (SS) and, protruding into the stomach, rotates against the typically saddle-shaped gastric shield covering the left dorso-lateral wall of the stomach. The gastric shield sends a flare into the left pouch (LP). The left pouch (Fig. 7) sees the origin of what Reid (1965) has termed the left duct tract (LDT), which passes into the food sorting caecum (Fig. 8, FC). On the right side of the stomach the right duct tract (RT) also passes into the food sorting caecum. Associated with the right duct tract are 2 groups of ducts to the digestive diverticula [DDD(1) & DDD(2)]. Similarly in the left pouch (Fig. 7) there are 2 further groupings of ducts leading to the digestive diverticula [DDD(3) € DDD(4)]. Purchon (1957) considered the right duct tract to be a sorting area and termed it sorting area 3 (SA3). The equivalent sorting area of the left duct tract would appear to be the floor and walls of the left pouch (Fig. 7). A further sorting area (SA2) can be recogniz- ed dorsal to the entrance of the food sor- ting caecum and separating this opening from the entrance to the left pouch. Each of these sorting areas is a system of ridges and grooves which Reid (1965) has called type A and which is found in all bivalves. The food sorting caecum is a com- paratively long finger-shaped pocket penetrated to its apex by the tongue of the major typhlosole (Fig. 8, TT). At the apex there is a sorting area which is of type B (Reid, 1965) and which is found only in those bivalves which Purchon (1960; 1963) has grouped together as the Gastrotriteia, and which is characteristic of the Mytilacea (Reid, 1965). In the stomach, cilia on the crests of the major typhlosole (Fig. 6) and inner folds of the left and right duct tracts pass food material entering the stomach into the food sorting caecum (Fig. 8). Ciliary currents in the grooves of the inner folds of the left and right duct tracts and the in- current fold of the intestinal groove also pass particles into the food sorting caecum. At the apex of the caecum the B type sor- ting area (Reid, 1965) sends acceptable particles of a suitable size into the outer folds of the left and right duct tracts which pass this material to the ducts of the digestive diverticula of the left pouch and right duct tract. Rejected particles pass out of the food sorting caecum in the excurrent intestinal groove of the major typhlosole and pass to the mid-gut for ultimate defecation. Particles of intermediate size are probably recirculated by the dorsal hood tract passing them back to the dorsal hood and gastric shield. Limnoperna possesses ducts leading to the digestive diverticula in the food sorting caecum (Fig. 8, DDD(5)). It is not known if these ducts occur in other mytilids although Fankboner (1971) illustrated similar ducts in the food sorting caecum of Adula. The minor the major typhlosole in clearing the stomach of un- wanted food into the mid-gut. No appen- dix could be observed in the stomach of Limnoperna as reported for Mytilus (Reid, 1965) and Adula (Fankboner, 1971). The basic structure of the ducts and the digestive tubules comprising the digestive diverticula bear a close similarity to those described by Owen (1955) for Mytilus edulis. typhlosole assists DISCUSSION Limnoperna fortunei has recently colonised the pipes, conduits and channels of part of the water supply system of Hong Kong. Details of the world-wide distribu- tion of this animal are unknown but it is DDD (2) GS B. MORTON believed to be restricted to S.E. Asia and to be widely distributed in the rivers of China. It seems likely that Limnoperna has been introduced into Hong Kong either indirectly via the Pearl river or directly as a result of the intake of raw water into Hong Kong from China sub- sequent to 1967. The first widespread reports of this animal in 1968 would sup- port the latter view and indicate that Lim- noperna is capable of undertaking an ar- tificial expansion of range given a suitable habitat. In this case, as apparently happened with Dreissena in Europe and Corbicula in North America, this process is facilitated by the construction of inter- connecting water supply systems. Whatever the source, Limnoperna has now firmly established itself in the water supply system of Hong Kong. Like Dreissena polymorpha in Europe, it would DDD (1) Ao 1mm RT FIG. 6. Limnoperna fortunei. The structure and ciliary currents of the interior of the stomach after opening by a horizontal incision in the right side (For abbreviations see p 267). BIOLOGY AND FEEDING OF LIMNOPERNA 275 DDD (5) FIG. 7. Limnoperna fortunei. The structure and ciliary currents of the food sorting caecum of the stomach. (For ab- breviations see p 267). seem that Limnoperna is ideally adapted in the possession of a stout byssus and heteromyarian form to a life in fast flowing waters. Dreissena, however, can also thrive in the relatively static waters of reservoirs (Morton, 1969b) and in this habit can cause problems of sedimentation (Milheev, 1967; Stanczykowska, 1968). It may be significant that very recently Lim- noperna has been dredged up from the bottom of Hong Kong's newest and largest reservoir, Plover Cove. It would seem that both of these animals, despite their ap- parently specialized form, are liberal in their choice of habitat and are potentially detrimental at all stages of the water supp- ly process. The close similarity in choice of habitat and form existing between Limnoperna and Dreissena could suggest some degree of phylogenetic affinity between the Dreissenacea and МуШасеа, as recently postulated by Purchon & Brown (1969). Yonge & Campbell (1968) showed that the similarities that existed between Dreissena and the mytilid Septifer were due to con- vergence. Morton (1970) and Taylor, Kennedy & Hall (1972) agree with this view and further suggest that from both a palaeontological and a morphological view the affinities of Dreissena lie with the Cor- biculacea. Dreissena would thus be more closely related to Corbicula manillensis, a pest of North American water supply systems. From Table 1 it can be seen that in near- ly all major anatomical respects Dreissena and Limnoperna are very different, and it is hard to account for the high degree of similarity obtained for Dreissena and the mytilids studied by Purchon € Brown (1969). Most of the few similarities that do exist between the 2 groups, e.g., the heteromyarian condition which occurs in a variety of unrelated Bivalvia, are at- tributable to convergent evolution and the colonisation of similar habitats. It is en- visaged both for Dreissena and Limnoper- na that the neotenous retention of the byssus (Yonge, 1962) in their respective ancestors resulted in the evolution in both groups of the heteromyarian form (Yonge & Campbell, 1968). Both have sub- sequently exploited this condition, with the development of osmoregulatory powers, in the colonisation of fresh waters. The close phylogenetic affinities of Lim- noperna are at present unknown. Soot- DDD (4) DDD (3) FIG. 8. Limnoperna fortunei. The structure and ciliary currents of the left pouch of the stomach. (For abbreviations see р 267). 276 В. MORTON Ryen (1955) did not mention this genus in his report on the family Mytilidae. However, Limnoperna shows a close similarity to the Australian species of Xenostrobus securis and X. inconstans (Wilson, 1967) in the possession of com- parable anatomical characters, e.g., the posterior byssal retractor muscle is divided into 2 and the mid-gut loops on the right side of the stomach. Furthermore both X. securis and X. inconstans live at the head of estuaries whilst other species, e.g., X. pulex are marine (Wilson, 1967). It would seem possible that Limnoperna evolved from forms essentially similar to these. Significantly Dreissena is closely related to the estuarine dreissenid species of Mytilopsis (Keen, 1969; Morton, 1970). It would thus seem that Dreissena and Limnoperna represent the apices of 2 phyletic streams both adapted for life in fresh waters. Significantly the hard sur- faces found in fresh water systems in many parts of the world are not normally colonised by bivalves, most species being infaunal, e.g., Unionacea, Corbiculacea. The hard surfaces niche was therefore a suitably vacant target for both Dreissena and Limnoperna. Significantly, within their own spheres of influence, both species would appear to be colonising this habitat as fast as it is artificially made for them. The ways in which Dreissena is adapted morphologicallv to a life in fresh waters has earlier been reported upon (Morton, 1969a). Limnoperna possesses ciliary tracts on the internal surfaces of the inhalant siphon which carry pseudofaeces towards the exhalant siphon. The intermittent rapid expulsion of water from the exhalant siphon blows these away together with the TABLE 1 Limnoperna fortunei Mantle 1. Periostracum 3 layered bo . Mantle fusion type A 3. Mantle fusion forms exhalant siphon only Shell 4. Heteromyarian 5. No byssal notch 6. Internal nacreous layer Ligament 7. Simple opisthodetic Musculature 8. Anterior adductor located on shell 9. Posterior pedal retractor located anteriorly Ctenidia 10. Homorhabdic, filibranchiate 11. Ciliation of type B(1) by ciliary fusion 13. Outer demibranch terminates abruptly 14. Ctenidial-labial palp junction | Alimentary 15. Style sac and mid-gut canal conjoined 16. Style sac and mid-gut loop between the byssal retractors 17. Stomach Type 3 Stomach Туре 1 2. Ctenidia attached dorsally Dreissena polymorpha Periostracum 2 layered Mantle fusion type A (Yonge, 1957) Mantle fusion forms both inhalant and exhalant siphons Heteromyarian Byssal notch No internal nacreous layer Complex opisthodetic Anterior adductor located on shell shelf Posterior pedal retractor located posteriorly Homorhabdic, eulamellibranchiate Ciliation of type C(1) (Atkins, 1937) Ctenidia attached dorsally by cuticular fusion Outer demibranch terminates gradually Ctenidial-labial palp junction Ш (Stasek, 1963) Style sac and mid-gut separate Style sac and mid-gut loop around the byssal retractors Stomach type 5 (Purchon, 1957) Stomach type ШО (Dinamani, 1967) BIOLOGY AND FEEDING OF LIMNOPERNA 277 faeces. Living as it can do in fast flowing waters, its siphons invariably facing the current, this process is a significant aspect of the morphology of Limnoperna since it enables the animals to feed and remove pseudofaeces at the same time but more importantly blows the waste material over the top of the animal and not straight out in front of it. This prevents the pseudofaeces from being taken back into the mantle cavity. The outer demibranchs of the ctenidia of Limnoperna are unusual- ly long. This adaptation gives a greater surface area for filtration and also places rejected particles travelling anteriorly on the crests of the ventral marginal food groove in much closer proximity to the rejection tracts of the mantle. The outer demibranch being longer dorso-ventrally but abruptly shorter antero-posteriorly to the inner demibranch also enables the labial palps to exert their selective т- fluence upon all 4 of the gill lamellae. For an animal living as Limnoperna can do in relatively silt-free, fast flowing waters this ctenidial-labial palp relationship ensures that all particles reaching the anterior end of the ctenidia are potentially usable as food. The alimentary system of Limnoperna is typical of the Mytilidae in general although the relatively large food sorting caecum in this species, when compared with the short caeca of species described by Dinamani (1967), may indicate a greater selective need in Limnoperna and thus ensure that all the potential food material is utilized. This would be perti- nent for such an animal living in silt-free, fast flowing waters. Significantly those mytilids (except Adula (Fankboner, 1971)) living in silt laden burrows possess small caeca (Dinamani, 1967). The food sorting caecum of Limnoperna and Adula (Fankboner, 1971) possess ducts to the digestive diverticula. These ducts in Lim- noperna, by increasing the total number of apertures to the digestive diverticula, may increase the capabilities of the animal for collecting a greater number of particles from a sparse food supply. Significantly perhaps, Dreissena polymorpha (Morton, 1969a) possesses an enlarged right caecum with a greater number of ducts to the digestive diverticula. Limnoperna is thus a relatively un- specialised mytilid, but those specialisations that do exist are concerned with greater efficiency in food collection and utilization. There are quite obviously physiological specialisations, especially with regard to the osmoregulatory processes. In essence, however, Limnoper- na is a typical mytilid and consequently possesses many primitive characters. Similarly Dreissena polymorpha is, anatomically, unspecialised and it has been suggested before (Morton, 1969b) that it is the retention of primitive characters in a habitat where there has been а trend in other lamellibranchs toward greater and greater specialisation that makes the possession of such primitive characters, e.g., the byssus and free swim- ming larvae, so successful. Limnoperna substantiates this view anatomically, but it yet remains to be seen whether or not Lim- noperna can be as successful as Dreissena in utilising these potentialities in the colonisation of new waterways. The oc- currence of Limnoperna in Hong Kong suggests that this may be so. SUMMARY The Asian fresh water bivalve Lim- noperna fortunei has recently been in- troduced into Hong Kong. In 4 years it has successfully colonised a large part of the water supply system. It thus reflects the pattern of colonisation of fresh water supp- ly systems in Europe and North America by Dreissena polymorpha and Corbicula manillensis respectively. Limnoperna possesses a highly efficient filtration and digestive system adapted for the collection and utilisation of food materials in fast flowing waters which may, characteristically, be devoid of much suspended material. Investigations into the anatomy of Lim- noperna show that it is a typical mytilid and is thus not related to Dreissena. Both animals show а superficial similarity to each other occasioned by convergent 278 В. MORTON evolution and the adoption of similar habits. Limnoperna further demonstrates the success of the anisomyarian condition in fresh waters typically possessing an in- faunal bivalve population. ACKNOWLEDGEMENTS | am grateful to Dr. Tadashige Habe of the National Science Museum, Tokyo, Japan and Dr. Barry Wilson of the Western Australian Museum, Perth, Australia for confirming the identity of Limnoperna fortunei. I am also grateful to Dr. Wilson for sending me specimens of Xenostrobus securis and for his comments on the synonyms of Limnoperna. Гат т- debted to the Director of the Waterworks Department of the Hong Kong Goverment for facilities provided during the course of this investigation and to Mrs. D. W. Kwan and Mr. D. Chi for technical assistance. REFERENCES ATKINS, D., 1937, On the ciliary mechanisms and interrelationships of lamellibranchs. Part ПТ. Types of lamellibranch gills and their food currents. Quart. J. microsc. Sci., 79: 375-421. BEEDHAM, G. E., 1958, Observations on the non-calcareous component of the shell of the Lamellibranchia. Quart. J. microsc. Sci., 99: 341-357. DINAMANI, P., 1967, stomach structure of the Malacologia, 5: 225-268. FANKBONER, P. V., 1971, The ciliary currents associated with feeding, digestion and sediment removal in Adula (Botula) falcata Gould 1851. Biol. Bull., 140: 28-45. GIUSTI, F., 1971, The fine structure of the style sac and intestine in Mytilus galloprovin- cialis Lam. Proc. malacol. Soc. London, 39: 95-104. COREA т. В. GOREAU, He Ll ESOO T RYEN, Т. & YONGE, С. M., 1969, On a new commensal mytilid (Mollusca: Bivalvia) opening into the coelenteron of Fungia scutaria (Coelenterata). J. Zool. London., 158: 171-195. GRAHAM, A., 1949, The molluscan Stomach. Trans Roy. Soc. Edinb., 61: 737:776. KEEN, M., 1969, In MOORE, В. C., ed., Treatise on invertebrate palacontology, Part Variation in the Bivalvia. N, Bivalvia. Geol. Soc. Amer. and Univ. Kan- sas Press KERNEY, M. P. & MORTON, B. S., 1970, the distribution of Dreissena polymorpha (Pallas) in Britain. J. Conchol., 27: 97-100. МКНЕКУ, У. P., 1967, Filtration nutrition of the Dreissena. Trudy usesojuzn. nauc isled. Inst., 15: 117-129. (In Russian) MILLER, В. С. € McCLURE, Е. A 1937 The fresh-water clam industry of the Pearl river. Lingnan sci. ]., Canton, 10: 307-322. MORTON, B. S., 1969a, Studies on the biology of Dreissena polymorpha Pall. 1. General anatomy and morphology. Proc. malacol. Soc. London., 38: 301-321. MORTON, B. S., 1969b, Studies on the biology of Dreissena polymorpha Pall. 3. Population dynamics. Proc. malacol. Soc. London., 38: 471-482. MORTON, B. S., 1969c, Studies on the biology of Dreissena polymorpha Pall. 4. Habits, habitats, distribution and control. Water Treatment and Examination, 18: 233-240. MORTON, B. S., 1970, The evolution of the heteromyarian condition in the Dreissenacea (Bivalvia). Palaeontology, 13: 563-572. OWEN, G., 1955, Observations on the stomach and digestive diverticula of the Lamellibranchia. Part 1. The anisomyaria and Eulamellibranchia. Quart. J. microsc. Sci., 96: 517-537. PURCHON, R. D., 1955, The structure and function of the British Pholadidae (Rock- boring Lamellibranchia). Proc. zool. Soc. London., 124: 859-911. PURCHON, R. D., 1957, The stomach in the Filibranchia and the Pseudolamellibranchia. Proc. 3001. Soc. London., 129: 27-60. PURCHON, R. D., 1960, The stomach in the Eulamellibranchia: Stomach Types IV and V. Proc. 2001. Soc. London., 135: 431-489. PURCHON, R. D., 1963, Phylogenetic classification of the Bivalvia with special reference to the Septibranchia. Proc. malacol. Soc. London., 35: 71-80. РОВСНОМ, В. D. € BROWN, D., 1969, Phylogenetic interrelationships among families of bivalve molluses. [Proc. Third Europ. Malac. Congr.] Malacologia, 9: 163- ТИ REID, В. С. B., 1965, The structure and func- tion of the stomach in bivalved molluses. J. Zool. London, 147: 156-184. SINCLAIR, В. M., 1964, Clam pests in Tennessee water supplies. J. Amer. Water Works Assoc., 56: 592-599. BIOLOGY AND FEEDING OF LIMNOPERNA SINCLAIR, В. M., 1971а, Corbicula variation and Dreissena parallels. The Biologist, 53: 153-159. SINCLAIR, R. M., 1971b, Annotated bibliography on the exotic bivalve Corbicula in North America, 1900-1971. Sterkiana, 43: 11-18. SOOT-RYEN, T., 1955, A report on the family Mytilidae (Pelecypoda). Allan Hancock Pacif. Exped., 20: 1-174. STANCZYKOWSKA, A., 1968, The filtration capacity of populations of Dreissena polymorpha Pall. in different lakes as a factor affecting circulation of matter in the lake. Ekol. Pol., B14: 265-270. (In Polish) STASEK, C. R., 1963, Synopsis and discussion of the association of ctenidia and labial palps in the bivalved Mollusca. Veliger, 6: 91-97. TAYLOR; J., KENNEDY, W. J: & HALL; A, 1972, The shell structure and mineralogy of the Bivalvia. Part 2, Chamacea-Poromyacea, Conclusions. Bull. Brit. Mus. (natur. Hist.) Zool. (In press). TCHANG-SI, LI SHIH-CHENG & LIU YUEN-YING, 1955, Bivalves (Mollusca) of Tung-Ting Lake and its surrounding waters, Hunan Province, China. Acta. Zool. Sinica, 17: 212-213. 279 TRUEMAN, E. R., 1950, Observations on the ligament of Mytilus edulis. Quart. J. microsc. Sci., 91: 225-235. WHITE, K. M., 1937, Mytilus. Liverpool Marine Biology Committee Memoirs, 31: 1- fe WILSON, В. R. 1967, A new generic name for three recent and one fossil species of Mytilidae (Mollusca-Bivalvia) in Southern Australasia, with redescriptions of the species. Proc. malacol. Soc. London., 37: 279-295. YONGE, C. M., 1955, Adaptation of rock- boring in Botula and Lithophaga (Lamellibranchia, Mytilidae), with a discus- sion on the evolution of this habit. Quart. J. microsc. Sci., 96: 383-410. YONGE, C. M., 1957, Mantle fusion in the Lamellibranchia. Publ. Staz. zool. Napoli, 29: 151-171. YONGE, С. M., 1962, Оп the primitive significance of the byssus in the Bivalvia and its effects in evolution. J. mar. biol. Assoc. U.K. 42: 113-125. YONGE, C. M. & CAMPBELL, J. I., 1968, On the heteromyarian condition in the Bivalvia with special reference to Dreissena polymorpha and certain Mytilacea. Trans. Roy. Soc. Edinb., 68: 21-43. ZUSAMMENFASSUNG EINIGE ASPEKTE DER BIOLOGIE UND FUNKTIONELLEN MORPHOLOGIE DER NAHRUNGSAUFNAHME- UND VERDAUUNGSORGANE VON LIMNOPERNA FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA) B. Morton Limnoperna fortunei (Dunker) wurde in letzter Zeit in das Wasserversorgungssystem von Hongkong eingeschleppt. Das erste Auftreten dieses Weichtiers kann mit dem Beginn der Wasserzufuhr vom East River in China nach Hongkong in Verbindung gebracht werden. Vermutlich wird Limnoperna die rasche Arealerweiterung erreichen kónnen, die wir bei Dreissena polymorpha in Europa und bei Corbicula manillensis in Nordamerika erlebt haben. Daher wurden die diesbeziiglichen Aspekte der funktionellen Morphologie und Biologie von Limnoperna untersucht. Vergleiche wurden angestellt mit anderen Mytiliden und mit Dreissena, die Limnoperna auf den ersten Blick ähnelt. Die Möglichkeit einer phylogenetischen Verwandtschaft zwischen diesen 2 Tieren wird als gering angesehen; die Ahnlichkeiten sind vielmehr auf konvergente Evolution und die Einnahme ähnlicher Lebensräume zurückzuführen. Die Entstehung der Heteromyarier- Verhältnisse bei Mytilacea und Dreissenacea, zusammen mit der nachfolgenden Ausbildung osmoregulatorischer Fähigkeiten, hat Limnoperna und Dreissena befähigt, Hartsubstrat in Süßwassersystemen zu erobern. In diesem Lebensraum begegnet ihnen keine Konkurrenz von Seiten der spezialisierten bodenbewohnenden Muscheln, wie sie 280 B. MORTON für Süßwasser kennzeichnend sind. Die Besiedelung dieses Lebensraums überschneidet sich bei Dreissena mit den Interessen des Menschen, soweit sie seine Wasserversorgung betreffen; bei Limnoperna muß man damit vielleicht ebenso rechnen. C.M.-B. RESUME ASPECTS DE LA BIOLOGIE ET DE LA MORPHOLOGIE FONCTIONNELLE DES ORGANES DE NUTRITION ET DE DIGESTION DE LIMNOPERNA FORTUNEI (DUNKER) (BIVALVIA: MYTILACEA) B. Morton Limnoperna fortunei (Dunker) a été recemment introduit dans les canalisations du ser- vice d eau de Hong Kong. La premiere apparition du mollusque peut étre rapportée au commencement de la mise en service de canalisations entre Hong Kong et la Riviere de l'Est en Chine. On pense que Limnoperna pourrait imiter la rapide expansion spatiale réalisée par Dreissena polymorpha en Europe et Corbicula manillensis en Amérique du Nord. Pour cette raison, on a étudié les aspects significatifs de la morphologie fonctionnelle et de la biologie de Limnoperna. Des comparaisons ont été faites avec d autres mytilidés et avec Dreissena qui ressemble superficiellement а Limnoperna. Га possibilité d'une affinité phylogénétique entre ces 2 animaux est écartée; les similitudes étant dues a une évolution convergente et à l'adoption d'un mode de vie similiare. L'évolution de l'hétéromairie, chez les Mytilacea et les Dreissenacea suivie de l’évolution du pouvoir os- morégulateur, a rendu capable Limnoperna et Dreissena d'envahir avec succés les sur- faces dures des canalisations d'eau douce. Dans cet habitat il п’у a plus la compétition des bivalves endogés caractéristiques des eaux douces. La colonisation de cet habitat a provoqué un conflit entre Dreissena et peut-ére aussi Limnoperna, et les intéréts humains en matiére de distribution d eau douce. ALE: RESUMEN ALGUNOS ASPECTOS DE LA BIOLOGIA Y MORFOLOGIA FUNCIONAL DE LOS ORGANOS DIGESTIVOS DE LIMNOPERNA FORTUNEI (DUNKER) (BIVALVIA- MYTILACEA) B. Morton Limnoperna fortunei (Dunker) fué introducida recientemente en el sistema de abastecimiento de agua potable en Hong Kong. Esta introducción se relacionó con la in- iciación de la toma de agua en Hong Kong del río del Este, en China. La rápida expansión de Limnoperna sugiere que puede repetirse la experiencia de Dreissena polymorpha en Europa y Corbicula manillensis en Norte América. Por tal razón se investigaron los aspectos pertinentes a la morfología funcional de Limnoperna, y se hicieron comparaciones con otros mitilidos, y con Dresissena a la cual Limnoperna se asemeja superficialmente. Se descarta la posibilidad de afinidad genética entre esos dos animales, y las similaridades que presentan se deben a evolución convergente y a la adop- ción de hábitos semejantes. La evolución de la condición heteromiaria en los Mytilacea y Dreissenacea, seguida de una evolución subsequente de poder osmoregulatorio, ha BIOLOGY AND FEEDING OF LIMNOPERNA capacitado a Limnoperna y Dreissena para la invasion favorable de las superficies duras en los sistemas fluviales: en tal habitat estan libres de la competencia de los bivalvos que son caracteristicos de las aguas dulces. La colonización de Dreissena, que ha entrado en conflicto con los intereses humanos para la provisión de agua dulce, puede repetirse con el mismo conflicto en el caso de Limnoperna. J.J.P. АБСТРАКТ НЕКОТОРЫЕ АСПЕКТЫ БИОЛОГИИ И ФУНКЦИОНАЛЬНОЙ МОРФОЛОГИИ ОРГАНОВ ПИТАНИЯ И ПИЩЕВАРЕНИЯ ЛВУСТВОРЧАТОГО МОЛЛЮСКА LIMNOPERNA FORTUNEI (DUNKER), MYTILACEA Б. МОРТОН Limnopevna fortunei (Dunker) недавно была интродуцирована в пресноводнук систему водоснабжения Гонконга. Изначальная встречаемость этого моллюска здесь может быть связана с началом водоснабжения Гонконга из рек восточного Китая. Предполагается, что Limnoperna могла бы конкурировать C быстрым расселением Dreissena polymorpha в Европе и Corbicula manillensis в Северной Америке. Поэтому были исследованы соответствующие аспекты функциональной морфологии и биологии Limnoperna. Было проведено сравнение с другим! митилидами и с Dreissena, на которую Limnoperna внешне похожа. Возможность филогенетической близости между этими двумя животными не принимается в расчет. Сходство происходит благодаря конвергентной эволюции и адаптации к сходным условиям обитания. Эволюция гетеромиарных признаков у Mytilacea и Dreissenacea, сопровождалась последующей эволюцией осморе гулятерных способностей и дала возможность Limnoperna и Dreissena успешно освоить твердый субстрат в пресноводных системах. В таких местообитаниях у них нет конкуренции с не специализированными двустворчатыми моллюсками инфауны, характерными для пресных вод. Заселение этого меестосоитания ДЛрейссеной и, возможно, Limnoperna, может вступать в противоречения © интересами людей, имея ввиду снабжение пресной водой. Z.A.F. 281 nae eye eee ee [LA AAT WIV SEL TER ORAN EN APT ARE 7 ry Th ses 16-06 п inst A alae the ex su». “buses ddl rg” «© mi ant gie Higg se mye) M paie ee Cat te nik Pa rung Saisie JA Lape | dl Adit MAN п 1 ¿dd di bw tenets ii O ee a" y ne. | фо «| Y ITA nee di MA se TE ho 08 wtp Nags 6 10 ма $ у orgie! ‘0 fo In a Y ae у So 97! Ho VAS AGA Dine sin a WAPI =e Ai es bare! taie (hits da A i o | NEE Sem as о F Me i, 2e Ome re an Oh = ie Air oe re si =F Vies E eee Ze Ver e Alla ab Wis o ne que o 1 heel JS Lie? mus Y | de pa Vie a рез OS opened aro free UD Zu en nf dt men Dr A On à 41. ir us р А vey „Чень +‘ a Mn gd. loli На os y ih a MALACOLOGIA, 1978, 12(2): 283-293 THE RECTUM OF “MODIOLUS” DEMISSUS (DILLWYN) (BIVALVIA: MYTILIDAE): A CLUE TO SOLVING A TROUBLED TAXONOMY! Sidney K. Pierce, Jr. Department of Zoology University of Maryland College Park, Maryland 20742, U.S.A. ABSTRACT The ribbed mytilid mussel Modiolus demissus (Dillwyn) has been placed in several genera during the past 150 years. Although Arcuatula (Jousseaume) Lamy, 1919, Geukensia, Van de Poel 1959, and Ischadium Jukes-Brown, 1905, have all been recently proposed as the correct generic taxonomic position for this species, M. demissus has per- sisted in the general literature. Data are reported which demonstrate a profound morphological difference between the relationship of the organs in the pericardial cavity of both Modiolus demissus and Ischadium recurvum, and that of other mytilids. The rectum of these 2 mussels, rather than passing through the pericardial cavity inside the ventricle as in other mytilids, leaves the heart through the dorsal surface of the ventricle about mid-way through the pericardial cavity. The rectum then passes in an are to the posterio-dorsal region of the pericardial cavity. Thus, the posterior end of the ventricle is not anchored in place as oc- curs in other mytilids. Internally, the typical mytilid rectum shows a reduced, flattened typhlosole. The Modiolus demissus rectum, in contrast, has a well-developed typhlosole which protrudes markedly into the rectal lumen. These morphological features, in company with shell morphology and some previously reported physiological data, are used to support the isolation of the ribbed mussel both from Modiolus and from other mytilid genera, and its relocation in Arcuatula. INTRODUCTION The systematics of the family Mytilidae has long been in turmoil. Thus, although a burgeoning literature deals with the various aspects of the biology of the mytilids, the continuing taxonomic juggling and the resulting incorrect iden- tifications have made interpretation of this literature most difficult. B. R. Wilson, in Australia, is presently attempting the monumental task of sorting out the taxonomy and systematics of this family on the basis of soft-part morphology (pers. comm. ). The specific taxon Mytilus demissus Dillwyn 1817 has been shuffled amongst several generic groups during the past 150 years. It has been perhaps most commonly recognized as a member of Modiolus Lamarck, 1799. Soot-Ryen (1955), however, placed this species in Arcuatula (Jousseaume) Lamy 1919, pointing out that Jousseaume chose Modiola plicatula Lamarck (=demissa Dillwyn) as the type of the genus although *Arcuatula certainly was intended to be used for Modiola ar- cuatula Hanley.” Soot-Ryen (1955), essen- tially redescribing Arcuatula, lists the following shell characteristics in support of the change: “the radial sculpture, crenulated anterior margin resulting from radial folds on the lunule, weak nymphae and light ligament.” Subsequently, Van de ! Contribution No. 4 from the Tallahassee, Sopchoppy and Gulf Coast Marine Biological Association (283) 284 5. К. PIERCE Poel (1959) proposed Geukensia Van de Poel (1959) as the appropriate generic designation for “Modiolus” demissus simply stating that Soot-Ryen (1955) had badly interpreted Lamy's (1919) descrip- tion. Most recently, Kenk (1966) has placed “Modiolus” demissus in Ischadium Jukes-Brown 1905, thereby allying it with another problematical mussel I. recurvum Rafinesque, 1820. Kenk (1966) used both shell and soft-part morphologies to support this generic change, but she ignored several important differences in the shell morphologies which seem to make her change inappropriate. These differences are discussed subsequently. Apparently none of these suggestions has been widely accepted, for the designation Modiolus demissus persists. Mention should also be made of some taxonomic confusion presented by another mytilid mussel used in this study. Modiolus americanus Leach, 1815, a taxon applied to subtidal mussels from the west coast of Florida, is apparently a mixture of 2 species (Beauperthuy, 1967). On the basis of shell characteristics, a new species M. squamosus Beauperthuy, 1967, has been described as distinct from M. americanus. Modiolus squamosus is the predominant subtidal mussel found in Apalachee Bay and St. George Sound off the coast of north Florida. Although the identity of the species used in this study has been confirmed for me by Wilson (pers. comm.) as being M. squamosus, R. T. Abbott (Delaware Museum of Natural History, pers. comm.) considers this mussel to be a subspecies of M. modiolus (Linnaeus) since, according to him, half- grown specimens of M. modiolus and M. squamosus are absolutely inseparable. However, the morphology of the periostracum of the 2 species is quite different (see Soot-Ryen, 1955, and Beauperthuy, 1967), and regardless of size, members of the 2 forms can readily be dis- tinguished on the basis of this structure. Since the morphology of the periostracum is used as a taxonomic character, Beauperthuy's species should probably stand. Consideration of characteristics, other than shell structure, might facilitate the construction of a more reliable and durable mytilid classification, free of the present taxonomic conflicts. To this end, a study of the comparative morphology of the pericardial region of several mytilids was carried out, after preliminary ex- amination of this region in several species of “Modiolus” had already indicated some morphological variation. A considerable literature on the comparative morphology (both gross and histological) of the bivalve pericardial cavity and associated struc- tures indicates familial constancy of the arrangement of organs contained therein (e.g. White, 1942; Jegla & Greenberg, 1968a,b). The pericardial complex in 5 dif- ferent species was examined here for both organological and histological organiza- tion and its variation. The differences pre- sented here elucidate the taxonomy of the genus Modiolus. MATERIALS AND METHODS The mytilids used in this study were Mytilus edulis (Linnaeus), Modiolus de- missus granosissimus (Sowerby), Modiolus demissus demissus (Dillwyn), Modiolus squamosus (Beauperthuy), and Ischadium recurvum (Rafinesque). Specimens of М. edulis were obtained from the Supply Department of the Marine Biological Laboratory, Woods Hole, Massachusetts. Modiolus demissus granosissimus were collected in a salt marsh on the tip of Alli- gator Point, Franklin County, Florida; the northern subspecies, M. d. demissus, were collected from the shore of the Patuxtent River near Solomons Island, Maryland. Modiolus squamosus specimens were found just below the low tide mark on the seaward edge of a sand bar in Alligator Harbor, Franklin County, Florida. Ischadium recurvum were collected from oyster trays suspended from the pier of the Chesapeake Biological Laboratory, Solomons Island, Maryland. The morphological relationships of the pericardial regions of these mussels were studied by both gross dissection and light microscopy. The following histological RECTUM OF MODIOLUS 285 procedure was used. The ventricle, auricles, and rectum were removed intact from large mussels and fixed in aequeous Bouin s fixative. Small whole animals were placed in formic Bouin s fixative in order to simultaneously decalcify the valves and fix the tissues. Fixed tissues were de- hydrated in an alcohol series, cleared in methyl salicilate, and imbedded in paraf- fin for sectioning. Sections were cut at a thickness of 7-10u and stained with either Masson's trichrome stain or Azure A and eosin (cf. Humason, 1967). The valve measurements reported were taken from single valves using vernier calipers or dividers and a mm scale. OBSERVATIONS AND DISCUSSION Kenk (1966) placed “Modiolus” demissus in Ischadium listing the fol- lowing distinctive features of the shell morphology: “sculpture consisting of bifurcating radial striations covering most or all of the shell, dorsal angle obtuse and broadly rounded, umbonal keel low, an- terior hinge teeth consisting of crenula- tions corresponding to the anterior ex- ternal ribbing, post ligamental teeth absent. This is a misleading description, both of “Modiolus” demissus and of the type of genus, I. recurvum. The anterior hinge teeth of I. recurvum are dysodont teeth corresponding to the radial ridges of the lunule and appearing quite like those of Mytilus edulis. “Modiolus” demissus, of course, totally lacks anterior hinge teeth. In addition, the valves of the 2 species differ in several other respects which Kenk (1966) either attributed to allometric growth or failed to mention. Ischadium recuroum is characterized by a broad mytiliform shape, anterior slightly sub- terminal umbones, ligament which extends anteriorly past the anterior byssus retractor muscle scar, and the lack of an anterior adductor scar. In contrast, the shell of “Modiolus demissus is basically an elongated modioliform shape, with dor- sal angle much less obtuse, no hinge teeth, umbones more inflated and posterior than I. recurvum, ligament beginning well posterior to the anterior byssus retractor scar, and an obvious, ovoid anterior adduc- tor scar. Thus, on the basis of shell morphology alone, “ Modiolus’ demissus does not seem to belong in Ischadium. In spite of the differences in shell morphology between these 2 species, the soft parts of “Modiolus” demissus and I. recuroum have in common а striking morphological feature which distinguish them not only from other species of Modiolus but also from those of Mytilus as well. This feature occurs within the peri- cardial complex and concerns the rela- tionship of the rectum with the ven- tricle. Most mytilid ventricles are suspended from 4 points: anteriorly from the aorta and rectum, posteriorly from the rectum and laterally from the auricles. The rectum passes longitudinally through the entire lumen of the ventricle, and therein throughout the length of the pericardial cavity. Such an arrangement of rectum and ventricle has been described in several mytilids (Field, 1922; White, 1942; Jegla & Greenberg, 1968a), and is illustrated in Modiolus squamosus, in Fig. 1. The suspension of the ventricles of “Modiolus” demissus (Fig. 2) and Ischadium recurvum is quite different from the standard mytilid plan and results from the modified path of the rectum through the pericardial cavity. The rectum passes only through the anterior portion of the ventricle. Then, emerging from the dorsal surface of the ventricle, it arches dorsally, in its own sheath, along the roof of the pericardial cavity, proceeding to its exit at the posterior end of the cavity. The posterior half of the ventricle, unsup- ported by the rectum, hangs freely in the pericardial cavity. The anterior end of the ventricle is suspended and anchored by the auricles and the rectum. One obvious physiological consequence of this arrange- ment is that the direction of ventricular beat in these 2 species is from posterior to anterior, rather than from lateral to medial as in most mytilids. It is difficult to ascribe any functional advantage to either plan of rectum traverse through the pericardial cavity of these mussels. There is, however, another 286 5. К. PIERCE ДА ee =< u ad «re = > SERLE ler Ro Tr Sa xs > > => y E ers FIG. 1. The pericardial complex of Modiolus squamosus. The pericardial membrane has been removed to reveal the ventricle with the rectum (1) passing internally between the anterior (2) and posterior (3) attachments of the ventricle. Note that throughout the length of the pericardial cavity, the rectum is inside the ventricle. The ventricle is suspended laterally, at the atrio-ventricular junction (4), by the glandular auricles (5). FIG. 2. The pericardial complex of Modiolus demissus granosissimus. The pericardial membrane has been removed. The rectum enters the ventricle at the anterior end of the pericardial chamber (1). The rectum then passes through the anterior portion of the heart and emerges through the dorsal surface of the ventricle (2), leaving the posterior portion of the ventricle (3) free in the pericardial chamber. Laterally, the ventricle is suspended by the atria (4) at the atrio-ventricular junction (5). Note that the rectum has been separated from the mantle (6) posterior to its exit from the ventricle. RECTUM OF MODIOLUS 287 TABLE 1 Distances from the most dorsal point of the posterior muscle scar to the dorsal valve edge of Mytilus edulis and Modiolus demissus. (n=25/species) Distance from Species Valve length Valve width posterior muscle at longest point at widest point scar to dorsal valve edge Mytilus edulis 58.9° 28.4 4.6 (+5.8) (43.3) (ESO) Modiolus demissus 61.1 24.0 3.8 (Gallo) (E12) (+0.6) ° Distance in mm (+ S.D.) FIG. 3. Cross-section of the ventricle and rectum of Mytilus edulis in the region of the atrio- ventricular junction showing the reduced typhlosole (T) and the mid-ventral furrow (М). Trichrome stain, 40Х. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum; C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V-ventricular muscle. 288 5. ©. PIERCE morphological difference between Mytilus edulis, Modiolus squamosus and Modiolus demissus which may account for the plan shown by M. demissus. The rectum in these mytilids, after leaving the ventricle and pericardial cavity, passes dorsally over a complex of muscles comprised of the pos- terior adductor, posterior byssus retractor, and posterior pedal retractor. If this mus- cle complex were located farther dorsad with respect to the heart in М. demissus than in М. edulis, the rectum of М. demissus would also have to follow a more dorsal route. In order to test this possibili- ty, measurements were made of the dis- tance between the highest point of the posterior muscle scar complex and the dor- sal edge of the valve in specimens of M. demissus and M. edulis of approximately equal length. These measurements, sum- marized in Table 1, indicate that, indeed, the posterior muscle complex of М. demissus is located some 20% closer (P<0.1) to the dorsal valve margin than that of M. edulis. I hasten to acknowledge the difficulties of drawing comparative conclusions based on valve measurements from different species of bivalves. The necessary assump- tions of identical growth patterns, iden- tical size and shape and identical organ placement are at best tenuous and most likely unwarranted (for a detailed dis- cussion see Stasek, 1963; Stanley, 1970). In FIG. 4. Cross-section of the ventricle and rectum of Modiolus squamosus in the region of the atrio- ventricular junction showing the reduced typhlosole (T) and the mid-ventral furrow (М). Trichrome stain, 40X. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum; C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V-ventricular muscle. RECTUM OF MODIOLUS 289 FIG. 5. Cross-section of the ventricle and rectum of Ischadium recurvum in the region of the atrio- ventricular junction showing the reduced typhlosole (T) and mid-ventral furrow (M). The rectum has already passed out of the dorsal surface of the ventricle. Azure A and eosin stain, 40X. LR-lumen of rectum; E-ciliated columnar epithelial lining of rectum; C-connective tissue layer; W-outer wall of rectum; V-ventricular muscle. fact, there may be a sound embryological or physiological explanation for the heart- rectum plan exhibited by Modiolus demissus and Ischadium recurvum, but to date an alternative explanation is not evi- dent. While it is tempting to stress the taxonomic implications of the similarities of organ arrangement in the pericardial cavities of Modiolus demissus and Ischadium recurvum rather than the difference in shell morphology, the rectum itself offers further evidence in favor of the generic separation of these 2 species. The internal morphology of the rectum of “Modiolus” demissus is also different from that of other mytilids including Ischadium recurvum. Fig. 3 shows a cross- section of the rectum of Mytilus edulis, as it passes through the ventricle in the region of the atrio-ventricular junction. Fig. 4 shows a similar section for Modiolus squamosus and Fig. 5 a similar section for I. recuroum. The rectums of these 3 mussels correspond quite closely to that of the generalized rectum of the Anisomyaria described by Jegla & Greenberg (1968a,b). In particular they are thin-walled, with few muscle fibers and the intestinal typhlosole is reduced to 2 wide ridges with a mid-ventral furrow. The rectum of М. demissus (Fig. 6), on the other hand, de- viates from this plan. While it is also thin- walled and shows few muscle fibers, the typhlosole protrudes markedly into the rectal lumen, resembling more closely the 290 5. Ke/ PIERCE м c Mi Ne E < 3 . к. г / e FIG. 6. Cross-section of the ventricle and rectum of Modiolus demissus granosissimus in the region of the atrio-ventricular junction showing well developed typhlosole (T) and median ventral furrow (M). Note that the rectum has already passed out of the dorsal surface of the ventri- cle. Trichrome stain, 40X. LR-lumen of rectum; E-ciliated columnar ephithelial lining of rectum: C-connective tissue layer; W-outer wall of rectum; LV-lumen of ventricle; V- ventricular muscle; P-pericardial space. RECTUM OF MODIOLUS 291 rectum of Atrina rigida Solander, 1786 [Pinnidae], than that of other mytilids (see Jegla & Greenberg, 19684). Interestingly, observed pharmacological differences between Modiolus’ demissus and other mytilids may substantiate the suggested taxonomic validity of the morphological findings reported here. Greenberg (1968) has observed that the tone and amplitude of beat of the isolated heart of M. demissus is depressed by 5- Hydroxytryptamine (5-HT). The hearts of M. americanus (actually M. squamosus) and M. modiolus, as well as Mytilus spp. are excited by 5-HT (Greenberg, 1968). Greenberg (1968) suggested that this dif- ference is a taxonomic feature. Unfor- tunately comparable pharmacological data are not available for Ischadium recurvum. Physiological data of this kind may prove to be a useful taxonomic tool, for although many physiological differences exist between M. demissus and other mytilids, most appear to be a function of the ex- tremely high intertidal position occupied by M. demissus (Lent, 1969; Pierce, 1970, 1971). Pharmacology, on the other hand, would appear to be a physiological parameter which is not intimately depen- dent on environmental influences. Finally, “Modiolus” demissus occupies a habitat which is rare or unique among the bivalves. One of the mussels used in this study, Modiolus squamosus occurs subtidially in marine environments only. Both Mytilus edulis and Ischadium recur- vum are found in the intertidal zone and occur well up into brackish water. М. demissus, also occurring in the intertidal zone and in brackish water, occupies a habitat that is virtually semi-terrestrial. In fact, in most areas of its occurrence along the eastern and Gulf coasts of the United States, М. demissus spends more time ex- posed to the atmosphere than submerged. Unlike other bivalves which close the valves tightly while exposed to air, М. demissus keeps its valves ajar and respires aerially (Lent, 1969). Thus, “Modiolus” demissus exhibits several morphological and physiological features, along with an unusual еп- vironmental position, which serve to dis- tinguish it from other members of the genus Modiolus and from other genera in the Mytilidae. These data, together with the shell morphology described by Soot- Ryen (1955), strongly support the shifting of this species into the mytilid genus Ar- cuatula (Jousseaume) Lamy 1919. ACKNOWLEDGEMENTS The author thanks Dr. Michael J. Greenberg for providing the facilities with which much of this research was done. Thanks also to Dr. Barry W. Wilson for verification of the identification of Modiolus squamosus and for helpful com- ments on the preliminary manuscript. Finally, the author is grateful to Mr. Larry Wolter for his excellent assistance with the valve measurements. LITERATURE CITED BEAUPERTHUY, I., 1967, Los Mitilidos de Venezuela (Mollusca: Bivalva). Bol. Inst. Oceanog. Univ. Oriente, 6: 7-115. FIELD, I. A., 1922, Biology and economic value of the sea mussel Mytilus edulis. Bull. Bur. Fish., 38: 127-259. GREENBERG, M. J., 1968, Comparative physiology of the heart: Current trends. Experientia, Suppl., 15: 250-265. HUMASON, G. L., 1967, Animal tissue techniques, W. H. Freeman and Co., San Francisco, 569 p. ТЕСТА, T. С. € GREENBERG, M. J", 1968a, Structure of the bivalve rectum, I. Morphology. Veliger, 10: 253-263. JEGLA, T. C. & GREENBERG, M. J., 1968b, Structure of the bivalve rectum, II. Notes on cell types and innervation. Veliger, 10: 314- 319. КЕМК VIDA © 1966; Brachidontes (Mollusca-Bivalvia). thesis, Harvard University. ‚AMY, E., 1919, Les Moules et les Modioles de la Mer Rouge (D’apres les materiaux recueillis par M. le Dr. Jousseaume). Bull. Mus. Hist. Nat. Paris, 25: 173-178. LENT, C. M., 1969, Adaptations of the ribbed mussel, Modiolus demissus (Dillwyn), to the intertidal habitat. Amer. Zool., 9: 283-292. PIERCE, 5. K., JR., 1970, The water balance of Modiolus (Mollusca: Bivalvia: Mvtilidae): А revision of PhD; — 292 Osmotic concentrations in changing salinities. Comp. Biochem. Physiol., 36: 521- 533. PIERCE, S. К., JR., 1971, Volume regulation and valve movements by marine mussels. Comp. Biochem. Physiol., 39A: 103-117. SOOT-RYEN, Т., 1955, A report on the family Mytilidae, Allen Hancock Pacific Expeditions, 20: 1-174. STANLEY, S. M., 1970, Relation of shell form эк. -PIERGE STASEK, C. R., 1963, Orientation and form in the bivalved Mollusca. J. Morphol., 112: 195- 214. VAN DE POBLE, Ш. 1959. Faune malacologique du Hervien, Troisieme note (premiere partie). Bull. Inst. Roy. Sci. Nat. Belgium, 35: 1-26. WHITE, K. M., 1942, The pericardial cavity and the pericardial glands of the Lamellibranchia. Proc. malacol. Soc. Lon- to life habits in the Bivalvia (Mollusca). Geol. don, 25: 37-88. Soc. Amer., Memoir 125, 296 p. ZUSAMMENFASSUNG DAS REKTUM VON “MODIOLUS” DEMISSUS (DILLWYN) (BIVALVIA: MYTILIDAE): EIN SCHLUSSEL ZUR LOSUNG EINES VERWORRENEN TAXONOMISCHEN PROBLEMS 5. К. Pierce, Jr. Die gerippte Mytilide Modiolus demissus (Dillwyn) wurde in den vergangenen 150 Jahren in wechselnden Gattungen untergebracht. Zwar wurden Arcuatula (Jousseaume) Lamy, 1919, Geukensia, Van de Poel, 1959, und Ischadium Jukes-Brown, 1905, in letzter Zeit als korrekte Gattungszugehórigkeit ftir diese Art vorgeschlagen, doch hat sich Modiolus demissus allgemein in der Literatur gehalten. Es werden Daten geliefert, mit denen ein tiefgreifender morphologischer Unterschied in den Verhältnissen der Organe der Pericardialhöhle zwischen М. demissus und I. recurvum einerseits und anderen Mytiliden andererseits gezeigt werden kann. Anstatt im Innern des Ventrikels durch die Pericardialhöhle zu verlaufen, wie bei anderen Mytiliden, verlässt das Rektum dieser 2 Muscheln das Herz vielmehr durch die dorsale Oberfläche des Ventrikels, ungefähr durch die Mitte der Pericardialhöhle. Dann verläuft das Rektum bogenförmig in den posteriodorsalen Teil des Pericards. Das hintere Ven- trikelende ist also nicht hier verankert, wie das bei anderen Mytiliden der Fall ist. Innerlich zeigt das typische Mytiliden-Rektum eine zurückgebildete abgeflachte Typhlosolis. Das M. demissus-Rektum hat dagegen eine voll ausgebildete Typhlosolis, die deutlich ins Darmlumen ragt. Diese morphologischen Merkmale werden, zusammen mit der Schalenmorphologie und einigen früher berichteten physiologischen Angaben, dazu verwendet, die Aussonderung der gerippten Muschel sowohl aus der Gattung Modiolus als auch aus anderen Mytilidengattungen und die Wiedereingliederung in die Gattung Arcuatula zu unterstützen. C.M.-B. RESUME LE RECTUM DE “MODIOLUS” DEMISSUS (DILLWYN) (BIVALVIA, MYTILIDAE): UN INDICE POUR RESOUDRE UNE TAXONOMIE INSTABLE 5. К, Pierce, Jr. La moule striée Modiolus demissus (Dillwyn) a été placée dans plusieurs genres, durant les 150 derniéres années. Bien que Arcuatula (Jousseaume) Lamy, 1919, Geuken- sia, Van de Poel, 1959 et Ischadium, Juke-Brown, 1905, aient été récemment proposés RECTUM OF MODIOLUS comme position correcte en taxonomie générique pour cette espéce, Modiolus demissus a persisté dans la littérature scientifique. Certaines données démontrent une profonde différence morphologique entre les organes de la cavité péricardique d'une part de М. demissus et 1. recurvum et, d autre part, ceux des autres mytilidés. Le rectum de ces 2 moules, bien que traversant la cavité péricardique à l'intérieur du ventricule, comme chez les autres mytilidés, quitte le coeur par la surface dorsale du ventricule à peu pres à mi-chemin а travers la cavité péricar- dique. Le rectum passe alors dans un arc vers la région postérodorsale de la cavité péricardique. Ainsi, la partie postérieure du ventricule n'est pas tenue en place comme cela arrive chez les autres mytilidés. Intérieurement, le rectum typique de mytilidé montre un typhosole réduit, aplati. Le rectum de M. demissus, par contre, posséde un typhosole bien développé qui fait nette- ment saillie dans la lumiére du rectum. Ces faits morphologiques, en relation avec la morphologie de la coquille et de quelques données physiologiques précédemment décrites, sont utilisés pour établir la distinction de la ‘moule striée” vis-a-vis de Modiolus et des autres genres de mytilidés et pour l'intégrer dans le genre Arcuatula. ACL: RESUMEN EL RECTO DE “MODIOLUS” DEMISSUS (DILLWYN) (BIVALVIA: MYTILIDAE): INDICADOR PARA LA SOLUCION DE UNA INTRINCADA TAXONOMIA S2 К Pierce ir: El mytilido -mejillón rayado- Modiolus demissus (Dillwyn) ha sido, durante los últimos 150 años, colocado en varios géneros diferentes. Aunque Arcuatula (Jousseaume) Lamy 1919, Geukensia Van de Poel, 1959, e Ischadium Jukes-Browne, 1905 fueron todos, en época más reciente, propuestos como las posiciones taxomicas correctas para esta especie, Modiolus demissus persistió generalmente en la literatura. Los datos que se han registrado evidencian una profunda diferencia morfológica entre la relación de los órganos de la cavidad pericardial de M. demissus e I. recurvum, y aquellos de otros mytilidos. El recto, en las dos especies mencionadas, en lugar de pasar adentro del ventrículo a través de la cavidad pericardial -como en otros mytilidos-, sale del corazón cruzando la superficie dorsal del ventrículo, en la parte relativamente media, a través de la cavidad pericardial. Pasa, entonces, formando un arco, a la región postero- dorsal de la cavidad. Así, la extremidad posterior del ventrículo no esta fijada al lugar en que ocurre en otros mytilidos. Internamente, el recto de un mytilido típico, muestra un ciego reducido y aplanado. En M. demissus el recto contrasta por tener un ciego bien desarrollado como una protuberancia que se interna marcadamente dentro del lumen rectal. A estos caracteres morfológicos internos, acompañan aquellos de la concha y, junto con otros datos registrados previamente acerca de su fisiologia, todos se utilizan para cor- roborar la separación del mejillón rayado, tanto de Modiolus, como de los otros géneros de mytilidos, y su re-colocación en Arcuatula. LLP. 293 9 р да. y u Ps N} ON у N 2 ae] AN u) $ 1 i} ‘ 4 В р A N 4 gi) hy | >, i 0 ¢ . у 0 h yA £ > L 7 | ny I р » 6 A? Г 4 ie | | | ¿ ati tien noe q км e “ne + Mr vea fr ем 7 y № IH ¿Mint é в cl aly ep joie sir 4 нц vA a i alin ai р oli na, ди Y om Pry ef : : ’ 8 пар ipa, по MALACOLOGIA, 1973, 12(2): 295-338 THE ORIGIN AND EVOLUTION OF THE NEOGASTROPODA W. F. Ponder The Australian Museum Sydney, Australia ABSTRACT The order Neogastropoda probably evolved from the Archaeogastropoda or from a very primitive mesogastropod type, and not from the higher mesogastropods as is generally believed. It is suggested that the unique features of the neogastropod alimen- tary canal could be derived from existing structures in the archaeogastropods. The Neogastropoda appear to have evolved into 3 groups, which are regarded here as super- families, the Muricacea, Conacea and Cancellariacea. The evolution of the various organ systems within the Neogastropoda is outlined and the tendency to modify structures in a parallel fashion is noted. The relationships of each family in the Muricacea is discussed. With 2 exceptions, it appears that within this group, there are no natural higher groupings, probably because all of the families evolved from a common ancestral form more or less simultaneously. Thus various structures are dis- tributed in an almost random fashion throughout the superfamily according to the way in which each family has evolved. The Marginellidae and Volutomitridae may have arisen independently, whereas the Buccinidae, Melongenidae, Nassariidae and Fasciolariidae are so closely related that they could possibly be regarded as subfamilies. INTRODUCTION The order Neogastropoda or Steno- glossa is generally regarded as containing the most highly advanced prosobranch gastropods. They are characterized by the elongate siphonal canal of the shell and rachiglossate or toxoglossate radula. The order is a large one, having at least 1119 Recent and fossil genera and subgenera (Taylor & Sohl, 1962). This number is similar to that of the Archaeogastropoda, but is exceeded by the Mesogastropoda (as defined by Thiele, 1929 and Wenz, 1938- 1943). The large number of species and genera speaks for the success of the Neogastropoda. Although they are not known to have invaded the land, and few have penetrated into freshwater, they have adapted to almost every marine environ- ment, commencing with an explosive radiation during the Cretaceous Period. The order Neogastropoda is usually divided into 2 suborders, the Toxoglossa and the Rachiglossa. Thiele (1929) and Wenz (1938) divided the Rachiglossa into 3 superfamilies (Stirps), the Muricacea, Buccinacea and Volutacea. These divisions have been accepted by the ma- jority of later authors. The use of these groupings is here considered open to ques- tion and they have been abandoned for the purpose of the following discussions. Instead the name Rachiglossa will be used to cover all 3 of them. The object of this paper is to attempt to: (1) clarify the origin of the Neogastropoda and therefore its relationship to the Mesogastropoda, (2) briefly examine the various organ systems within the group, and the evolution of the group and (3) re- view the distinctive features of the families of the rachiglossate neogastropods and to arrange them in meaningful higher categories. Recommendation 29A of the Inter- national Commission on Zoological Nomenclature (ICZN) in 1961 recom- mends the superfamily ending—oidea, but this is not used in this paper because the ending—acea has been used consistently by most molluscan workers and this en- (295) 296 W. F. PONDER ding is used in the Treatise on Inverte- brate Paleontology, a work which will be a major reference source for students of the Mollusca for a long time. Some of the facts presented here are based on the writer s unpublished observa- tions. They are noted by the inclusion of the writers initials in parenthesis following such information. The following account is divided into 3 parts; a discussion of the origins of the neogastropods, the evolution of the main organ systems and the higher clas- sification of the order. PART 1. THE ORIGIN OF THE NEOGASTROPODA Most authors have indicated that the neogastropods evolved’ from proboscidiferous mesogastropods, such as the Tonnacea. This belief has been expressed by workers who have looked at several different organ systems, including Amaudrut (1898), Bouvier (1887), Troschel (1865-1875), Perrier (1889), Graham (1941), and Wilsmann (1942). Morton (1963) expressed the belief that there is little difference between the higher Mesogastropoda and the Neo- gastropoda and this view was also held by Risbec (1955). Cox (1960) combined the Mesogastropoda and the Neogastropoda, calling them the Caenogastropoda. He suggested that the Caenogastropoda were polyphyletic, being derived from various archaeogastropod taxa, which may have even been distinct suborders, and that they have no more in common than that they have advanced to a certain stage along more-or-less parallel lines of gas- tropod evolution. One group, the Hetero- gastropoda, was later separated from the Mesogastropoda (Kosuge, 1966). Knight, et al. (1954) have given the most detailed scheme to be advanced re- cently on the evolution of the Gastropoda. They indicated that the Neogastropoda were probably derived from the extinct Subulitacea in the Mesozoic, that this superfamily divided into the Muricacea, Buccinacea and the extinct Nerineacea, and that the latter gave rise to the Volutacea and Conacea. The 4 Recent superfamilies existed in the early Cretaceous, all arising more-or- less simultaneously, and all were clearly recognizable and surprisingly modern in appearance by the middle Cretaceous (Sohl, 1964). Patterson (1969) has shown that the chromosome numbers of the Mesogastropoda and Neogastropoda are very different. The haploid number varies from 28-36 in the Neogastropoda, 7-20 in the Mesogastropoda and 9-21 in the Archaeogastropoda. There is therefore lit- tle relationship in the chromosome num- bers of the neogastropods to those of the other 2 orders; althowgh* the Neogastropoda could have arisen by polyploidy from either. The evidence given below suggests that the Neogastropoda are a group derived in- dependently from an archaeogastropod or a very primitive mesogastropod ancestral form. They have followed certain general gastropod evolutionary trends which have resulted in their superficial similarity to other groups, such as the carnivorous mesogastropod superfamily Tonnacea. These lines of evolution include the forma- tion of a proboscis, the reduction of the ctenidia to a single, monopectinate gill, and the enlargement of the left os- phradium and marked increase in its sen- sory surface by the formation of lateral leaflets. The enlargement of the os- phradium was probably coupled with the formation of an anterior siphon. A siphon was probably present in the Subulitacea as members of this group had а well- developed anterior notch in the aperture. The osphradium functions as an efficient chemoreceptive organ in the neogastropods (Kohn, 1961b), the anterior siphon giving it directional significance. Fig. 1 indicates how the foregut of the Neogastropoda may have evolved. The salivary glands (sg) in the early archaeogastropods (Fig. 1, A) are simple glandular sacs attached to the buccal cavi- ty. They lie just behind the nerve ring (nr) in many archaeogastropods, and probably EVOLUTION OF NEOGASTROPODA 297 the salivary ducts of the ancestral neogastropod were pulled, by the elonga- tion of the snout, through the nerve ring at this primitive stage of development (Fig. 1, B-D) as Graham (1941) suggested. Two pairs of histologically different salivary glands are found in the Acmaeidae (Thiem, 1917) and also in some Neritidae. In the latter family, in Theodoxus (Whitaker, 1951) and Septaria (Bourne, 1908), the 2nd pair of salivary glands are blind, glandular tubules which open into a short, ventral extension of the buccal cavi- ty below the odontophore. In structure and position these glands resemble the accessory salivary glands (asg) in the Neogastropoda. The 2nd pair of salivary glands found in some Archaeogastropoda were probably present in the group that give rise to the Neogastropoda, although it is highly unlikely that the Neritacea or the Patellacea were this group. The structure of the mid-oesophagus is of particular interest in the neogastropods because it is this part of the alimentary canal, together with the radula, which provides the most distinctive and reliable means of separating the group from the remainder of the Prosobranchia. Amaudrut's (1898) and Graham s (1941) hypothesis for the derivation of the gland of Leiblein (or “unpaired foregut gland”) from an oesophageal gland is in keeping with the hypothesis advanced here for an archaeogastropod origin for the Neogastropoda, although these authors believed the group to have originated from the highly evolved mesogastropod group, the Tonnacea. The valve (or pharynx) of Leiblein (vl) (=esophageal bulb of Hyman, 1967) is always composed of a glandular pad lying around a ciliated cone or fold (v) which acts as an oesophageal valve (Graham, 1941). Apparently the only function of the glandular pad is to bind together food par- ticles. There is not complete agreement over the derivation of the valve of Leiblein. Graham (1941) suggested that it represents an enlargement of the oesophageal dorsal folds. Amaudrut (1898) supposed that this structure, together with the glandular mid-oesophageal folds, 15 homologous with the oesophageal pouches of the mesogastropods. Graham (1941) rejected the idea because the oesophageal pouches in mesogastropods, unlike the dorsal folds, are ventral structures. It does, however, seem possible that the valve of Leiblein is homologous with the buccal (or oesophageal) pouches (bp) of primitive archaeogastropods (Fig. 1, A) such as Haliotis and, other Zeugobranchia, the Trochidae, and the Patellacea. These pouches, at least in Haliotis, are lined with tall, glandular cells which stain with acid dyes (Crofts, 1929). Just behind the buccal pouches in Haliotis are dorsal and ventral ciliated valves and immediately behind lies the glandular mid-oesophagus. The oesophageal gland is confluent with the mid-oesophagus over all of its length and gradually revolves from a ventral to a dor- sal position (Fig. 1, A; og). The homology of the oesophageal pouches and the stenoglossan valve of Leiblein is implied by Hyman (1967) who refers to this struc- ture in the oesophagus of all prosobranchs as the “esophageal bulb.” The anterior oesophagus of the rachiglossan neogastropods probably represents an elongation, coupled with a ventral closure, of the roof of the buccal cavity in front of the buccal pouches. This idea is supported by the presence of dorsal folds and the absence of ventral folds in the rachiglossan anterior oesophagus. In addition, the dorsal folds generally lie laterally or ventro-laterally. In the more advanced archaeogastropods and in the mesogastropods, the anterior oesophagus appears to have been derived by elonga- tion behind the buccal pouches and valve (Fig. 1, H, I) and, consequently, sometimes has a pair of ventral folds. Thus the anterior oesophagus in the Rachiglossa and Mesogastropoda have different origins. The buccal pouches and valves in the Rachiglossa would thus be separated from the buccal mass (Fig. 1, D) and, after being pulled through the nerve ring by the general elongation of the anterior gut, would lie in the correct morphological position for the valve of Leiblein (Fig. 1, 298 W. Е. PONDER FIG. 1. Hypothetical evolution of the anterior and mid-gut of the ancestral types of the main groups of the Neogastropoda. The oesophageal gland and salivary glands are stippled and the nerve ring is shown in solid black. The dotted line in В, Е, and С indicate the scar left by the removal of the oesophageal gland; in E it represents the dorsal food channel. The double-headed arrows indicate the area of elongation of the oesophagus. A, Hypothetical archaeogastropod forerunner; В, conacean; С, cancellariacean; and D, muricacean ancestral types. E, Hypothetical fore-runner of marginellid-volutomitrid group. F, Families showing torsion within or behind nerve ring; С, Families showing torsion within valve of Leiblein. H, I, Mesogastropoda. asg, accessory salivary glands; be, buccal cavity; bp, buccal pouch; df, dorsal folds; nr, nerve ring; og, oesophageal gland; pr, proboscis; sg, salivary gland; у, oesophageal valve; vf, ventral folds; vl, valve of Leiblein. EVOLUTION OF NEOGASTROPODA 299 E, Е, С). The glandular parts of the buccal pouches must have spread around the oesophageal wall and thus form the glan- dular part of the valve of Leiblein. The oesophageal valves would be homologous with the ciliated cone overlying this pad. The salivary ducts, which in other prosobranchs enter the buccal wall, are often embedded in the anterior oesophageal wall (usually lying beneath the dorsal folds) in rachiglossans, this providing further evidence of the buccal derivation of the anterior oesophagus in the Rachiglossa. The buccal pouches are variable in posi- tion in the archaeogastropods, lying along- side the buccal cavity in Haliotis, but be- hind (as in Fig. 1, A) in Nacella (Haller, 1894) and in some lower mesogastropods (Fig. 1, I) such as Littorina (Fretter € Graham, 1962). The ancestral neogastropod possibly had the glandular buccal pouches lying on either side of the anterior end of the mid-oesophageal gland because the valve of Leiblein sometimes lies at the site of torsion. The buccal ganglia lie beneath the valve of Leiblein, perhaps indicating the valve's buccal origin. In the Cancellariidae (Graham, 1966) and in proboscidiferous mesogastropods, the buccal ganglia are situated just behind the buccal mass and have very long connectives, which pass through the proboscis. Graham (1966) showed that the mid-oesophagus lies in front of the nerve ring in Cancellaria (Fig. 1, C) and that the valve of Leiblein is just behind the buccal cavity. The mid- oesophageal gland is probably represented by a zone of glandular tissue lying below the dorsal folds of the oesophagus. Thus, in Cancellaria, the mid-oesophagus has been pulled through the nerve ring and the ventral valve of Leiblein (buccal pouches) has not departed from its primitive position. In the toxoglossans the valve of Leiblein has been lost (Smith, 1967) and may never have evolved past the oesophageal pouch stage. The mid-oesophagus presumably commences immediately behind the buc- cal cavity. This is suggested by the salivary ducts entering the buccal cavity without being attached to the oesophageal walls and by the relative position of the nerve ring. The development of a poison gland by the stripping off of the glandular, mid- oesophageal dorsal folds (Ponder, 1970a), probably took place before the separation of the Terebridae and Conidae from the Turridae. Graham (1941) stated that Nucella and Buccinum must have evolved from different groups because they exhibit dif- ferent positions of torsion in the mid- oesophagus. If this were the case then the Vexillidae (Ponder, 1972b), Marginellidae (Ponder, 1970a) and the Olividae (W.F.P.) must have evolved from a 3rd group, because in all of these families torsion oc- curs just behind the nerve ring (Fig. 1, Е). In the Muricidae, Turbinellidae (Ponder, 1973b), Volutidae (Ponder, 1970b) and possibly the Mitridae (Ponder, 1972b) tor- sion of the gut occurs within the valve of Leiblein (Fig. 1, G), but in Buccinum there is a gradual rotation throughout the mid-oesophagus. There is a similar vari- ability in the position of torsion in the Archaeogastropoda (Fretter & Graham, 1962). The variations in the neogastropods might have resulted from similar varia- tions in the archaeogastropod ancestor that were in evidence before the valve of Leiblein was pulled through the nerve ring. In the Volutomitridae (Fig. 1, E) the oesophageal gland appears to have retreated from the anterior part of the mid-oesophagus and has become stripped off from behind forwards (Ponder, 1972b). Thus it would appear that the divergence of the various rachiglossan families commenced before the main elongation of the proboscis and the associated changes in the foregut and, therefore, before the site of torsion of the gut in each group became a stabilized feature. If these suppositions are correct, similarity in the position of torsion in 2 or more groups would not necessarily in- dicate a close relationship, as it would probably have been evolved independent- ly, 300 There are thus 3 basic organization of the foregut in the Neogastropoda. It is maintained here that each has evolved quite separately and that all were probably derived from an early neogastropod forerunner before the elongation of the snout to form a proboscis. These groupings are: (1) The rachiglossan group in which the dorsal wall of the buccal cavity provided elonga- tion of the oesophagus during the forma- tion of the proboscis; (2) The cancellariids in which the mid-oesophagus is the site of elongation after being pulled through the nerve ring; and (3) The toxoglossan families in which the buccal mass has remained in its primitive position im- mediately in front of the nerve ring, the formation of a proboscis being brought about by the elongation of a tube connec- ting the buccal cavity with the mouth (Fig. В): The 3 types of organization referred to above form 3 natural groups within the living Neogastropoda and will be referred to in the following discussion in parts 1 and 2 as the Conacea, Cancellariacea and Rachiglossa respectively. In part 3 it is sug- gested that the name Muricacea be used for the whole of the Rachiglossa but this usage is avoided at this stage because of the confusion that is likely to arise be- tween the restricted and extended inter- pretations of the Muricacea. The origin of the rachiglossan and toxo- glossan radulae has generally been regarded as a natural progression from the taenioglossan type. However, both the taenioglossan and the stenoglossan radula could have been produced from a reduced rhipidoglossan type. A convenient ancestral stenoglossan radula would have a multicuspid central tooth, a pair of large lateral teeth and a pair or more of marginal teeth in each row (Fig. 2, No. 8). Such a radula could have given rise to the steno- glossan and taenioglossan types. A similar radula with only one pair of marginal teeth is seen in some members of the Clavinae (Turridae). From this type of radula, the rachiglossan and toxoglossan types may have been derived. With the loss of the patterns of W. F. PONDER lateral teeth and the central tooth the nor- mal toxoglossan radula would result. Maes (1971) believes that many turrid radulae have 4 marginal teeth in each transverse row. If this is the case the primitive toxo- glossan radula would have had 2 marginal teeth and may have closely resembled the taenioglossan type. The cancellariid type consists of a single row of peculiar, elongated teeth (see Olsson, 1970), which are probably pes with the central teeth of the remainder of the Neogastropoda. Graham (1941) advanced the hypo- thesis that the oesophageal gland in the Rachiglossa was stripped from the mid- oesophagus, during the elongation of the proboscis, when the valve of Leiblein was dragged forward through the nerve ring (Fig. 1, F, G). The removal of this bulky oesophageal gland left a scar, which shows its original line of attachment. The gland then opens by a narrow duct into the posterior end of the mid-oesophagus. This is a much more satisfactory arrangement in a carnivorous gastropod than the widely open connection seen in most meso- gastropods and archaeogastropods. A narrow duct to the oesophageal gland has evolved independently in the Triphoridae (Fretter, 1951). Possibly the advantages of the possession of a narrow duct precipitated its evolution in the Rachiglossa, rather than the mechanical explanation offered by Graham. The stomach of some neogastropods re- tains a gastric shield and recognizable style sac (Smith, 1967a), and thus resembles those of generalized archaeogastropods, such as Monodonta (Graham, 1949). A pronounced posterior caecum is found in many neogastropod species, which may, in some cases, be a secondary structure, although in others it is probably the rem- nant of a sorting caecum. Graham (1949) summarized the advances of the neogastropod stomach as including (1) the loss of the caecum and therefore the ab- breviation of the major typhlosole and in- testinal groove, (2) the anterior migration of the opening of the oesophagus coupled with its opening into the main gastric cavi- EVOLUTION OF NEOGASTROPODA 301 ty, (3) the loss of the sorting areas, and the disappearance of the gastric shield. These simplifications, Graham concluded, are due to the carnivorous diet of the neogastropods. These features were observed by Graham (1949) in the Muricidae, but Nassarius reticulatus (Lin- naeus) was shown to have a gastric shield, a long posterior caecum and a remnant of a posterior sorting area. Morton (1960) and Brown (1969) recorded a crystalline style in 2 species of the Nassariidae, and Ponder (1972b) noted a prominent gastric shield in the Microvolutidae. Thus some of the features of the archaeogastropod stomach are. present in some groups of neogastropods, whereas in others it has become simplified, or, as in Alcithoe arabica (Gmelin) (Ponder, 1970b), secon- darily complex. An anal (rectal) gland, such as that oc- curring in many Neogastropoda has not been definitely encountered in any Mesogastropoda (Fretter & Graham, 1962, р 233). Simple types do occur in the Archaeogastropoda, in some members of the Trochidae and Scissurellidae (Fretter & Graham, 1962, p 233), where they are actually an enlargement of the intestinal groove or a pouch on the side of the end of the rectum. They apparently have a lubricating function, but it is conceivable that a gland derived in this way could take over an excretory function like that shown for the neogastropod anal gland (Fretter, 1946). The possession of а gonopericardial canal in the male genital system of a few neogastropods is a very primitive feature and this is not shared by any mesogastropod, although some show traces of such a duct (Fretter & Graham, 1962). The development of an ingesting gland from a median sperm pouch must also have been an early development for at least 2 of the superfamilies (Muricacea, Conacea; as here recognized) have this structure. Other evolutionary trends in the neogastropods run largely parallel to those in the mesogastropods. The coiled shell causes a loss of the right auricle, right renal organ and right pallial complex. The right renal organ remains only as an element in the organization of the genital ducts, whereas the pallial glandular parts of the genital ducts may have been derived from the right hypobranchial gland. The reduc- tion and loss of the organs on the right side has allowed the expansion of the left ctenidium, osphradium and hypobranchial gland, and also the migration of the rec- tum to the right side of the pallial cavity. Associated with these changes, the rectum no longer penetrates the ventricle as it does in many archaeogastropods and both structures come to lie on opposite sides of the body. The shell has lost its nacreous layer and the operculum its spiral form. Many of the above changes also took place in the early mesogastropods, so that it is probable that the 2 orders may have been derived from the same archaeogastropod group which was begin- ning to show these tendencies. Separation must, however, have been at a very early stage if this were the case. In summary it is suggested that the neogastropods arose from an archaeo- gastropod, or very primitive mesogastro- pod, for the following reasons: 1. Neogastropods have some organs not found in mesogastropods but known in some archaeogastropods. These include 2 types of salivary glands, a rectal pouch (anal gland of neogastropods) and a gono- pericardial duct in the male reproductive system. 2. The anterior alimentary canal in the mesogastropods and neogastropods differs in the following ways. (a) The salivary ducts pass through the circum- oesophageal nerve ring in mesogastropods and do not in the neogastropods. (b) The valve of Leiblein seems to be derived from the oesophageal pouches of an archaeo- gastropod because in mesogastropods these lie ventrally and the oesophageal valve is lost. (c) The site of elongation of the oesophagus is different in the mesogastropods and in the 3 groups of neogastropods. The Subulitacea have all of the shell features required in an ancestral neogastropod. As well as the loss of the 302 W. Е. PONDER nacreous layer and development of an anterior notch, they have lost the primitive median sinus and many have a columellar fold. Knight, et al. (1960) suggested that this group originated in the Loxonematacea. The adoption of a carnivorous mode of life set the ancestral neogastropods apart from their microphagous forebears. They probably commenced feeding on en- crusting and other colonial animals, a habit seen in some modern archaeo- gastropods, and still found in some neogastropods. The Magilidae, for exam- ple, may have been at first predatory grazers on corals and have now become suctorial, whereas the primitive vexillid genus, Austromitra, is still found to feed on ascidians (Ponder, 1972b). The adoption of a carnivorous habit re- sulted in a complex radiation, in which nearly every marine environment was penetrated. Rapid specialization followed in feeding habits, habitat preferences and morphology, so that the various family groups appear more-or-less simultaneously in the fossil record. The rapid rise in the importance of the neogastropods is paralleled by a similar, but even more diversified, radiation in the mesogastropods (Sohl, 1964). PART 2. EVOLUTIONARY TRENDS IN THE NEOGASTROPODA One of the most significant factors of neogastropod evolution is the well-marked tendency towards parallel evolution of the various organ systems. Each family, equipped as it was with a fundamental neogastropod structure, has shown, de- spite some degree of adaptive radiation, an independent evolutionary tendency towards a similar modification of the inter- nal organs. Their internal structure is, on the whole, rather uniform, but it is sug- gested that the head-foot, shell and radula underwent early adaptive modifications which, from the outset, stamped a distinc- tive pattern on each major group and on the separate families within them. The Shell, Head-foot and Pallial Cavity These 3 parts of the animal will be treated together, as they deal with the ex- ternal environment and are often the first structures to be modified by it. The basic structure of the pallial cavity and head- foot is shown in Fig. 5. The shell in most neogastropods is large, usually fusiform, rather heavy, has a long or short anterior siphonal canal, and usual- ly the animal can withdraw into it com- pletely. The great variability in shell form is found within the Buccinidae and the families allied to it that are included in Thiele's Buccinacea (Fasciolariidae, Nas- sariidae, Galeodidae, Turbinellidae, Colubrariidae and Pyrenidae). The mem- bers of these families are capable of living on hard and soft substrata and their foot is usually of moderate proportions, but in those species found on hard sub- strata the foot is often small (e.g., Buccinu- lum (Bu:cinidae) and many Fasciolariida ) and they generally have a short anterio: siphon. The Nassariidae live mainly on soft substrata and have a larger foot, which reaches a considerable size in Bullia (H. & A. Adams, 1853; Quoy & Gaimard, 1833), and a long siphon. The shell and foot are sometimes well adapted for burrowing (e.g., Cyclope; Morton, 1960). Versatility in ecology is the keynote to the success of these families. The Turbinellidae and some Fasciolariidae have developed columellar plaits as a means of providing additional surface for the attachment of the colu- mellar muscle. The pallial cavity in all of the above families opens in front and on the right side of the animal, but it is not placed as far back on the right as in some of the other families that are modified for burrowing. An exception is seen in the Pyrenidae in which the aperture is often elongate. Although the hypobranchial gland pro- duces copious quantities of mucus and other pale-coloured secretions, no purple fluid is produced in any of the families listed above. EVOLUTION OF NEOGASTROPODA 303 The foot usually bears an operculum, al- though this is lost in some Pyrenidae, possibly because of their elongate con- stricted apertures. The Nassariidae have 2 short tentacles on the posterior end of the foot and the operculum is usually small. The opercular nucleus in all of the above families is usually terminal in position. In contrast with the above families, the Muricidae have solid, strongly or- namented shells which often bear varices, although parallel examples are occasional- ly encountered in the Buccinidae (e.g., Phos, Hindsia). The muricids generally live on hard surfaces so that the foot is usually small. Concholepas peruviana (Lamarck) is limpet-shaped, being the end product of a trend in the “thaid” group to enlarge the aperture and foot as an adap- tation to life on wave-swept shores. The pallial cavity in the Muricidae is unspecialized and is probably the closest to the primitive neogastropod type that exists in the modern neogastropods. A purple hypobranchial secretion is produced by most muricids and has been shown by several workers to contain a poisonous component (reviewed by Halstead, 1965). The siphon rarely projects much be- yond the end of the siphonal canal of the shell, although the canal itself, as in some species of Murex, is occasionally very long. The operculum is usually large and has a terminal, subterminal or lateral nucleus. On the sole of the foot there is an accessory boring organ that secretes an acid and pos- sibly a calcase enzyme which aids in the boring of shells, a feature for which this family is well known (Fretter, 1946; Carriker, 1961, 1967; Smarsh, et al., 1969). The Columbariidae have a small foot and a very long anterior canal projects from the small, round aperture of the shell. The shell often bears 1 or 2 rows of spines; the operculum is large and has a terminal nucleus. Little is known of their habits ex- cept that they mostly occur in deep water. One of the most bizarre neogastropod groups is the Magilidae. This family con- tains genera whose shells resemble those of the Muricidae (e.g., Coralliophila, Tolema), and others in which the shells have become limpet-shaped (e.g., Quoyula) or are embedded in coral and be- come vermiform (e.g., Magilus). The pallial cavity of the Magilidae is similar to that of the muricids, but the osphradium is small (Gohar € Soliman, 1963). The foot in sedentary forms functions as a sucker, aiding in boring the holes in which the animals live (Gohar € Soliman, 1963). In Tolema, which is presumably a free moving member of the family, the foot is similar in size to that of members of the Muricidae (W.F.P.). An operculum with a lateral nucleus is present in members of this family. Thiele's Stirps Volutacea contains an assemblage of unrelated families, most of which are modified, to some degree, for burrowing in soft substrata. These families are the Mitridae, Vexillidae, Volutomitridae, Harpidae, Volutidae, Marginellidae and Olividae. The first 4 families are the least modified, although their shells have long, often narrow aper- tures, an adaptation which culminates in displacing the right angle (exhalant aper- ture) of the pallial cavity far towards the posterior end of the shell. This allows the pallial cavity to function efficiently while the animal is burrowing. The shells of the first 3 families are sometimes elaborately ornamented and are never covered by the mantle or parts of the foot, and the foot is of moderate size only. Some of the genera in the Mitridae and Marginellidae have become adapted to hard substrata but it seems likely that they have been derived from a burrowing ancestral form. In the other families the shell is sometimes sculp- tured, but rarely elaborately, and is usually smooth. By contrast with the earlier families, most Marginellidae and a few Volutidae have the mantle edges overlapping the shell. In these 2 families the pallial cavity has swung completely to the right, the siphon lying immediately above the head and the exhalant aperture opening on the posterior edge of the long body whorl. In most Volutidae the shield-shaped head is formed from the fusion of the tentacle bases, over the rhynchostome. There is 304 W. F. PONDER usually a pair of siphonal lappets, which aid in blocking off the anterior end of the pallial opening. In the Olividae the foot has reached its greatest development. Lateral and anterior flaps from the foot are developed which sometimes enclose the shell completely (e.g., Ancilla, Amalda). Pallial tentacles are sometimes developed, but it appears that the mantle never covers the shell in the Olividae. The eyes are reduced or ab- sent in the Olividae and small in most Volutidae. The foot in the Olividae is usually divided into an anterior segment (propodium) and a large posterior portion (metapodium). Wilson (1969) has shown how the propodium is used as a swimming organ in Ancillista cingulata (Sowerby). D Orbigny (1841) recorded swimming ac- tivity effected by movement of the metapodial flaps in Oliva tehuelchana (d’Orbigny), and Olsson (1956) and Mar- cus & Marcus (1959) reported the same type of swimming in Olivella species. The Harpidae have a very large foot which has a distinct propodium, as in the Olividae, but the shell is not covered by the animal (Quoy & Gaimard, 1833). The columellae of all of the families in this burrowing group of families, except the Harpidae and Olividae, usually have strong plicae, whereas the latter 2 have weak plaits. Usually the foot is large in the Volutidae, Olividae, Harpidae and Marginellidae and the operculum lost, although this is retained in some Olividae and a few Volutidae. A purple hypo- branchial secretion occurs in at least some mitrids and volutes. The enlargement of the foot, and par- ticularly its encroachment on the shell in the Olividae, has resulted in loss of the ver- satility of movement seen in the Buc- cinidae and its allies. The Cancellariidae have neither the foot nor the mantle cavity particularly modified. They have all lost the oper- culum and the shell is sculptured, ovate, and usually has columellar folds. Little is known about the habits of this family. The conacean families have only 1 over- all distinctive feature of the shell, and that is the presence of a posterior sinus in the aperture. The shell of the Turridae is often spindle-shaped, with a long or short anterior canal. The turrids appear to match the Buccinidae in versatility of habitat but, although there are a great number of species, they are rarely in- dividually abundant, and in particular are lacking in the intertidal zone. The Conidae, on the other hand, are often abundant as individuals and also live on both hard and soft substrata. Their shells are cone-shaped, usually smooth, and the spire is usually very short. In the sand burrowing Terebridae the shell has a long, slender spire, and it is smooth or weakly sculptured. The foot in the majority of conacean species is small, and the head in the Conidae and Turridae bears prominent eyes, which are often situated near the tips of the tentacles. The eyes and tentacles are usually reduced or lost in the Terebridae and at least some species in this family pro- duce a purple hypobranchial secretion. The parallel evolution of shell features has often resulted in a confused taxonomy. Several families have developed members that have a superficial resemblance to genera in other families. Some examples are the overall resemblance of the Mitridae, Vexillidae and Volutomitridae, the similarity of some Muricidae (e.g., Uttleya) to the Buccinidae and the resemblance of genera such as Phyllo- coma (Muricidae) and Colubraria (Colubrariidae) to the Cymatiidae (Ton- nacea). The Alimentary Canal The basic lay-out of the rachiglossan alimentary canal is shown in Fig. 5. The feeding habits of the majority of groups are not discussed here, but a detailed sum- mary is given by Purchon (1968). The Proboscis: The proboscis in the Rachiglossa is always of the pleurembolic type and this form is also found in the Cancellariacea (Graham, 1966). The proboscis is usually relatively short and broad in the small species of every family, but in the larger species noticeable dif- ferences occur. Those families which EVOLUTION OF NEOGASTROPODA 305 specialize in grasping the prey with the foot (Olividae, Volutidae) and the Muricidae (which must use the pedal accessory boring organ in conjunction with the buccal mass in order to drill the shell of their prey) have a short proboscis. The Buccinidae, Nassariidae, Galeodidae and Fasciolariidae usually have а long proboscis and the walls of the proboscis sac are normally capable of almost complete introversion. This also applies to Vasum in the Turbinellidae, but in Tur- binella the very long, slender proboscis is coiled in a wide, thin walled sac which is not capable” of introversion (Ponder, 1973b). A similar sac with an even longer proboscis is found in Columbarium spp. and Coluzea spp. in the Columbariidae (W.F.P.), whereas an intermediate type is seen in Ratifusus reticulatus (A. Adams) (=mestayerae Iredale), in the Colubrariidae (Ponder, 1968) and in some Mitridae (Ponder, 1972b). The species with a long proboscis can “feed at a dis- tance’ and are thus capable of preying on animals that live in crevices, narrow holes and tunnels. If additional length is required in a proboscis that is already packed into the cephalic cavity, the sheath must become a wide sac to accommodate the longer, and of necessity, narrower proboscis. The 2 specialized types of proboscis in the Turridae that were described by Smith (1967) can be derived from a more basic type which also occurs within the family. In the primitive subfamilies that extend back into the Paleocene, the Turrinae, Borsoniinae and the Clavinae, and the even earlier Turriculinae (Powell, 1966) (the Conorbiinae has not been examined by the writer) there is a simple intraem- bolic proboscis within a wide rhynchodeum (proboscis sac). The long tube, characteristic of the Conacea, traverses the proboscis from the buccal cavity at its base. In Splendrillia debilis Finlay (Clavinae), Comitas onokeana vivens Dell (Turriculinae) and Epidirona gabensis (Hedley) (Turrinae) the proboscis is of moderate size compared with the rhynchodeum, but in Borsonia sp. and Scrinium neozelanicum (Suter) (Bor- soniinae) it is more elongate (W.F.P.). This type also occurs in the Conidae (Alpers, 1931; Shaw, 1915) and in Terebra cancellata (О. € С.) (Risbec, 1953) and it presumably gave rise to the advanced type of intraembolic proboscis (Smith, 1967) by the invagination of the distal end seen in Parabathytoma luhdorffi (Lischke) in the Borsoniinae (W.F.P.). Many species of Mangeliinae have the advanced, intra- embolic type of proboscis (Robinson, 1960; Smith, 1967; W.F.P.) and some Conidae have also developed it (Amaudrut, 1898). It is characterized by a method of proboscis retraction not found in the other 2 neogastropod superfamilies. Another development from the primi- tive toxoglossan proboscis resulted in the reduction of the proboscis and an in- creased emphasis on the development of the mobile lips of the rhynchostome. Intermediate stages in the development of the polyembolic (Smith, 1967) type of proboscis can be seen in some turrids, in which the relatively small original proboscis fills only half of the rhynchodeum in the contracted state. A very powerful sphincter surrounds the long, narrow rhynchostomal opening which is often produced into a snout. This condition is seen in some advanced Clavatulinae (Phenatoma rosea (Quoy € Gaimard) and Maoritomella albula (Hut- ton) (W.F.P.)) and in Pontiothauma spp., in the Daphnellinae (Pace, 1903). The final stage of this development, in which the rhynchostome forms a pseudoproboscis (Rudman, 1969) which can be inverted, is generally associated with the shortening of the original proboscis. In some species however, the 2 structures, both of moderate length, coexist (Philbertia pur- purea (Montagu) (=boothi Wood); Smith, 1967; and Hastula cinerea (Born); Marcus & Marcus, 1960). Species in which the original proboscis has become atrophied include Philbertia leufroyi (Michaud) (Mangeliinae); Cenodagreutes spp. (Smith, 1967), Daphnella cancellata (Hut- ton) (W.F.P.) (Daphnellinae), Terebra maculata (Linnaeus) and certain other 306 W. F. PONDER species of the Terebridae (Rudman, 1969). Terebra maculata has the pseudoproboscis greatly developed, so that it is folded into the rhynchodeum. The pseudoproboscis or polyembolic proboscis is thus a new structure developed from the rhynchostome and is not homologous with the original neogastropod proboscis. Whereas the original proboscis was developed by the elongation of the archaeogastropod snout, in the Conacea a new elongation of the “pseudosnout has resulted in a “pseudo- proboscis. | Since the above was written Miller (1971) has produced a preliminary report on his work on the feeding mechanisms of the Terebridae. He shows that there are 3 main types of feeding mechanism in this family. Туре 1 has a pseudoproboscis, salivary glands and а short proboscis. There is no poison gland or radula. Type 2 are typically toxoglossan having a long proboscis, a poison gland and a radula. Туре 3 has а peculiar accessory feeding organ consisting of a “long posterior glan- dular and muscular stalk, terminating anteriorly in a series of muscular papillae. ” This type does not have a radula or poison glands and many have lost the salivary glands and buccal tube as well. Rudman (1969) has described a 4th type in Pervicacia tristis (Deshayes) which is similar to Miller s Ist type but differs in the possession of a radula with an odon- tophore. The loss of salivary glands, poison gland and radula is sometimes associated with the development of the polyembolic type of proboscis or pseudoproboscis ( Terebra maculata (Rudman, 1969), Cenodagreutes spp. (Smith, 1967)). The Buccal Cavity and Salivary Glands: The buccal cavity, although showing a general uniformity throughout the Neogastropoda, has been modified т some families. The mouth opens directly into the buccal cavity in most families, but is surrounded by a peristomial rim in the Muricidae (Carriker, 1943) and Mitridae (Ponder, 1972b). There is a long oral tube in the Vexillidae (Ponder, 1972b), and the Cancellariidae (Graham, 1966). No true jaws are found in the Neogastropoda, but members of the Muricidae have a median, dorsal, jaw-like sclerite (Carriker, 1943; Wu, 1965). In the Magilidae the buccal cavity appears to extend to the base of the proboscis and the odontophore and radula have disappeared. In this family the buccal cavity is used as a pump in feeding on the coelenterate prey (Ward, 1965). A minute buccal apparatus is found in some Colubrariidae (Ponder, 1968), the Har- pidae (Bergh, 1901), and Vitularia in the Muricidae (W.F.P.), and Coluzea in the Columbariidae (W.F.P.). The conacean families have a long tube leading from the buccal cavity which lies at the base of the proboscis but not at its distal end as in the Rachiglossa. In this group many species lose the muscular odontophore and, although this is retained in several primitive genera (W.F.P.), it seems unlike- ly that it is ever protruded from the mouth, as in rachiglossans. The duct of the unpaired foregut gland in the Rachiglossa and its toxoglossan homologue, the poison gland, opens into the buccal cavity in the Conacea and in some Marginellidae (Graham, 1966; Ponder, 1970a). A few terebrids (Troschel, 1856-1893; Bouvier, 1887; Risbec, 1953) and turrids (Smith, 1967), have lost the radula, salivary glands and poison gland. Many neogastropods possess 2 types of salivary gland (see Fig. 1) or buccal glands (Hyman, 1967). One type is homologous with the “nor- mal’ salivary glands (sg) of most other gastropods. These are white, usually paired, often irregular, bodies composed of masses of minute tubules made up of cuboidal secreting cells. Their ducts usual- ly open laterally into the buccal cavity. These glands will be referred to in the following discussion as “salivary glands.’ The 2nd type of salivary gland, often termed accessory salivary gland (asg), usually consists of a pair of elongate vesicles containing the secretion рго- duced by glandular tissue adhering to their outsides. They open by way of a very EVOLUTION OF NEOGASTROPODA 307 narrow duct at the anterior end of the buc- cal cavity. Nearly all neogastropods have salivary glands. These glands are usually massive in the Muricidae and Mitridae, as well as in the Buccinidae and its allied families. In these groups there are usually 2 types of cells making up the glandular epithelium (Dakin, 1912 (Buccinum); Fretter & Graham, 1962 (Nassarius); Ponder, 1972b (Strigatella); W.F.P. (Taron, Cominella) and Wu, 1965 (Drupa, Morula)). They are also large in the Turbinellidae (Ponder, 1973b) but their histology has not been examined. The salivary glands of the VolmtidaecesPonder. 1970b)0.the Marginellidae (Ponder, 1970a), the Micro- volutidae, the Vexillidae (Ponder, 1972b) and the Olividae (Marcus & Marcus, 1959) are composed of more-or-less discrete tubules, in which there is only 1 type of secretory cell, and the entire gland is often small. The salivary glands of the Conacea are frequently rather small, and sometimes are reduced to a single gland with only 1 duct (which may be 2 fused ducts), as in Conus lividus (Briig.)(Alpers, 1931). There is only 1 type of gland cell present and in Conus it is tall and vacuolate (Alpers, 1931), but in the Turridae it is like the normal neogastropod salivary cell (W.F.P.). The cancellariids have long, narrow salivary glands that lie within the proboscis (Bouvier, 1887; Amaudrut, 1898; Graham, 1966). The salivary ducts often lie beneath the dorsal folds in the oesophageal wall, but are free in some Buccinidae, Nassariidae, Mitridae and Olividae and in the Conacea and Cancellariacea. They usually open into the posterior end of the buccal cavity above the opening to the radular sac, but in the Pyrenidae (Marcus & Marcus, 1962a) and Conacea (Smith, 1967) they open into this sac. In the Pyrenidae the salivary ducts sometimes form a small vesicle just before they open. In the Volutomitridae and Vexillidae (Ponder, 1972b) the ducts migrate ven- trally to open on the buccal floor and in the Mitridae (Ponder, 1972b) they are pro- jected in front of the mouth by an epiproboscis. In Olivella (Marcus & Mar- cus, 1959) the salivary ducts open at the anterior end of the buccal cavity and in Coralliophila abbreviata (Lamarck) they unite dorsally before entering the buccal cavity (Ward, 1965). The accessory salivary glands consist of a vesicle lined with columnar epithelium in the Muricidae (Bouvier, 1888: Fretter & Graham, 1962; Wu, 1965) and squamous epithelium in the Olividae (Kiittler, 1913) and the Volutidae (Ponder, 1970b). This epithelium is surrounded by a layer of cir- cular and some longitudinal muscles, and these are penetrated by the ducts of gland cells lying outside the muscles. The glan- dular layer consists of 1 or more layers of irregular, subepithelial cells and the secre- tion fills the vesicle of the gland. Paired accessory salivary glands have been recorded in the above families and in Фе Vexillidae (Risbec, 1928; Ponder, 1972b) and the Cancellariidae (Amaudrut, 1898; Graham, 1966), but are not found in the Mitridae (Risbec, 1928; Ponder, 1972b), Harpidae (Bergh, 1901), Terebridae (Risbec, 1953; Marcus & Mar- cus, 1960) and most Turridae (Smith, 1967; W. Е. P.), although the writer has located them in 2 species of the Bor- soniinae. None of the families that are generally regarded as related to the Buc- cinidae possess them (Dakin, 1912; Thiele, 1929), including the Pyrenidae (Risbec, 19542 Marcus). do.) Miareus..1 19623) Galeodidae (Pierce, 1950; W.F.P.), Nassariidae (Bouvier, 1888; Risbec, 1952; Graham, 1941), Fasciolariidae (Marcus & Marcus, 1962) and the Colubrariidae (Ponder, 1968). The Columbariidae (W.F.P.), Turbinellidae (Moses, 1923; Ponder, 1973b) and the Magilidae (Bouvier, 1888; Ward, 1965; W.F.P.) also lack them, whereas in the Volutomitridae (Ponder, 1972b) and the Marginellidae (Ponder, 1970a) a single gland is present, though it is sometimes absent in the latter family. The function of the accessory salivary glands 15 still obscure. Bouvier (1888) found it in all of the Muricidae that he 308 W. F. PONDER examined, it being very minute in Murex trunculus( Linnaeus), larger but embedded in the normal salivary glands in Trophon philippianus Dunker and very large in Ocenebra erinaceus (Linnaeus) and Nucella lapillus (Linnaeus). The ability to bore into shells is best developed in Nucella and Ocenebra and so, in this fami- ly, its size may be correlated with the animals feeding habits. Wu (1973) has shown that at least 2 muricids lack these glands. However none of the other families that possess it have so far been shown to have the ability bore into shells, but the structure of the gland nearly identical in all, except for the difference in the internal epithelium in the Muricidae mentioned above. Several workers have tested the secre- tion of the accessory salivary gland and have failed to find anything significant. The salivary glands of some Muricidae contain proteolytic enzymes (Mansour- Bek, 1934) and a toxic secretion has been recorded in some Buccinidae (Welsh, 1956; Fange, 1960). The Radula: There is an overall tenden- cy toward reduction of the number of radular teeth and their cusps in most of the families of the Neogastropoda, as also oc- curs in the Opisthobranchia. Examples in- dicating this trend are shown in Fig. 2. The inner circle shows а hypothetical ancestral type of radula. The next zone (A) includes examples of multicuspate radulae, showing the maximum number of teeth present in each family. The maximum number found in all the Rachiglossa is 3 teeth in each row, but some of the Clavinae (Turridae) in the Conacea have 5 teeth in each row (No. 20). Some families are not represented in this zone (A), but this does not necessarily in- dicate that the radular teeth in families such as the Muricidae are any more specialized than those included in the in- ner zone. The diagram indicates trends and is not necessarily of phylogenetic significance. Zone B includes those radular teeth that show some simplification or modification from a more basic pattern. Some are assumed to be secondarily multicuspid such as Olivella (No. 16), and Vexilla (No. 32). The Olivellinae (Olividae) (No. 16) and the Nassariidae (Nos. 43, 45) often develop accessory plates between the cen- tral and lateral teeth. These are probably independently evolved, new structures be- cause they occur in all stages of develop- ment in both groups. The variation in radular pattern in the Buccinidae, and the general similarity in the teeth of all of the families included in Thiele’s Buccinacea, should be noted. The radular teeth shown in zone C are those in which the number of teeth has become reduced. In the Mitridae, Volutidae, Marginellidae, Volutomitridae and Cancellariidae the lateral teeth have been lost, but in the Buccinidae, Pyrenidae and the toxoglossan families the central tooth has disappeared. The lateral teeth in some Harpidae (Peile, 1939) and Volutidae (Pace, 1902) are vestigial, whereas in the Pyrenidae the large lateral teeth may func- tion as tweezers (Marcus & Marcus, 1962а). The marginal teeth of advanced toxoglossan genera (Nos. 25-27) are hollow and capable of being charged with poison. They are used as harpoons in the capture of active prey (Kohn, 1959; Pearce, 1966) which is then swallowed whole. Some Conacea have more primitive radulae that probably function in tearing the prey (Nos. 21, 28), while the “prototypic” type in the Clavinae (No. 20) is probably capable of combining a food tearing and a spearing function. There are undoubtedly other methods of employing the varied types of radula (Nos. 22, 23) within the Turridae. The Cancellariidae have a single row of elongated, blade-like teeth (Barnard, 1958; Graham, 1966), each an aggregate of “rectangular tubes which form a canal system which transverse the whole length of the radular filaments’ (Olsson, 1970). Several families have lost the radula altogether, these being indicated in the outermost zone (D). Only the Magilidae have no known members with a radula. Some of these “aglossate” forms are probably suctorial feeders (Magilidae, EVOLUTION OF NEOGASTROPODA 309 Marginellidae), whereas others (Terebridae, Turridae) probably engulf their prey whole. It is not known how the Cancellariidae feed, although Olsson (1970) suggests that they may feed on micro-organisms, these being transported down the minute tubes that make up each tooth. The Mid-oesophagus and Сапа of Leiblein: The evolution of the mid- oesophagus (mo) in the Rachiglossa follows 2 main trends, which run parallel in several families. These are (1) the strip- ping off of the gland of Leiblein and oesophageal dorsal folds from the oesophagus to form a “poison gland” and (2) the loss of the original, glandular oesophageal dorsal folds. Both of these trends have ultimately resulted in genera that have lost all of the glandular struc- tures associated with the mid-oesophagus. The oesophageal gland attached by a narrow duct is usually referred to as the “gland of Ге ет.” Hyman (1967) uses the name “unpaired foregut gland.” In order that the following discussion be clarified the use of these terms will be strictly defined. The unpaired foregut gland can be used for the unpaired gland which enters the oesophagus by way of a narrow duct. This can include the poison gland of the conaceans, as I have recently shown (Ponder, 1970a) that it is probably homologous to the unpaired foregut gland of the rachiglossans. The gland of Leiblein can be used for that part of the unpaired foregut gland that was derived from the oesophageal gland. In some species the unpaired foregut gland consists solely of the gland of Leiblein but in others it in- volves other parts of the oesophagus, as is shown below. Fig. 3 shows the evolution of the rachiglossan mid-oesophagus. A and В show a generalized type of mid- oesophagus (although not necessarily the most primitive) which is encountered in several families as the least specialized type. The unpaired foregut gland consists only of the small gland of Leiblein (gl). The mid-oesophagus (mo) is moderately long (A), or short (B) and has glandular dorsal folds and a prominent valve of Leiblein (vl). The type shown in diagram A occurs in the Volutidae (Volutocorbis abyssicola (Adams & Reeve); Woodward, 1900) and the Vexillidae (Austromitra rubiginosa (Hutton); Ponder, 1972b), but in some Olividae (Oliva sayana Ravenel and Olivancillaria (Lintricula) auricularia (Lamarck); Marcus & Marcus, 1959) the mid-oesophagus is shorter, as in diagram B. The unpaired foregut gland increases in bulk in the Muricidae (diagram C) but still usually only consists of the gland of Leiblein. The mid-oesophagus is some- times short but still contains the glan- dular dorsal folds (Graham, 1941; Wu, 1965). The “Trophoninae,” probably the most primitive of the muricid groupings, has the smallest gland of Leiblein. In the Columbariidae (W.F.P.) and the Magilidae (Ward, 1965; W.F.P.) the dorsal folds are not glandular, but the valve of Leiblein is large (diagram D). In the families Buccinidae (Dakin, 1912; Graham, 1941), Nassariidae (Graham, 1941; Risbec, 1952), Fasciolariidae (Mar- cus & Marcus, 1962), Pyrenidae (Risbec, 1954; Marcus & Marcus, 1962a) and Tur- binellidae (Ponder, 1973b), the dorsal folds are lost or have become т- conspicuous, the valve of Leiblein 15 sometimes reduced in size, and the un- paired foregut gland (entirely gland of Leiblein) remains small and sometimes becomes very thin walled and saccular (diagram E). Busycon canaliculatum (Lin- naeus) (Pierce, 1950) and B. contrarium Conrad (W.F.P.) in the Galeodidae are organized like the Buccinidae, but some members of the Galeodidae (Melongena melongena (Linnaeus) Vanstone, 1894; M. corona (Gmelin; W.F.P.) have lost the gland of Leiblein (diagram F). In Melongena the valve of Leiblein is much reduced and a caecum-like expansion lies just behind the nerve ring which may be homologous with a similar, short caecum found in the anterior part of the posterior oesophagus in Buccinum undatum and 310 W. F. PONDER FIG. 2. The evolutionary trends in the neogastropod radula. Levels A to D are explained in the text. Mitridae (1) Cancilla (Domiporta) sp. (Cooke, 1920); (2) Scabricola desetangsii (Kiener) (=variegata Reeve) (Cooke, 1920); (3) Pterygia crenulata (Gmelin) (Thiele, 1929). Volutidae (4) Volutocorbis abyssicola (Ad. & Rve.) (Thiele, 1929); (5) Voluta musica Linnaeus; (6) Scaphella junonia Shaw (Clench & Turner, 1964); (7) Alcithoe arabica (Gmelin) (original). (8) Hypothetical ancestral radula. Marginellidae (9) Diluculum inopinatum Barnard (Barnard, 1962); (10) Persicula persicula (Linnaeus) (Thiele, 1929); (11) Volvarina (Haloginella) philippinarum (Redfield) (Troschel, 1868). Volutomitridae (12) Paradmete typica Strebel (Thiele, 1929); (13) Microvoluta australis Angas (Peile, 1922). Olividae (14) Pseudoliva crassa (Gmelin) (Thiele, 1929); (15) Oliva sayana Ravenel; (16) Olivella verreauxii (Duclos) (Marcus € Marcus, 1959). Harpidae (17) Harpa amouretta (Róding) (Peile, 1939). Vexillidae (18) Vexillum sp.; (19) Pusia sp. (original). Turridae (20) Drillia umbilicata (Gray) (Thiele, 1929); (21) Hormospira maculosa (Sowerby) (Powell, 1942); (22) Aforia goodei persimilis (Dall); (23) Polystira picta (Reeve); (24) Inquisitor cf crennularis (Lamarck) (Powell, 1966); (25) Phenatoma rosea (Quoy & Gaimard) (Thiele, 1929). Conidae (26) Conus (Asprella) mucronatus Reeve (Thiele, 1929 (after Bergh)). Terebridae (27) Hastula (Impages) coerulescens (Lamarck) (Troschel, 1866); (28) Diplomeriza duplicata (Lin- naeus) (Troschel, 1866). Cancellariidae (29) Cancellaria sp. (original). Columbariidae (30) Columbarium pagodum (Lesson) (Habe, 1943). Muricidae (31) Bedeva hanleyi (Angas); (32) Vexilla taeniata (Powis) (Thiele, 1929). Turbinellidae (33) Turbinella ovoideus (Kiener); (34) Vasum ceramicum (Linnaeus) (Thiele, 1929). Columbellidae (35) Pseudanachis duclosiana (Sowerby) (Thiele, 1929); (36) Pyrene (Strombina) gibberula (Sowerby) (Troschel, 1869, after Moerch); (37) Paxula paxillus (Murdoch) (original). Buccinidae (38) Proneptunea duplicarinata Powell (Powell, 1951); (39) Liomesus dalei (Sowerby) (Thiele, 1929); (40) Mohnia mohni Friele (Thiele, 1929 after Kobelt); (41) Buccinum undatum Linnaeus (Troschel, 1868); (42) Meteuthria martensi (Strebel) (Thiele, 1929). Nassariidae (43) Cyclope neritea (Linnaeus) (Troschel, 1868); (44) Ilyanassa obsoleta (Stimpson) (Troschel, 1869); (45) Cyllene lyrata (Lamarck) (Thiele, 1929). Fasciolariidae (46) Peristernia australiensis (Reeve) (Thiele, 1929); (47) Granulifusus niponicus (Smith) (Habe, 1945). Melongenidae (48) Semifusus (Pugilina) тото (Linnaeus) (Thiele, 1929). Colubrariidae (49) Iredalula striata (Hutton) (Ponder, 1968). Neptunea antiqua (Linnaeus) (Fretter & been partially stripped from the mid- Graham, 1962). The Mitridae (Risbec, 1928; Ponder, 1972b) have no unpaired foregut gland and the valve of Leiblein and dorsal folds are inconspicuous. In Harpa (Bergh, 1901; W.F.P.) the mid-oesophagus has lost all trace of the valve and unpaired foregut gland and of the dorsal folds (diagram P). The mid- oesophagus of the Colubrariidae (Ponder, 1968) has become secondarily elongate and glandular after the loss of the un- paired foregut gland (diagram С). The mid-oesophagus is very long in the muricid Poirieria zelandica (Quoy & Gaimard) (W.F.P.) and the glandular dor- sal folds are conspicuous (diagram H). In Murex tenuispina Lamarck (=M. pecten Lightfoot) (Haller, 1888) and in Vexillum spp. (Ponder, 1972b) the dorsal folds have oesophagus (diagram I) by the fusion of their apices. This process has proceeded still further (diagram J) in Xymene am- biguus (Philippi), Paratrophon quoyi quoyi (Gray) (Muricidae), Amalda (Baryspira) australis (Sowerby) (Olividae) (W.F.P.) and in most Volutidae (Clench & Turner, 1964; Ponder, 1970b). In these species the dorsal folds have been stripped from the mid-oesophagus up to the edge of the nerve ring. The resultant glandular tube lies, as a more-or-less convolute mass, anterior to the gland of Leiblein (sensu stricto). The whole structure (the unpaired foregut gland) is usually referred to as the gland of Leiblein, but in fact, the part derived from the dorsal folds (the tubular part) is the main secretory area. The gland of Leiblein itself (the terminal bulbous part) is merely a muscular appendage with EVOLUTION OF NEOGASTROPODA 311 Melongenidae Colubrariidae 1 4 NM Buccinidae 41 / VAS eS И Nie 43 1 1 y Se Я Pyrenidae м 34 NZ in и “Ay Muricidae Turbinellidae Magilidae a rather thin epithelium which appears to have hardly any functional significance. The Volutomitridae (diagram K) appear to have derived the gland of Leiblein from the oesophageal gland in a different fashion from other Rachiglossa (Ponder, 1972b). It appears to have been stripped from the oesophagus forwards, rather than backwards. This family has several features in common with the Marginellidae, and if it is possible that they both had a common origin, the gland of Leiblein in the Marginellidae may have arisen in the same way as Volutomitridae. There is, however, no direct evidence to support this assumption eo Columbariidae in the Mitridae Volutidae Ÿ I “ Marginellidae BIN < > NA er ee Ro 9 © yf, 5 Volutomitridae 1] Sera À \ \ DI Olividae E \ < 15 \ \ \ ‘ ‘ 17 Ws ca 26 pike ae Sy) DM нае 18 er Y ) ON о Vexillidae № ‘ A A / de 74 . 4 . 4 ee | / = / я К uf À zi \ 22 Ay in 7 97 Terebridae 21 ER \ ys Cancellariidae (Ponder, 1970a). In the most primitive marginellid examined (Diluculum sp. ), the small gland of Leiblein has been stripped from the mid-oesophagus (diagram L), to which it is attached by only a narrow duct (Ponder, 1970a). The following stages in the evolution of the marginellid unpaired foregut gland have been described in detail elsewhere (Ponder, 1970a). Briefly it includes the formation of a pre-torsional tube that bypasses the valve of Leiblein (diagram L) and, following this, the com- plete stripping off of the dorsal folds along the remainder of the mid (diagrams M, N) and anterior oesophagus (diagram О). Thus a separate tube is formed which 312 W. F. PONDER opens directly into the buccal cavity (diagram О). The formation of a poison gland in the Conacea probably occurred in a similar fashion to that in the marginellids. In the Conacea, however, there is either a very short anterior oesophagus or this is absent altogether, so that the process would be simplified. Evidence in support of the poison gland having formed in this way is provided by the lack of any reports of oesophageal dorsal folds in the Conacea. A detailed account of the structure of the poison gland of Conus mediterraneus (Briig.) was given by Martoja (1960). The nature of the mid-oesophagus in the cancellariids is described above. Graham (1941) suggested that because of the different position of the scar in- dicating the path of torsion in Buccinum and Nucella, the Muricacea and Buc- cinacea must have had different origins. The scar in Buccinum shows torsion oc- curring in that part of the oesophagus FIG. 3. The evolutionary trends in the mid-oesophagus of the Muricacea. The gland of Leiblein is shown stippl- ed and the mid-oesophagus and the valve of Leiblein are hatched. The valve of Leiblein and the glandular parts of the mid-oesophagus are indicated as broader portions of the mid-oesophagus. For explanation, see text. EVOLUTION OF NEOGASTROPODA 313 which passes through the nerve ring, and Marcus & Marcus (1962) have shown a similar type in the Fasciolariidae. Most Buccinidae, Pyrenidae (Marcus & Marcus, 1962a), Olividae (Marcus & Marcus, 1959) and Nassariidae (Graham, 1941) do not show the path of torsion. The same is true for the Mitridae (Ponder, 1972b), although there is some indirect evidence that it oc- curs at the site of the valve of Leiblein, as it does in the Muricidae (Graham, 1941), Volutidae (Ponder, 1970b) and Tur- binellidae (Ponder, 1973b). А 3rd type which probably represents a modification of that seen in the Buccinidae, shows tor- sion occurring just behind the nerve ring. This is seen in the Marginellidae (Ponder, 1970a), Vexillidae (Ponder, 1972b) and in the Olividae (Amalda (Baryspira) australis, W.F.P.). The Volutomitridae have had the anterior part of the mid-oesophagus pulled through the nerve ring so that the position of torsion now lies a little behind the valve of Leiblein, whereas, originally it probably lay just behind the nerve ring (Ponder, 1972b). The secretion of proteases by the un- paired foregut gland has been investigated in Murex (Mansour-Bek, 1934; Hirsch, 1915), Buccinum (Brock, 1936) and Babylonia (Yamaguchi, et al., 1961). Studies by Kohn, et al. (1960) and Whyte € Endean (1962) have been made on the chemical and pharmacological properties of the venom of Conus and a summary of this work, together with some new infor- mation, is provided by Halstead (1965). The pyriform valve of Leiblein is a characteristic feature of the Rachiglossa. A reduction in its size is often associated with a small unpaired foregut gland (as in Buc- cinum) and when this gland is absent the valve is either very small or completely missing (Melongena, W.F.P.; Harpa, Bergh, 1901; Mitridae, Ponder, 1972b). Alternatively if the oesophagus 1$ Бу- passed by the unpaired foregut gland, as in the Conacea and in some Marginellidae, the valve of Leiblein is lost (Smith, 1967; Graham, 1966; Ponder, 1970a). Thus the main function of the valve is probably to retain the enzymatic secretion from the unpaired foregut gland and from the glan- dular dorsal folds within the mid and posterior oesophagus. The Stomach: Graham (1949) outlined the features of the neogastropod stomach, which he based on a study of Nassarius reticulatus (Linnaeus), Nucella lapillus (Linnaeus) and Ocenebra erinacea (Lin- naeus). Smith (1967a) suggested that 2 evolutionary trends were represented in the stomachs of the neogastropods that he investigated. He found that in the buc- cinids and the turrids the stomach in- dependently takes on a U-shape. The neogastropod stomach has, in fact, evolved in several different ways. The anterior migration of the oesophagus has occurred in all groups, resulting in a basically U- shaped stomach. Many neogastropod stomachs (see Fig. 5) have primitive features not found in higher mesogastropods. This is especially noticeable in the Nassariidae (Graham, 1949; Smith, 1967a) and the Pyrenidae (Marcus & Marcus, 1962a), both of these families having species which still retain the gastric shield, style sac and vestiges of a sorting area. The tendency to form а spacious posterior caecum (с) occurs in several groups, all of which have a distinct style sac area (ss) with recognizable typhlosoles. These include Neptunea antiqua (Smith, 1967a) and Buccinum undatum (Brock, 1936) in the Buccinidae, and the Nassariidae (Graham, 1949; Morton, 1960; Smith, 1967a), it being especially pronounced in Nassarius (Alectrion) aoteanus Finlay (W.F.P.). Morton (1960) has shown that a crystalline style occurs in Cyclope neritea (Linnaeus), whereas Jenner (1956) and Brown (1969) have reported one in Nassarius (Ilyanassa) ob- soletus (Say). Oliva sayana Ravenel has a caecum, but in Olivella verreauxii (Duclos) this has been transformed into a cuticle lined gizzard (Marcus & Marcus, 1959). A gizzard is also found in the Mitridae (Ponder, 1972b) but in this family it is formed in the oesophageal region of the stomach, there being no caecum. The Vexillidae (Ponder, 1972b) have a broad 314 W. Е. PONDER caecum, and so does Peculator hedleyi (Murdoch) in the Volutomitridae (Ponder, 1972b). In the above examples having a caecum, the digestive gland apertures open near the entrance of the oesophagus. Cominella spp., Buccinulum spp., Austrofusus glans (Röding) (W.F.P.), and Penion adustus (Philippi) (Ponder, 1973a) in the Buc- cinidae and Microvoluta biconica (Mur- doch & Suter) in the Volutomitridae (Ponder, 1972b) do not have a caecum. A prominent gastric shield is present in some Nassariidae, some Pyrenidae, and in the Volutomitridae, but certain other families have examples which show remnants of this structure. А general tendency for the gastric Nassariidae Fasciolariidae Pyrenidae Columbariidae pr, os) | - || | / lumen (1.е., the stomach cavity excluding the style sac) to elongate is seen in Cominella (W.F.P.) and Colus gracilis (da Costa) (Smith, 1967a) in the Buccinidae and «Taron ‘dubius (М. EAP?) and Leucozonia nassa (Gmelin) (Marcus & Marcus, 1962) in the Fasciolariidae. In these examples the 2 digestive gland aper- tures have become widely separated and lie at each end of the gastric lumen. This tendency is increased in Penion (Ponder, 1973a) and Buccinulum (Buccinidae) (W.F.P.) in which the gastric lumen ос- cupies most of the stomach and is, itself, U-shaped. In the Buccinidae the oesophagus opens into the stomach behind the intestine, but in the Colubrariidae (Ponder, 1968) it Buccinidae Melongenidae Colubrariidae \ Turbinellidae “ N N N Mitridae y „ - О \ | N Vexillidae is Muricidae Г DS 1 < 1 PEN \ 1 IS N Г \ - 7 Volutomitridae Magilidae a x iS E Mar ginellidae Ca Volutidae i aa ae is = Er Olividae Harpidae FIG. 4. The evolution of the families of the Muricacea. The inner, solid circle represents the lower Mesozoic, ancestral neogastropod group. The middle circle indicates the boundary of the Mesozoic and Tertiary Periods. The relative size of each family at the edge of the outer circle is approximately proportional to the total number of Recent and fossil genera within each group. No attempt has been made to show the proportions of the genera throughout the Tertiary Period. EVOLUTION OF NEOGASTROPODA 315 opens at the anterior end of the very elongate stomach, which has the intestine opening posteriorly and the style sac is lost altogether. Narrow, superticially U-shaped stomachs have been evolved in the Turridae (Smith, 1967a) and the Terebridae (Marcus & Marcus, 1960), but in these families the wide oesophagus oc- cupies most of the left side of the U, whereas the right side is derived from the style sac. In the Turbinellidae (Ponder, 1973b) the style sac area occupies nearly all of the U. The muricid stomach has evolved a bag- like, posterior swelling which is, in reality, a wide, short caecum (Graham, 1949; Righi, 1964; Wu, 1965; Smith, 1967a). The marginellid stomach (Ponder, 1970a) has incorporated the digestive gland duct as part of the fundus of the stomach in some species at least, and, as in Alcithoe arabica (Gmelin) in the Volutidae (Ponder, 19706) the style "sac; although recognizable, has lost its typhlosoles. The posterior part of the stomach of Alcithoe, which is homologous with the gastric lumen in other neogastropods, contains complexly ciliated, leaf-like structures. The overall trend in the neogastropod stomach is toward a large, relatively simple sac with the walls closely opposed. This allows the available ciliary currents to act to the best advantage in moving waste material, or in keeping food particles in suspension so that they mix with the en- zymatic secretion from the digestive gland. Achievement of these conditions is obtained by the elongation of either the style sac or mixing area, or by the forma- tion of a caecum. The formation of a crop in the posterior oesophagus of many neogastropods serves to store food and, in many cases, it is a site of preliminary digestion. Thus the food can often be broken down before reaching the stomach. The Anal Gland: An anal (or rectal) gland is found in many neogastropod families. It is possessed by species in all 3 superfamilies and has a similar structure in at least 2 of them (its histology has not been described in the Cancellariidae). It usually consists of 1 or more branching tubules, that, in the Muricidae (Fretter, 1946), some Magilidae (W.F.P.) and Volutidae (Ponder, 1970b) form a large black mass. Fretter (1946) stated that the gland in Nucella lapillus (Linnaeus) has an excretory function, but this has not been demonstrated in any other neogastropod. Smith (1967a) commented on the structure of the gland in the Turridae and the Muricidae. Other families in which the gland occurs are the Columbariidae (W.F.P.), Olividae (Marcus € Marcus, 1959), Vexillidae, Mitridae, Volutomitridae (Ponder, 1972b), Marginellidae (Ponder, 1970a), Tur- binellidae (Ponder; ВО, Cancellariidae (Graham, 1966), and the Terebridae (Marcus & Marcus, 1960). In some families normally possessing the anal gland, certain genera appear to have lost it, these including Уазит in the Tur- binellidae (Ponder, 1973b) and Diluculum in the Marginellidae (Ponder, 1970a). In some species it is very small and possibly of little functional importance. Ward (1965) has shown that Coralliophila abbreviata (Magilidae) does not possess an anal gland. None of the families in Thiele's Buc- cinacea appear to have the gland, nor has the Colubrariidae. Smith (1967a) pointed out the similarity of the granules in the anal gland of some neogastropods to those in the amoebocytes surrounding the digestive gland. In some instances, however, they do not resemble these latter granules. The refringent granules encountered in renal tissue and often seen in the gland of Leiblein are also similar. The Male Genital Ducts In all neogastropods the male genital duct (see Fig. 5) consists of a coiled, upper vas deferens modified to form a sperm storing seminal vesicle (sv) and, in some species, the walls ingest spermatozoa (Fretter, 1941; Smith 1967b). The lower or renal part of the vas deferens is usually straight and it is connected to the pericar- dium by a renopericardial duct or a strand 316 W. Е. PONDER of tissue representing it. The Volutomitridae (Ponder, 1972b), the turrid Oenopota (=Lora) travelliana (Turton) (Smith, 1967b) and possibly the turbinellid Vasum turbinellum (Linnaeus) (Ponder, 1973b) have a gonopericardial duct. The remnants of this duct have been recorded in some Muricidae, Buccinidae (Fretter, 1941), Fasciolariidae (Marcus & Marcus, 1962) and Turridae (Smith, 1967b). Some others have the renal vas deferens located so close to the pericardial wall that the existence of a vestigial duct cannot be es- tablished. A diverticulum of the renal organ approaches the renal vas deferens in the Marginellidae (Ponder, 1970a) and in Leucozonia in the Fasciolariidae (Marcus & Marcus, 1962). In the most primitive condition, the renal vas deferens opens into an open pallial groove lined with prostatic tissue, such as occurs in the Volutomitridae (Ponder, 1972b), Harpidae (Bergh, 1901), and in some volutes (Woodward, 1900; Pace, 1902). In Alcithoe arabica in the Volutidae, the sides of this groove become massive, glandular lobes (Ponder, 1970b). A line of fusion showing where the lobes were sealed is found in some muricids (Fretter, 1941) and some turrids (Smith, 1967b), whereas in the Turbinellidae all gradations between open and closed pallial grooves are found (Abbott, 1959; Ponder, 1973b) and Wu (1973) has noted the existence of 3 types of prostate gland in the Muricidae. It thus appears as though the closed prostate gland (p) developed independent- ly in at least several families. In most families in which a closed prostate gland is found, there is no trace of a line of fusion but they usually have a narrow, posterior, pallial connection, either in the form of a short, ciliated tube or a slit. Such a situa- tion is found in all of the remaining families except the Fasciolariidae which (in Leucozonia at least) has lost the posterior opening of the prostate (Marcus & Marcus, 1962). The penis (pen) is usually of moderately large size, and the duct mostly sealed and embedded in the central part of the penis. There is, however, an open penial groove in some Turbinellidae (Tudicula; Abbott, 1959), Volutidae (Volutocorbis; Woodward, 1900) and in the Volutomitridae (Ponder, 1972b). Several forms show a line of fusion representing the edges of an originally open groove such as Olivancillaria (Olividae) (Marcus & Marcus, 1959), Alcithoe (Volutidae) (Ponder, 1970b) and several genera in the Turbinellidae (Abbott, 1959; Ponder, 1973b). Prostatic cells occur in the penial ducts of Buccinum, Nassarius (Fretter, 1941), some Marginellidae (Ponder, 1970a), Mangelia (Turridae) (Robinson, 1960), and in the Olividae (Marcus & Marcus, 1959). The Volutomitridae have prostatic tissue lying within the penis and dis- sociated from the penial groove (Ponder, 1972b). The Pyrenidae have some unusual modifications in the male genital system (Marcus & Marcus, 1962a). In some, the penis lies within a pouch between the hypobranchial gland and the pallial roof, and some have a seminal vesicle lying either just behind, or in front of, the upper pallial opening of the pallial sperm duct. In 1 species the prostate is divided into 2 separate bodies, but it usually forms a con- volute part of the duct. In other species the prostate gland is absent, and in some the penial duct contains prostatic tissue. Bouvier (1888) and Gohar € Soliman (1963) have shown that the burrowing Magilidae have a penis, however it is sometimes rudimentary. Although copula- tion cannot take place, spermatozoa are apparently taken in by the inhalant current of the female and fertilization is in- ternal (Gohar € Soliman, 1963). The Female Genital Ducts The basic organization of the neogastropod female genital tract is shown in Fig. 6. Nucella lapillus and Ocenebra erinacea (Fretter, 1941) have a typical structure and have been thoroughly de- scribed. The duct in these 2 species con- sists of a short, upper and renal oviduct (od) leading from the ovary with a gono- EVOLUTION OF NEOGASTROPODA 317 st FIG. 5. Generalized muricacean neogastropod removed from its shell and viewed dorsally with the pallial cavity and anterior body cavity opened mid-dorsally and the proboscis extended. adg, anterior lobe of digestive gland; ag, anal gland; ao, anterior oesophagus; asg, accessory salivary gland; bm, buccal mass; с, caecum; cog, circum-oesophageal ganglia; ct, ctenidium; ed, ejaculatory duct; f, foot; hg, hypobranchial gland; gdf, glandular dorsal folds; gl, unpaired foregut gland; m, mouth; mo, mid-oesophagus; о, operculum; os, osphradium; р, prostate gland; pc, pericardium; pdg, posterior lobe of digestive gland; pen, penis; po, posterior oesophagus; r, rectum; ro, renal organ; sd, salivary duct; sg, salivary gland; ss, style sac; st, stomach: sv, seminal vesicle; t, cephalic tentacle; tes, testis; v, ventricle; vl, valve of Leiblein. 318 W. F. PONDER pericardial duct (gpd) at the junction of the latter duct with the albumen gland. The albumen gland (ag) is a thickened part of the oviduct itself in Nucella, and is humped, with the ventral surface of both halves in contact. A much lobulated in- gesting gland (rs) opens by way of a sperm storing duct into the area between the albumen and capsule glands. The capsule gland (cg) forms most of the pallial section of the duct and at its anterior end there is a thin-walled ventral channel (vc) that is a short, muscular vagina (vag). A short, muscular bursa copulatrix (be) opens into the vestibule, running from which is a thin-walled ventral channel (vs) that is overlain by 2 ciliated folds and a heavy, glandular lobe on the right. A gonopericardial duct is present in at least some Muricidae, Buccinidae, Nassariidae (Fretter, 1941), Olividae (Mar- cus & Marcus, 1959), Pyrenidae (Marcus & Marcus, 1962a) and Cancellariidae (Graham, 1966). The renal oviduct of the Volutomitridae sometimes has a connec- tion with the renal organ instead of the pericardium (Ponder, 1972b), and a blind, renal diverticulum lies alongside the renal oviduct in the Marginellidae (Graham, 1966; Ponder, 1970a). The albumen gland in most Conacea and Rachiglossa is similar to that in Nucella, but has often been separated from the oviduct completely, so that it communicates by a separate duct into the region between the capsule and albumen gland into which the ingesting gland and renal oviduct open. This is the case in the Vexillidae and Volutomitridae (Ponder, 1972b), Vasum in the Turbinellidae (Ponder, 1973b) and at least some Marginellidae (Ponder, 1970a). There is apparently no albumen gland in Tur- binella (Ponder, 1973b). The ingesting gland has tall, brown- coloured cells which ingest spermatozoa and sometimes yolk (Fretter, 1941; Ponder, 1972b). Although Fretter record- ed sperm ingestion in Nassarius reticulatus (Linnaeus), Johansson (1957) did not observe it in N. pygmaeus (Lamarck) or in N. incrassatus (Stróm.). In at least some Fasciolariidae (Leucozonia, Marcus & Marcus, 1962; Taron dubius, W.F.P.) the epithelium of the “ingesting gland” con- sists of simple, short, columnar cells that do not ingest spermatozoa, but instead the “gland” acts as a seminal receptacle. Seminal receptacles have been recorded in Olivella and Oliva sayana Ravenel (Marcus & Marcus, 1959) and in both of these species there is no functional in- gesting gland, although there is one in another member of the Olividae, Olivan- cillaria (Lintricula) auricularia (Marcus & Marcus, 1959). Narrow accessory ducts to the ingesting gland in Alcithoe (Volutidae) (Ponder, 1970b) store sperm and may be related to the seminal receptacles of the olivids. The duct of the ingesting gland usually acts as a seminal receptacle, storing orien- tated spermatozoa. In the species in- vestigated by Fretter (1941) (members of the Buccinidae, Muricidae and Nassariidae), and in the Volutidae (Ponder, 1970b) the ingesting gland duct opens into the ventral part of the gland and is not ciliated. In the Mitridae and Vexillidae (Ponder, 1972b) it is ciliated and opens into the dorsal part of the gland which is, in addition, not as lobed as in the preceding families. Ciliated ducts that do not store sperm are found in the Volutomitridae (Ponder, 1972b) and the Marginellidae (Ponder, 1970a), and the gland in these families is lined with large cuboidal cells that do not ingest sper- matozoa. The ingesting gland of some turrids is capable of sperm absorption (Smith, 1967b), but Martoja-Pierson (1958) did not find any evidence for this in Conus mediterraneus (Brüg.). There is, ap- parently, no albumen gland or ingesting gland in Turbinella pyrum (Linnaeus) (Ponder, 1973b). The capsule gland is usually the largest gland in the female oviduct, although in Alcithoe (Ponder, 1970b) it is shorter than the albumen gland. Typically it has several zones showing different staining proper- ties and has a ventral channel. This channel is overhung by ciliated folds, usually 2 or 3 in most rachiglossans, EVOLUTION OF NEOGASTROPODA 319 FIG. 6. Generalized neogastropod oviduct viewed laterally from the right side. ag, albumen gland; be, bursa copulatrix; cg, capsule gland; 0, ovary; od, upper oviduct; rs, seminal receptacle or ingesting gland; v, vestibule; vag, vagina; ve, ventral channel. but the smaller species are rather anomalous, the Pyrenidae having 0 to 2 (Marcus & Marcus, 1962a) and the Marginellidae being similarly variable (Ponder, 1970a). Alcithoe arabica (Volutidae) has 1 ciliated fold on the right (Ponder, 1970b) and Strigatella pauper- cula (Linnaeus) in the Mitridae has only the left fold present, but Imbricaria con- ularis (Lamarck) has an additional, small, right fold (Ponder, 1972b). A glandular lobe on the left side of the capsule gland also overlies the ventral channel in some Muricidae (Fretter, 1941) and in Alcithoe (Ponder, 1970b). Wu (1973), however, has shown that there are at least 4 types of organization in the Muricidae. One ciliated fold is present on the right side in Conus mediterraneus (Martoja-Pierson, 1958) but Haedropleura septangularis (Montagu), a member of the primitive turrid subfamily Clavinae, has a capsule gland like that of Nucella (Smith, 1967b). Thus, probably, the loss of the ciliated folds and even of the ventral channel in some other turrids (Smith, 1967b) is a secondary feature. The bursa copulatrix is a terminal sac for sperm reception, but in some species it has become modified for other purposes. In the majority of the Rachiglossa there is lit- tle variation in the bursa copulatrix, although it is very large in Vexillum spp. (Ponder, 1972b) and in Oliva sayana (Mar- cus & Marcus, 1959). It is often modified for storing orientated sperm as well as catering for temporary sperm storage im- mediately after copulation. A separate bur- sa copulatrix is missing in some marginellids (Graham, 1966), Turbinella pyrum (Ponder, 1973b) and some turrids (Smith, 1967b). Some Turridae (Smith, 1967b) have 2 regions in the anterior part of the oviduct, 1 modified for sperm receiving, therefore strictly speaking a bursa copulatrix, and the other for sperm storage. This latter organ is referred to by Smith as a sperm sac, but is almost certainly homologous with the separate bursa copulatrix of other neogastropods and turrids. The “bursa copulatrix in those species with a sperm sac (and in some without) opens directly into the capsule gland and is thus homologous with the vagina of other Neogastropoda. There is little advantage in changing the names of these structures which have acquired slight alterations (or presumed alterations) in function. The vestibule and vagina sometimes form a long outgrowth from the capsule gland. In the turrid genus, Mangelia 320 W. F. PONDER (Robinson, 1960; Smith, 1967) there is an elongated part of the oviduct in front of the short capsule gland and по bursa copulatrix. In the terebrid Hastula a similar, but open, structure occurs, as well as a small bursa copulatrix (Marcus & Mar- cus, 1960). A narrow, tubular vagina runs alongside the massive bursa copulatrix in Vexillum spp. (Ponder, 1972b). Olivella (Marcus & Marcus, 1959) has a bulb lying between the capsule and albumen glands and this is connected by a long, separate duct to the very short vagina. This bulb is lined with tall epithelial cells and contains faecal material with which the egg capsules are covered. It is possible that the long, ciliated duct of this bulb is the pinched-off ventral channel of the capsule gland and that the sperm groove now found in the capsule gland is a new structure. Alternatively it may be a bursa copulatrix as Marcus & Marcus suggest, but there is a small pouch near the genital aperture that could also be homologous with the bursa copulatrix. In Olivancillaria (Lintricula) (Marcus & Mar- cus, 1959) the gonopore lies near the junc- tion of the capsule gland and albumen gland where the bursa copulatrix and in- gesting gland also open. The Pyrenidae have several unusual features in the female reproductive system (Marcus & Marcus, 1962a). They fall into 2 groups; 1 having no albumen gland, a gonopericardial duct which, together with the pericardium stores sperm, and a pallial opening from the pericardium. In 1 species sperm is ingested in the gonopericardial duct. The 2nd group has an albumen gland but no gonopericardial duct and does have an anteriorly placed, sperm storage organ (bursa copulatrix) the epithelium of which ingests spermatozoa in some species. The vestibule is, in addi- tion, usually very muscular, with folded walls, and in 1 species there are 2 separate gonopores, | to receive the penis and the other for the passage of eggs. Smith (1967b) has shown that Propebela (=Lora) turricula (Montagu) is an her- maphrodite. Many neogastropods have а ventral pedal gland in the female, which aids in moulding the egg capsule. This appears to be absent in at least some members of the Vexillidae, Volutomitridae (Ponder, 1972b) and the Turridae (Smith, 1967b). Egg Capsules The resistant, chitinous, neogastropod egg capsule is a useful taxonomic feature, particularly at the generic and specific level, because the egg capsules have become diagnostic in shape, yet extremely varied in overall pattern. Many neogastropod egg capsules have been described in the literature, but the majori- ty remain unknown. Ankel (1929) and Fretter (1941) have shown how the capsule is moulded by the ventral pedal gland in the female. Within each major family group there is an evolutionary trend in the shape of the egg capsules. This involves a progressive raising of the primitive, lens-shaped cap- sule from the substratum and its eventual attachment by a narrow stalk. In many cases the examples and references given below are only a few of those actually available in the literature. The most primitive type of capsule is the lens-shaped form, which is encountered in the lower mesogastropods (Littorinacea and Rissoacea) and in the ar- chaeogastropod Neritacea. This type is found in most Turridae (Thorson, 1935, 1946; Knudsen, 1950; Lebour, 1934, 1937), some Marginellidae (Knudsen, 1950: Ponder, 1970a) and Olividae (Mar- cus € Marcus, 1960a), in the “Trophoninae in the Muricidae (Hedley, 1917; Habe, 1960; Amio, 1957; Dell, 1964; Thorson, 1940b, 1946), and Sipho spp. in the Buccinidae (Thorson, 1935, 1949; Lebour, 1937). The lens-shaped type pre- sumably gave rise to the hemispherical type, there being every gradation between these 2 forms. Hemispherical capsules are found in the Volutomitridae (Ponder, 1972b), in some Marginellidae (Knudsen, 1950) and Volutidae (Cooke, et al., 1895; Allan, 1934; Cotton, 1937; Graham, 194la), in Austromitra in the Vexillidae (Ponder, 1972b), and in EVOLUTION OF NEOGASTROPODA 321 Volutopsis norwegicus (Gmelin) in the Buccinidae (Thorson, 1935). A progressive elongation of the capsule, with the even- tual formation of a basal stalk, follows in several families. These include the Buc- cinidae, Pyrenidae, Nassariidae, Muricidae, Marginellidae and Turridae. The latter 2 families and the Pyrenidae have only a few examples with stalked cap- sules (Knudsen, 1950; Risbec, 1929) but these occur in the majority of the genera in the other 3 families. Thais (Muricidae) and allied genera often have parallel-sided capsules (Lebour, 1945; Hedley, 1906). Long chains of capsules on a common stalk occur in the Turbinellidae (Turbinella, Hornell, 1922), the Galeodidae (Busycon, Abbott, 1954) and the Buccinidae (Austro- fusus glans (Riding) (W.F.P.). Ball-like clusters of capsules are found in some buc- cinids (Buccinum spp. Thorson, 1935; Neptunea spp. Golikov, 1961; and Penion adustus (Philippi), Ponder, 1973a). The Mitridae (Ostergaard, 1950) have vase-shaped capsules, whereas the Conidae (Ostergaard, 1950; Kohn, 1961a) and the Harpidae (Risbec, 1932) have flattened pouches. The Magilidae have thin-walled egg sacs which are retained in- side the pallial cavity of the female (Gohar € Soliman, 1963). The capsule of Cancellaria sp. described by Knudsen (1950) is scalpel-shaped and attached by a long stalk. Some volutid egg capsules have a calcareous covering, secreted by the pedal gland (Graham, 1941a). The types of larval development in the neogastropods are reviewed by Anderson (1960).' Planktonic development of the veliger larva is retained in many Nassariidae, Pyrenidae, Muricidae, Mitridae, Conidae, some Turridae, Magilidae and Terebridae. Complete development within the egg capsule is found in at least some Buccinidae, Galeodidae, Fasciolariidae, Turbinellidae, Marginellidae, Volutomitridae, Olividae, Volutidae and Vexillidae. Several families such as the Turridae, Muricidae and Pyrenidae combine both types of development and closely allied genera, or even subgenera, often have different types of life history. Clearly the length of larval life has adaptive significance and the suppression of the free-swimming stage is probably brought about initially by environmental pressures. There is no definite example of the secon- dary acquisition of a free-swimming larval stage. In those families exhibiting direct development, usually a large number of “nurse eggs” do not develop, but provide nutriment for those that do (Portmann, 1925; Thorson, 1940a, b). Some, ш- cluding the Marginellidae (Ponder, 1970a) and Vexillidae (Ponder, 1972b), appear to rely only on yolk contained within the large egg(s), while others use albumenous material secreted by the pallial oviduct (e.g., Alcithoe arabica, Ponder, 1970b). The Renal Organ The renal organ (Fig. 5; ro) lies at the base of the pallial cavity. Perrier (1889) divided the neogastropods into 2 groups, the Méronéphridiens and the Pye- nonéphridiens, on the basis of the struc- ture of their renal organs. These, he con- cluded, were 2 natural divisions, the former group having the primary and secondary renal lamellae separated and the latter having them interdigitated. This classification was not used by later authors because of the obvious working dis- advantages and, like many classifications that rely on the structure of a single organ, it has little phylogenetic significance. Both of these types of renal organs occur in the Turbinellidae (Ponder, 1973b) and the re- mainder of the families fall into 1 or the other groups, so far as is known. However, relatively few species have been examined, and with further work the variation within each family group may be found to be greater than our present knowledge in- 'A detailed summary of patterns of development in neogastropods has recently been given by Radwin, С. E. and Chamberlin, J. L., 1973 (Patterns of larval development in stenoglossan gastropods. Trans. San Diego Soc. Nat. Hist., 17(9): 107-117). 322 W. Е. PONDER dicates. It is by no means certain which arrangement is the more primitive. Most Méronéphridiens have the primary and secondary lamellae (or fila- ments) interdigitating to a slight extent. The families with this type of renal organ are the Conidae (Perrier, 1889), the Terebridae (Marcus & Marcus, 1960), the Volutidae (Perrier, 1889; Ponder, 1970b), the Pyrenidae (only partially separated) (Marcus & Marcus, 1962a), the Olividae (Marcus & Marcus, 1959), the Mitridae (Ponder, 1972b) and the Marginellidae (Ponder, 1970a). The Pycnonéphridien group includes the Muricidae, Buccinidae (Perrier, 1889), Vexillidae, Volutomitridae (Ponder, 1972b), Fasciolariidae (Marcus & Marcus, 1962) and the Harpidae (Perrier, 1889). The Nervous System The nervous system of the Neogastropoda has received relatively lit- tle attention. The studies of Haller (1882, 1888), Bouvier (1887) and Marcus & Mar- cus (1959, 1960, 1962, 1962a) have pro- vided much of the detailed information available. The nervous system of the Rachiglossa usually shows considerable concentration of all of the circum-oesophageal ganglia and the buccal ganglia are attached by very short connectives to the cerebral ganglia. This type of situation is seen in the Muricidae (Haller, 1882, 1888; Bouvier, 1887), the Buccinidae (Bouvier, 1887; Dakin, 1912), the Pyrenidae (Marcus € Marcus, 1962a), the Fasciolariidae (Haller, 1888; Bouvier, 1887; Marcus & Marcus, 1962), the Marginellidae (Bouvier, 1887), the Mitridae (Bouvier, 1887; Ponder, 1972b), the Vexillidae and the Volutomitridae (Ponder, 1972b), the Harpidae (Bouvier, 1887; Bergh, 1901) and in some Volutidae. A few species in the last family have the supra-oesophageal ganglion separated by a long connective from the right pleural ganglion (details given by Ponder, 1970b). The cancellariids (Bouvier, 1887; Graham, 1966) have concentrated ganglia, but their buccal ganglia lie just behind the buccal mass at the distal end of the proboscis, thus having very long connec- tives. In the Conacea the ganglia are, in all 3 families, much more separated than they are in any rachiglossans, with the excep- tion of the cerebral and pleural ganglia (Bouvier, 1887; Shaw, 1915; Marcus & Marcus, 1960). There are 2 or 3 visceral ganglia near the base of the pallial cavity, these being well separated from the circum-oesophageal ganglia to which they are connected by the visceral loop. PART. 3 THE CLASSIFICATION OF THE NEOGASTROPODA The classification of the neogastropods has attracted the attention of many authors, not only because of the many con- spicuous groups it contains, but also because the order contains some of the more economically and biologically impor- tant gastropods. It is not intended to give a detailed ac- count of the history of the classification of this order, but a brief examination of some of the more important contributions is necessary in order to understand the derivation of the modern classification. Contributions to the classification of this group can be divided into 2 groups. Firstly there are those that are reviews of the whole of the gastropods. In these accounts the classification is mainly concerned, out of necessity, with the shell. The other group includes studies on various organ systems, the results of which have been used to modify existing classification. The work of Adams € Adams (1853) is the earliest comprehensive account of the Mollusca that we need to consider. Their treatment of the families now included in the Neogastropoda differed in a number of cases from the modern interpretation, but nevertheless, the majority of the family groups were much as we know them at present. The names Stenoglossa, Toxo- glossa and Rachiglossa were used in Troschel's (1856-1893) classification, bas- ed on the radula, which is essentially like that in use today. The classifications of EVOLUTION OF NEOGASTROPODA 323 Perrier (1889) based on the renal organ and Bouvier (1887) on the nervous system mostly supported the familiar classification based on dentition. Certainly any classification based on a single structure must have its short- comings, but the radula has the advan- tages of being readily accessible, as well as easily interpreted and preserved. The radula has indeed proved to be a fairly reliable indicator of the familial position of species in the Neogastropoda, but parallel development of similar types has occurred in distinct families as shown above. Tryon (1880-1884) and Fischer (1887) produced comprehensive reviews of the families of neogastropods, but their classi- fication differs little from that of Troschel. Thiele (1929) and Wenz (1938-1943) have both provided similar, detailed accounts of gastropod classification and it is these which are generally in use today. The only modern attempts at a critical assessment of gastropod classification are those of Risbec (1955) and Fretter & Graham (1962). The curious classification of Iredale & McMichael (1962) of the Rachiglossa calls ¿for comment. They use, apparently for the y first time in several cases, a number of “family” names and include some hetero- 7 At gastropods in this group. Their new y amilies are, without exception, erected without indication or any explanations, and in some cases represent the up- grading of already existing subfamilies. Since Troschel's (1856-1893) momen- tous work on the gastropod radula, the Neogastropoda (Stenoglossa) have usually been divided into the Rachiglossa and the Toxoglossa. Apart from the inclusion of the Mitridae (e.g., Risbec, 1955) and the Cancellariidae (e.g., Troschel, 1856-1893; Keen, 1958), the Toxoglossa is equivalent to the Conacea discussed above. The main distinguishing characters of the 3 super- families given briefly earlier in this paper ane, outlined in Table 1. The Neogastropoda, can be defined as follows: Order Neogastropoda Shell without inner nacreous layer, and with anterior siphonal canal. Operculum, if present, chitinous, with terminal or lateral nucleus. Radula, if present, with each row consisting of combinations of a central tooth, and a pair of lateral and marginal teeth. Animal with mono- pectinate ctenidium, bipectinate os- phradium and anterior siphon. Proboscis usually pleurembolic, but may be intra- embolic or polyembolic. Mid-oesophagus usually with oesophageal gland connected by a narrow duct (unpaired foregut gland). Buccal pouches, if present, forming a pad of glandular tissue at anterior end of the mid-oesophagus and surrounding the oesophageal valve to form the valve of Leiblein. Salivary glands with ducts not passing through nerve ring, and accessory salivary glands often present, their ducts opening at the anterior edge of the buccal cavity. Anal gland often present; intestine short and relatively straight. Usually car- nivorous. Circum-oesophageal ganglia at least moderately concentrated but visceral connectives rather long. Sexes usually separate, female typically with an in- gesting gland (sometimes a seminal recep- tacle) lying between a pallial albumen and capsule gland, and with a ventral pedal ‚ gland which aids in forming the usually horny egg capsules. Male duct with an open or closed pallial portion, and with a penis. Only left auricle and renal organ present, the latter containing 2 types of lamellae and a nephridial gland. Superfamily Cancellariacea (Synonym Nematoglossa Olsson, 1970) There are 2 families assigned to this superfamily, the Cancellariidae and Paladmetidae. The latter family is an extinct group lacking columellar folds, and is discussed in some detail by Sohl (1964). Olsson (1970) has provided the order Nematoglossa for the cancellariids, stating that the radula “is unique and differs so fundamentally from those of other named taxa that a new term based upon radular structure is necessary. In most other respects the Cancellariidae falls within the neogastropod group and it is unnecessary, in my opinion, to separate this family at the level of order or suborder. 324 W. F. PONDER Table 1. Comparison of the main features of the neogastropod superfamilies Muricacea Сопасеа Cancellariacea о > no na not distinct usually distinct not distinct à © =o" 9 = =: с n pleurembolic with buccal intraembolic or polyembolic pleurembolic; > cavity at its distal end with buccal cavity at its with buccal e proximal end cavity at its 2 distal end a usually present sometimes present very elongate Corral teeth 8 Ну present rarely present absent al = usua resen УР УР teeth a Marginal bsent resent absent MT P teeth 3.9 behind nerve ring behind nerve ring in front of nerve ring i = 85 as a © [= n о ES usually long absent absent 98 во (о en | с n 5 at posterior end of immediately behind os anterior oesophagus, absent buccal mass, ventral o я pyriform Zico o e] short short long 3 @ 9 E < 2 usually concentrated; usually loosel y usually closely connected; Q SO lie just behind valve of Leiblein connected; lie just lie near base of proboscis 2 8 8 behind buccal cavity ag 3 8 . . ос Separated from mid- separated from mid- not separated from Е E 5 oesophagus oesophagus from mid-oesophagus (or 2 ас Е absent ?) 27370 OS o 3 EVOLUTION OF NEOGASTROPODA 325 Superfamily Conacea (Synonym Toxoglossa Troschel, 1848) The families of the Conacea (Conidae, Turridae, Terebridae and Speightiidae) will not be discussed in detail. Powell's (1942) placing of the extinct Speightiidae in the Conacea is based on the presence of a posterior sinus in the aperture, but other- wise the shells look like fasciolariids. Powell (1966) has reviewed the genera and subfamilies of the Turridae and McLean (1971) has proposed 3 additional sub- families in a review of the higher clas- sification of the Turridae. Rudman (1969) has created a new family, Pervicaciidae, but his basis for its separation from the Terebridae is very slight, particularly in view of Miller's (1971) findings on the variation in the morphology of the terebrids, and its recognition does not appear to be necessary. Superfamily Muricacea (Synonym Rachiglossa Troschel, 1848, and a combination of Thiele's (1929) Muricacea, Buccinacea and Volutacea, together with Risbec’s (1955) Mitracea and Olsson’s (1956) Olivacea.) Every attempt on the part of the writer to determine detailed patterns of relation- ship in the families of the Muricacea has met with little success. It appears, from the morphological and palaeontological evidence, that most of the muricacean families arose independently in the Mesozoic (Fig. 4) and are all more-or-less equally distinct, with the exception of the Buccinidae, Galeodidae, Fasciolariidae and Nassariidae. The muricacean families are discussed below in an attempt to clarify their relationships to one another. Table 2 summarizes some of the more im- portant features of each family. The family group names Muricacea, Buccinacea and Volutacea all date from Rafinesque, 1815 and were erected in the above order, and Thiele (1929) and Wenz (1938) both use the superfamily names in the same order. For this reason the name Muricacea has been chosen. The name Rachiglossa does not suit the require- ments for formal use as a superfamily name, as it is not based on a contained genus name (Article 11(e), ICZN, 1961). Buccinidae, Nassariidae, Fasciolariidae, and Galeodidae Differentiation between these groups is usually possible on shell features and/or radular features. The magnitude of the differences, however, is not great and there are practically no anatomical features which can be used consistently to separate them. The writer has followed the generally accepted practice of retaining these groups as families but, in fact, they show levels of differentiation from one another that could be treated as sub- familial. The Buccinidae is an extremely large and varied family (as listed by Wenz, 1938) and about 20 family and subfamily names have been based on the genera con- tained within it. Tryon (1881) included 6 subfamilies, and Fischer (1887) and Coss- mann (1901) used 7 within the 1 family.? Powell (1929) recognized 3 family groups, the Buccinidae, Cominellidae and Neptuniidae, but in 1951 he made the cominellids a subfamily of the Buc- cinulidae. These groups are based on radular and opercular characters that seem very minor when the total variation within the group is considered, and should not be recognized even as subfamilies. The majority of the other groups erected have been based solely on shell features and, even on this basis, they are hardly separable. Many Buccinidae pass through their lar- val stages within the egg capsules, this resulting in a paucispiral protoconch, but the nassariids often have a free swimming larval stage. This difference may, in part, be due to the Buccinidae mainly being in temperate latitudes whereas the majority of nassariids are tropical or subtropical in distribution. This view is reinforced by *Habe, T. and Sato, J., 1972, (A classification of the family Buccinidae from the north Pacific, Proc. Jap. Soc. Syst. Zool., 8: 1-8) have recognised 6 subfamilies among the larger buccinids of the north Pacific. jueseid jueseid jueseid Aj jonsn jueseJd juesqo juesed jueseid juesoid juasqo 10 juasaid jueseid R = 4 PONDE juesqo W. 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J0¡¡9unjo wnjnoiedO Asosseoo DINPD uo¡B ynBai0y posiodu PLA Ш [29 | У |ПР5У EL] y n | *SO!|/WDj UDBDDILINW OU} JO 5940}09} ULDW O44 JO ewos jo uosiindwoT *Z 9D] 20! [1X2 эор! W эор!||эч!6лоу\ эор! 4! шо под эор!9лон эор!^|О эорци|од эор!!109шп| о эор!! 65 Sopı>Luny (eouisbA) eDPISDA (eoui|peuiqin]) appiuaidg э0р!!15491 |905) эор!роз| го ©0р!110|015$0.} 90р! 1105$ 54 9DP1U1DING Any EVOLUTION OF NEOGASTROPODA 327 Phos and some other tropical/subtropical buccinid genera having multispiral proto- conchs. The group including Phos and its allies are sometimes separated as a family, Photidae. Risbec (1952) and Bouvier (1888) both show that the Nassariidae and Buccinidae lack any distinctive morpho- logical features that could separate them into 2 groups. The presence of 2 posterior tentacles on the foot does, however, give the nassariids a certain distinctiveness. The radula of the Nassariidae is very similar to that of many Buccinidae, although it often bears an accessory plate, a structure not known in the Buccinidae. The group is a very homogeneous one, although Cossmann (1901) recognizes 3 subfamilies within it. Some Nassariidae have become, secondarily, deposit feeders and have a crystalline style in the stomach (Morton, 1960; Brown, 1969). The Fasciolariidae differs from the above families and from the Galeodidae in usually having a red-pigmented head-foot. The radula, too, is distinctive, with mul- ticuspid lateral teeth and small central teeth. In the 2 species investigated, the structure in the female pallial genital tract that functions as an ingesting gland in the above 2 families acts as a seminal recep- tacle only. Typical members of the Fusinus group appear to differ from the remainder of the family only in having a long siphonal canal, although they are sometimes separated as a family, the Fusinidae. However, there are many genera difficult to place in 1 group or the other so that the recognition of this group is not recommended. No members of the Galeodidae (=Melongenidae, Volemidae) have been described in detail, but their anatomy appears to be like that of the Buccinidae (Vanstone, 1894; Kesteven, 1904; Pierce, 1950; W.F.P.) except that species in the genus Melongena have lost the unpaired foregut gland. The morphological similarity of these 3 families, together with the allied families Pyrenidae and Colubrariidae, might sug- gest that Thiele's Buccinacea should be used to cover this homogeneous group. If this were done then the difficulty of placing families such as the Turbinellidae and Mitridae, which also show many “buc- cinacean” features, would show that the distinctiveness of such a group was, in fact, well below the normal level that one would expect in a superfamily. If one were to retain a division Buccinacea, then most of the other neogastropod families would require different superfamilies. The similarity of the Pyrenidae to the Buccinidae may be due to parallel evolu- tion, although there are по records of species assigned to this family before the Paleocene, whereas the galeodids, buc- cinids, and fasciolariids were all present in the Upper Cretaceous (Wenz, 1938; Sohl, 1964). Colubrariidae (= Fusidae ) The features of this family, based on Ratifusus reticulatus (A. Adams) (= mestayerae (Iredale)) and Iredalula striata (Hutton), are outlined by Ponder (1968). This group was probably derived from an early buccinid stock. The protoconch is small and multispiral, so that it is probable that they have a pelagic larval life. The stomach and mid-oesophagus are different from those encountered in the Buccinidae. The shell of Colubraria is superficially like that of some members of the Cymatiidae (Tonnacea, Mesogastropoda), but some other genera in the family have a resemblance to certain buccinids. Cernohorsky (1971) indicated that the anatomical information presented by Ponder (1968) for Ratifusus and Iredalula suggested their placement in the Buc- cinidae, and not that the Colubrariidae is “buccinacean”. This view he attempted to substantiate by showing that the type species of Colubraria, C. maculosa (Gmelin, 1791) (= muricata Lightfoot, 1786) does not have a radula whereas ' Ratifusus and Iredalula do have a minute radula, which is, however, virtually vestigial. A study of the anatomy of Colubraria cf. sowerbyi (Reeve) (W.F.P.) has shown that it possesses the same peculiar glandular mid-oesophagus that differentiates Ratifusus and Iredalula from 328 W. F. PONDER the Buccinidae and the other features of the anterior alimentary canal are also similar except that there is no odontophore or radula. It thus appears that some Colubrariidae have lost the radula and that it is relatively small or vestigial in the remainder. It is possible that the whole Metula-Ratifusus series discussed by Cer- nohorsky (1971) belong in the Colubrariidae as they all have similar shell features. The Upper Cretaceous genus Fulgerca Stephenson is possibly a colubrariid, although Sohl (1964) includes it doubt- fully in the Buccinidae. Another possible Upper Cretaceous colubrariid is Plesiotriton cretaceus Sohl (Dr. A. G. Beu, pers. comm.). Colubraria extends back to the Paleocene (Wenz, 1938). Turbinellidae (=Vasidae, =Xancidae) The features of this family will be dis- cussed elsewhere (Ponder, 1973b). It shows similarity, on the one hand, with the Buccinidae and its allied families, in not having accessory salivary glands and in the possession of a thick, heavy, spindle- shaped shell, large operculum and long proboscis. Discordant features are the radula and anal gland of Turbinella, the open or partially fused pallial sperm grooves and the columellar folds. Vasum has a radula like that of Melongena, and it apparently does not possess an anal gland. The first appearance of this family, like many of the Muricacea, is during the Cretaceous (Fig. 4) and it seems likely that most of its features were derived quite in- dependently from, but in a parallel fashion to, the buccinid-nassariid-galeodid- fasciolariid complex. The Pyrenidae, too, probably acquired the “buccinacean” features of the alimentary canal т- dependently. The subfamilies Turbinellinae and Vasinae appear to be quite distinct anatomically (Ponder, 1973b). Pyrenidae (=Columbellidae) The pyrenids exhibit both specialized and primitive features. Risbec (1954) and Marcus € Marcus (1962a) have provided most of the available information on the anatomy of the family. The alimentary canal is rather uniform and is similar to that of the Buccinidae. The radula shows a tendency towards suppression of the cen- tral teeth and the lateral teeth are usually attached by narrow bases. The reproduc- tive system shows considerable diversity and Marcus & Marcus (1962a) suggest that the family could eventually be divided into 2 groups on the basis of the structure of the genital organs. Some pyrenids have become herbivorous (Marcus € Marcus, 1962a). Many species have lost the oper- culum and their shells usually have long, narrow apertures. Muricidae (=Thaididae, etc.) Distinctive morphological features of the Muricidae (in the broad sense) include accessory salivary glands, a purple hypo- branchial secretion, a massive gland of Leiblein, a broad caecum in the stomach, an anal gland and a large, closed, prostate gland. The path of torsion is indicated in the conspicuous valve of Leiblein by a narrow groove, and the primary and secon- dary lamellae of the renal organ are not separated. The small foot has an accessory boring organ on its anterior, ventral sur- face and the radula has 3 teeth in each transverse row, the central tooth usually having 3 primary cusps. The muricids form a rather homogeneous group in which Cossmann (1903) recognized 5 sub- families (Ocenebrinae, Muricinae, Trophoninae, Typhinae, and Rapaninae), with the Purpuridae (=Thaididae) as a separate family. The differentiation be- tween the subfamilies is small, although they do appear to form fairly natural groups. The Thaididae is no more distinct than any of the subfamilies contained within the Muricidae and could be regarded as one also. Morphological differentiation between the “subfamilies” is slight, but, judging from the few species that have been examined, the accessory salivary glands show a progressive en- largement and separation from the normal salivary glands through the Muricinae and Trophoninae to the Thaidinae, EVOLUTION OF NEOGASTROPODA 329 Ocenebrinae and Вараптае. The small radular and shell differences that have been cited between the various groups (e.g., Vokes, 1964) do not appear to be consistent (Ponder, 1972a), although the case for use of several subfamilies has been put strongly by Radwin & D Attilio (1971) and Vokes (1971). The operculum has often been cited as evidence for the separation of Thaidinae and Ocenebrinae from the remainder of the family because in these groups it has a lateral nucleus. However opercula with both terminal and lateral nuclei occur within the genus Murex and other exceptions are known. There appears to be little advantage in retaining these subfamilial groupings until stronger evidence for their distinctiveness is forthcoming. Wu (1973) has outlined some of the variation of anatomical structures in the Muricidae. Radwin & D'Attilio (1971) recognize the Rapanidae, Thaididae, and the Muricidae as separate families on the basis of shell, radular and opercular details. Magilidae (=Coralliophilidae, Rapidae) The shells of some members of the fami- ly closely resemble those of some Muricidae, but the 2 groups can be separated on the absence of a radula in the Magilidae. The unpaired foregut gland is massive and its interior is divided trans- versely by conspicuous partitions (Bouvier, 1888; Ward, 1965). This structure was mis- identified as the stomach by Gohar € Soliman (1963). The sedentary species that live in burrows within coral appear to possess an anal gland (W.F.P.) whereas the actively mobile Coralliophila abbreviata (Lamarck) (Ward, 1965) does not. It is pos- sible that some magilids may be found to possess a vestigial radula and it might be found that, in such species, the Magilidae and Muricidae closely approach one another. The few species of the Magilidae investigated however, have only 1 pair of salivary glands, the ducts of which join to form a common dorsal duct in Coralliophila abbreviata (Ward, 1965). In the sedentary and freely moving species so far examined the female stores the egg capsules inside the mantle cavity, a habit not seen in any other neogastropod. These gastropods feed suctorially on coelenterates (Robertson, 1970), although it is not certain how species such as Magilus (which are permanently em- bedded in their coral host with only a tiny external aperture through which the proboscis can emerge) feed. Columbariidae The possession of a very long proboscis makes this group distinct from the Muricidae. The radula, too, is rather different from the normal muricid type. The family resembles the Muricidae in having a large unpaired foregut gland and an anal gland, but is similar to the Buc- cinidae in the lack of any glandular dorsal folds in the mid-oesophagus and in the absence of accessory salivary glands. Thiele (1929) included Columbarium in the Muricidae but Tomlin (1928) separated it, as a family, on shell and oper- cular features. It was reduced to a sub- family of the Muricidae by Wenz (1938), but Iredale (1936) gave it full family status, which is followed here, based on the anatomy of Coluzea spiralis (A. Adams) and С. mariae (Powell) (W.F.P.). Iredale placed the family near the “Fusinidae (Fasciolariidae). This family has recently been reviewed by Darragh (1969). Volutidae Distinctive features of the majority of the Volutidae include the broad hood over the rhynchostome, formed by the tentacle bases, the large foot, and the siphonal appendages. Both types of salivary gland are present and there is sometimes a pur- ple hypobranchial secretion. The dorsal folds of the mid-oesophagus are usually in- corporated as a duct-like structure in the unpaired foregut gland and the path of torsion is indicated in the valve of Leiblein. The primary and secondary renal lamellae are separated and the pallial, male, genital tract is often an open groove 330 W. Е. PONDER or prostate gland. Typically the shell has columellar plaits, and there is usually no operculum. The radula nearly always con- sists of only the central teeth. Develop- ment is nearly always complete in the cap- sule, although some species have small multispiral protoconchs suggesting pelagic larval development. Cossmann (1899) used 6 subfamilies in the Volutidae, but Wenz (1938) used only 4 (excluding the Volutomitrinae). Pilsbry & Olsson (1954) introduced 8 new sub- families and a number of tribes. Altogether they divided the family into 12 sub- families and 8 tribes. While this is almost certainly excessive considering the evidence available, there should be no doubt as to the pure composition of each of their groups. It is probable that an assess- ment of the characters of the male genital system, together with the radula and shell, would derive a more conservative clas- sification that would, at the same time, be natural. Clench & Turner (1964) divided the subfamilies on the basis of the appearance of the salivary glands, the un- paired foregut gland and the shape of the radula. Weaver & duPont (1970), in their monograph of the family, recognize 9 sub- families among the Recent species. Olividae Olsson (1956) created a superfamily for the Olividae in which Marcus & Marcus (1959) included the Harpidae. The morphology of the Olividae has so much in common with that of the rest of the Muricacea that, in the writer s opinion, a separate superfamily is unwarranted. Olsson (1956) included 4 subfamilies and, doubtfully, a 5th, the Pseudolivinae, which he suggested possibly does not belong in the family in which it is placed by Thiele (1929) and Wenz (1938). Coss- mann (1899) included the Pseudolivinae in the Buccinidae. Marcus & Marcus (1959, 1968) gave a detailed account of the morphology of 5 species of Olividae. Olivella stands out sharply in its morphological differentia- tion. Marcus & Marcus (1959) suggest that the Olividae has some features in common with Thiele's Buccinacea and Volutacea and may have been derived from a com- mon ancestor. Perhaps this is so, but the common features they mention such as the large foot and concentrated nervous system were probably derived by parallel evolution, and do not indicate a direct relationship. The olivids superficially resemble the harpids and volutids, but differ from them in having the sides of the foot extending over the shell. The harpids have no accessory salivary glands, but these are found in most olivids and the region of tor- sion in the gut of the olives is different from that in the volutes. The radula of Harpa is more like that of the Volutidae than the type that is found in most olivids. Both Harpa and the olivids have a distinct propodium, a feature not found in any other neogastropods, but this by itself does not necessarily indicate their close rela- tionship. The Olividae and the Harpidae may have both independently developed the muscular propodium of the foot, which is such a useful digging tool. There are several other differences between the 2 families, for example the harpids have a pallial sperm groove (Bergh, 1901), but this is a closed duct in the olivids. Harpidae An account of the morphology of this family is given by Bergh (1901) and Quoy & Gaimard (1833). These authors describe how the posterior end of the foot can be automatized. The valve and gland of Leiblein have been lost and there is ap- parently no anal gland or purple hypobranchial secretion. There is no oper- culum. The lack of an anal gland and accessory salivary glands, together with the pyc- nonéphridien condition of the renal organ, suggest affinity with the Buccinidae. This, however, is rather unlikely considering the other morphological features. Volutomitridae and Marginellidae A list of morphological features of these 2 families is given by Ponder (1970a, EVOLUTION OF NEOGASTROPODA 1972b). They have several unusual features in common and thus they may have arisen from a common stem. These characters include а single accessory salivary gland; the seminal receptacle lined with large, cuboidal cells; the absence of an ingesting gland; and a narrow diverticulum of the renal organ which approaches or enters the renal genital duct. From the situation in the Volutomitridae, it would appear also that the unpaired foregut gland may have been stripped off the mid-oesophagus forwards instead of backwards. Both families consist of species with small shells which have columellar plaits.\ All marginellids and many microvolutids D have lost the operculum but some micro- volutids have retained it or have it as a rudiment. The lateral radular teeth are ab- sent in the Marginellidae and weak or ab- sent in the Microvolutidae. Differences be- tween the 2 families include the structure of the mid-oesophagus, the male repro- ductive system, the stomach and the renal organ. Cernohorsky (1970) has reviewed the Volutomitridae. Wenz (1938) gives an Eocene origin for the Marginellidae, but the Upper Cretaceous genus Myobarbum Sohl is possibly an early marginellid. Mitridae and Vexillidae The structural differences between these 2 families have been outlined by Ponder (1972b). The 2 groups appear to have evolved quite independently, but show a remarkable parallelism in their shell morphology. Differences in the ali- mentary canal, including the radula, and in the renal organ, set the 2 families apart. There is a similarity in the reproductive organs, but this is probably part of the general uniformity in these organs throughout the Neogastropoda. Cer- nohorsky (1970) has reviewed these 2 families (as the Mitridae) in some detail. ACKNOWLEDGEMENTS I would like to thank Dr. M. Winter- bourne, Dr. D. Hoese, Dr. V. Fretter, Prof. 3Now the National Museum. 331 A. Graham and Dr. R. D. Turner for their comments on the manuscript and my wife for help in checking the manuscript. Mr. E. K. Yoo prepared Fig. 1. 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K., 1965, Comparative functional studies of the digestive system of the muricid gastropods Drupa ricina and Morula granulata. Malacologia, 3(2): 211-233. WU, S. K., 1973, Comparative studies on the digestive and reproductive systems of some muricid gastropods. Bull. Amer. malacol. Union: 18. YAMAGUCHI, М... ОНО TSUKAMOTO. М., УАСО. Ща TAKATSUKI, S., 1961, On the nature of the carbohydrase and protease of salivary gland and mid-gut gland in the marine gastropod, Babylonia japonica Reeve. 1. Zool. Mag., Tokyo, 70: 115-119. ZUSAMMENFASSUNG ABSTAMMUNG UND ENTWICKLUNG DER NEOGASTROPODEN W. F. Ponder Die Ordnung Neogastropoda entwickelte sich wahrscheinlich aus den Archaeogastropoden und nicht von den höheren Mesogastropoden, wie allgemein angenommen wird. Es wird angenommen, daß die Eigenarten des Verdauungssystems der Neogstropoden von Bildungen abgeleitet werden können, die bei den Arch- aeogastropoden existieren. Die Neogastropoden haben sich augenscheinlich in 3 Gruppen entwickelt, die hier als Oberfamilien betrachtet werden, die Muricaceae, Conaceae und Cancellariaceae. Die Entwicklung der verschiedenen Organsysteme bei den Neogastropoda wird skiz- ziert und dabei die Tendenz bemerkt, Struktureren in paralleler Richtung zu modifizieren. Die Beziehungen der einzelnen Familien innerhalb der Muricaceae un- tereinander werden diskutiert. Es scheint, daß innerhalb dieser Gruppe keine natürlichen höheren Gruppierungen existieren, zwei Fälle ausgenommen, Wahrschein- lich, weil alle diese Familien von der gleichen Stammform mehr oder weniger gleichzeitig abgezweigt sind. So sind verschiedene Strukturen ziemlich zufällig durch die Oberfamilie verteilt, je nach der Weise, wie sich jede Familie weiterentwickelt hat. Die EVOLUTION OF NEOGASTROPODA Marginellidae und Volutomitridae können unabhängig entstanden sein, während die Buccinidae, Melongenidae, Nassariidae und Fasciolariidae so nahe verwandt sind, daß sie möglicherweise als Unterfamilien angesehen werden können. HZ: RESUME L'ORIGINE ET L EVOLUTION DES NEOGASTROPODES W. F. Ponder L’ordre des Néogastropodes а probablement évolué а partir des Archéogastropodes et non des Mésogastropodes supérieurs, comme on le сгой généralement. П est probable que les caractéres uniques du canal alimentaire des néogastropodes aient pu dériver de structures existant chez les archéogastropodes. Les néogastropodes semblent avoir évolué en 3 groupes qui sont ici considérés comme des superfamilles: les Muricacea, Conacea et Cancellariacea. Dans la présente étude on a tracé à grands traits l’évolution des divers appareils а l’intérieur des néogastropodes et Гоп y a noté la tendance à modifier les structures dans des voies paralleles. Les liens de parenté entre chaque famille chez les Muricacea, ont été discutés. A deux exceptions pres, il apparait que dans ce groupe, il n y a pas de groupe- ments naturels de plus haut niveau, sans doute parce que toutes les familles évoluent а partir Чип ancétre commun а peu prés simultanément. Ainsi les divers types de struc- tures sont distribuées presqu au hasard à travers la superfamille, selon la voie dans laquelle chaque famille a évolué. Les Marginellidae et Volutomitridae peuvent étre ap- parues indépendamment, tandis que les Buccinidae, Melongenidae, Nassariidae et Fasciolariidae sont de parenté si proche, qu elles peuvent étre considérées comme des sous-familles. A.L. RESUMEN ORIGEN Y EVOLUCION DE LOS NEOGASTROPODA W. F. Ponder El orden Neogastropoda probablemente tuvo descendencia de los Archaeogastropoda y no, como generalmente se cree, de los mäs evolucionados Mesogastropoda. Se sugiere que las caracteristicas, únicas, del canal alimenticio en neogastrópodas, pueden haber derivado de estructuras ya existentes en arqueogastrópodos. Parece que, en su evolución los Neogastropoda han producido tres grupos, a los cuales se asigna aqui el rango de superfamilias: Muricacea, Conacea y Cancellariacea. Se han delineado en forma general los varios sistemas de órganos en Neogastropoda, y se hace notar la tendencia hacia la modificación de estructura en modo paralelo. Se dis- cute tambien las relaciones entre las familias de los Muricacea. Con un par de excep- ciones, no parece haber dentro del conjunto grupos naturales de más alta jerarquia, probablemente porque todas las familias se derivan de un antecesor común más o menos simultaneamente. Asi, varias estructuras se distribuyen casi al azar en toda la super- familia, de acuerdo al modo en que cada familia ha evolucionado. Los Marginellidae y los Volutomitridae pueden haber tenido independiente origen, mientras que los Buc- cinidae, Melongenidae, Nassaridae y Fasciolariidae estan tan estrechamente relacionados, que posiblemente podrían considerarse como subfamilias. PIE: 337 338 W. F. PONDER ABCTPAKT ПРОИСХОЖДЕНИЕ И ЭВОЛЮЦИЯ NEOGASTROPODA В.Ф. ПОНДЕР Отряд возможно развился из Archaeogastropoda, a не от высших Mesogastropoda, как это обычно считают. Предполагается, что характерные черты строения пищеварительного канала y Neogastropoda можно произвести OT yxe существующих их структур У Archaeogastropoda. Neogastropoda видимо должны быть разделены на 3 группы, которые автором рассматриваются как надсемейства - Muricacea, Сопасеа И Cancellariacea. Рассматривается эволюция систем различных органов внутри отряда Neogastropoda и подчеркивается тенденция к параллелизму в модификации их структур. Обсуждаются родственные связи каждого семейства в отряде Muricacea. За двумя исключениями внутри этого отряда видимо нет более высоких естественных группировок, может быть потому, что все семейства произошли более или менее одновременно от общего предка. Таким образом, различные структуры встречаются довольно случайно BO всем надсемействе, соответственно происхождению каждого входящего в него семейства. Marginellidae и Volutomitridae могли возникнуть независимо друг от друга, в то время, как Buccinidae, Melongenidae, Nassariidae и Fasciolariidae имеют такое близкое родство, что их возможно рассматривать как надсемейство. Z.A.F. MALACOLOGIA, 1973, 12(2): 339-378 SUR LES MOLLUSQUES FLUVIATILES DE MADAGASCAR E. Fischer-Piette et D. Vukadinovic Muséum National d’ Histoire Naturelle 55, rue de Buffon, Paris Ve, France RESUME Ce travail est ип complément а celui de Starmühlner paru dans MALACOLOGIA en 1969. Il le compléte surtout en mentionnant les Lamellibranches en plus des Gastéropodes et en donnant pour beaucoup de Gastéropodes des provenances plus nom- breuses. Pendant trés longtemps la faune malacologique fluviatile de Madagascar ne fit l'objet d aucun travail important! Enfin, en 1969, Starmühlner (Malacologia, 8(1-2)) a publié un gros mémoire ou les Gastéropodes sont étudiés, et souvent de facon trés approfondie, en particulier au point du vue de l'anatomie, histologie comprise. Le present travail est en somme ип complément а celui de Starmühlner, pour celles des especes dont cet auteur пе s était pas occupé (Lamellibranches, etc.), et aussi, pour les autres, pour faire connaître des localités supplémentaires, grâce à l’abondance des matériaux qui depuis longtemps se sont accumulés au Muséum de Paris. Clithon brevispina Lamarck 1822 Neritina brevi-spina, LAMARCK, 6(2): 185. 1838 Neritina brevispina, POTIEZ & MICHAUD, p 301, pl. 29, fig. 3, 4. 1841 Neritina brevispina, DELESSERT, pl. 32, fig. 5. 1843 Neritina auriculata, SGANZIN, p 20. 1850 Neritina brevispina, PETIT de la SAUSSAYE, 1: 76. 1849 Neritina brevispina, SOWERBY, 2: 524, pl. 110, fig. 45, 51, 52. 1860 Neritina brevispina, MORELET, 2: 126. 1888 Neritina brevispina, TRYON, 10: 65, pl. 23, fig. 16-18; pl. 24, fig. 19-28, 31-34. 1956 Clithon brevispina, FRANC, 13: 17, fig. 8. Espece а trés large répartition. Le premier auteur qui Гай citée de Madagascar est Sganzin, qui la dit “tres commune dans toutes les rivieres de Madagascar. Les autres auteurs qui l'ont citée de l'île, Petit de la Saussaye et Morelet, n'ont pas donné de provenance précise. Nous doutons que cette espéce soit aussi bien représentée que Га dit Sganzin, car nous nen avons pas trouvé dans les nombreuses récoltes de Madagascar qui nous sont parvenues, si ce n'est un échantillon que nous avons extrait d'un lot de №. madecassina qui était accompagné de l'étiquette suivante: “Mr. Férussac l'avait dans sa collection pour le nom de Мег. Barbabac nom pour lequel on la lui avait envoyée de Madagascar. “donné par Mr. Sganzin.” (339) 340 FISCHER-PIETTE ET VUKADINOVIC Clithon (Clithon) longispina Recluz 1841 Neritina longispina, RECLUZ, p 312. 1849 Neritina longispina, SOWERBY, 2: 522, pl. 110, fig. 62, 63. 1860 Neritina longispina, MORELET, 2: 120, 126. 1879 Neritina longispina, MARTENS, ed. 2, 2(10): 147, pl. 15, fig. 16, 17, 20, 21. 1888 Neritina longispina, TRYON, 10: 63, pl. 23, fig. 3-5. 1908 Paranerita (Neritina) longispina, BOURNE, р 847. 1969 Clithon (Clithon) longispina, STARMUHLNER, 8: 56. Espéce a large répartition. Pour Madagascar, nous ne croyons pas qu aucune provenance précise ait jamais été donnée. Les collections du Muséum renferment, avec la seule indication Madagascar” neuf lots; ceux pour lesquels le donateur ou récolteur est indiqué sont de Eydoux, Texor de Ravisi, 1853, et Lamare Piquot, 1865. Clithon madecassina Morelet 1795 Nerita corona Bengalensis, CHEMNITZ, 11: 176, pl. 197, fig. 1911. 1838 ?Neritina Bengalensis, POTIEZ € MICHAUD, p 300, pl. 29, fig. 1, 2. 1849 Neritina Bengalensis, SOWERBY, 2: 525, pl. 109, fig. 30, 31. 1850 Neritina Bengalensis, RECLUZ, 1: 148. 1860 Neritina madecassina, MORELET, 2: 122, pl. 6, fig. 2. 1879 Neritina (Clithon) madecassina, MARTENS, ed. 2, 2(10): 149, pl. 16, fig. 1-3. Il est possible que la dénomination Neritina Bengalensis Pot. et Mich. doive l'emporter sur Neritina madecassina Morelet. Mais Potiez & Michaud disent que leur espéce est “d'un beau vert-pomme tacheté de jaune fauve.” Or vonMartens (1879, р 149) dit n avoir pas rencontré de teinte vert-pomme, et il en est de méme pour nous. Nous ne connaissons que du vert olive ou du brun parfois trés foncé. Espece répartie assez largement. La seule localité précise qui avait été donnée pour Madagascar est l’île Sainte-Marie (Morelet). Les collections du Muséum permettent d’a- jouter les provenances suivantes: Rivière des Caimans (Decary); Maroansetra, ruisseau (Brygoo, 1957); embouchure de la riviére Mananara (Decary, 1920); Ivontaka (Decary, 1920); Anjahambe, riviére Manantsatrana (Brygoo, 1957); Ampasina, riviére Maningory (Brygoo, 1957); riviére Ivoloina (G. Petit, 1926); Foulpointe, riviére Onibe (Decary, 1920). Toutes ces localités sont portées sur notre Fig. 1. On remarquera que toutes sont sur la cóte, et uniquement dans le Nord et le Nord-Est. Clithon (Clithon) spiniperda Morelet 1860 Neritina spiniperda, MORELET, 2: 121, pl. 6, fig. 3. 1879 Neritina spiniperda, MARTENS, ed. 2, 2(10): 266. 1881 Neritina spiniperda, CROSSE, 29: 208. 1883 Neritina spiniperda, MORELET, 31: 203. 1888 Neritina spiniperda, TRYON, 10: 70, pl. 26, fig. 78. 1890 Neritina (Clithon) spiniperda, BOETTGER, 22: 101. 1892 Neritina (Clithon) rhyssodes, BOETTGER, 24: 57. 1969 Clithon (Clithon) spiniperda, STARMUHLNER, 8: 28, fig. 4-7. Cette езрёсе était connue de Nossi-Bé et Nossi-Comba. Les collections du Muséum permettent d'ajouter une autre provenance: Ambanja-Anorotoangana (Waterlot). Voir carte Fig. 1. Neritina rhyssodes avait été décrite par Boettger sans figure, mais le type a été figuré par Hass (1929), sous le nom Neritina (Clypeolum) pulligera knorri. MOLLUSQUES DE MADAGASCAR 341 eClithon madecassina norel. AClithon spiniperda xorel Nossi-Bé Nossi- Comba A Amlboanja _{ Wa Maroansetra Mananara Ile St’ Marie Ampasina Ivontaka hiba Anjahambe____, - MOI Foulpointe FIG. 1. Distribution de Clithon madecassina Mor. et de Clithon spiniperda Mor. Neritina (Neritina) pulligera Linné 1767 Neritina pulligera, LINNE, 12: 1253. 1786 Nerita Rubella, Pulligera, CHEMNITZ, 9: 64, pl. 124, fig. 1078, 1079. 1841 Nerita Knorri, RECLUZ, p 274. 1849 Neritina pulligera, SOWERBY, 2: 510, pl. 111, fig. 65, 66. 1849 Neritina Knotrii, SOWERBY. р 511, pl. 111, fig. 78; pl. 113, fig. 150. 1860 Neritina Knorri, MORELET, 2: 120. 1879 Neritina pulligera, MARTENS, ed. 2, 2(10): 49, pl. 1, fig. 4, 5. 1879 Neritina Knorri, MARTENS, ed. 2, 2(10): 55, pl. 8, fig. 4-6. 1881 Neritina Knorri, CROSSE, 29: 207. 1888 Neritina pulligera, TRYON, 10: 56, pl. 18, fig. 6-13; pl. 19, fig. 14-19, 22, 24. 1890 Neritina (Neritaea) knorri, BOETTGER, 22: 98. 1890 Neritina (Neritaea) stumpffi, BOETTGER, 22: 99. 1914 Neritina (Clypeolum) pulligera var. knorri, ROBSON, 32: 377. 1919 Neritina pulligera var. knorri, ODHNER, 12: 43. 1929 Neritina pulligera, DAUTZENBERG, 3: 526. 1929 Neritina (Clypeolum) pulligera knorri, HAAS, 57: 428, fig. 27 (fig. 25-26 excl.). 1969 Neritina (Neritina) pulligera, STARMUHLNER, 8: 69, fig. 73-76. Neritina stumpffi Boettger, décrite sans figure a été placée par Haas (qui en a figuré le type, fig. 27) dans la synonymie de pulligera; Starmühlner $ est conformé а cette opinion; nous faisons de méme, la description donnée étant détaillée. Une autre espéce, créée sans figure, Neritina truncata Sganzin (1843) de Madagascar, a été placée par Starmühlner 342 FISCHER-PIETTE ET VUKADINOVIC dans la synonymie de pulligera, mais il est impossible de savoir de quoi il s agit, ce nom truncata n étant accompagné que de quelques mots si insuffisants que c'est à peu pres un nomen nudum. Cette езрёсе, а trés large répartition, était connue pour Madagascar, des provenances suivantes: Nossi-Bé, Morelet, Crosse, Boettger; Nossi-Comba, Boettger; riviere An- drohibe, Odhner; Majunga, Haas; entre Tamatave et la baie d'Antongil, Robson. Les collections a Muséum permettent d'ajouter les provenances suivantes: riviére des Caímans (Decary); Ambanja (Waterlot); riviere Andranomalaza а Maromandia (Decary, 1922); и (Н. Soula, 1968); Ankavanana (H. Soula, 1968); Ambatofotsy sur riviere Ankavia (Н. Soula, 1969); Virembina (H. Soula, 1969); Antsiafapiana (H. Soula, 1969); Maroansetra (D. Brygoo, 1957); Andratambe, riviere Mananara (Decary); An- dranomavo (С. Petit, 1926); riviere Kapiloza (С. Petit, 1926); Fenerive (Brygoo, 1957); Tamatave (G. Petit). Toutes ces localités sont portées sur notre carte Fig. 2. On remarquera, d'une part qu'elles sont toutes sur la côte ou non-loin, et d'autre part qu elles sont toutes dans le tiers Nord de Tile. Neritina (Neripteron) auriculata Lamarck 1822 Neritina auriculata, LAMARCK, 6: 186, pl. 455, fig. 6 de ГЕпсусюр. méth. 1838 Neritina auriculata, DESHAYES, ed. 2, 8: 572. 1843 Neritina auriculata, SGANZIN, р 20. 1860 Neritina auriculata, MORELET, 1: 126. 1879 Neritina auriculata, MARTENS, ed. 2, 2(10): 30, pl. 6, fig. 13-15, 24-27. 1888 Neritina (Neripteron) auriculata, TRYON, 10: 73, pl. 21, fig. 58-63. 1969 Neritina (Neripteron) auriculata, STARMUHLNER, 8: 56, fig. 58. Espece à trés large répartition, citée à plusieurs reprises de Madagascar, mais une seule fois (Starmühlner) avec une localité précise, St. Augustin. Les collections du Muséum permettent d'ajouter les provenances suivantes: Maroansetra (Brygoo, 1957 ); enbouchure de la riviere Mananara (Decary, 1920); Maintinandry, riviere Sakamila (Brygoo, 1957) et Sandranoro (H. Bertrand, 1970). Voir notre carte Fig. 3. Neritina (Vittina) turrita Chemnitz 1786 Nerita turrita, CHEMNITZ, 10(2): 71, pl. 124, fig. 1085. 1849 Neritina turrita, SOWERBY, 2: 539, pl. 112, fig. 91, 113, 114. 1850 Nerita turrita, RECLUZ, 1: 152, pl. 3, fig. 8. 1879 Nerita turrita, MARTENS, ed. о, 210): 105. 21.72. fig 5; ple Al fig. 18-21 1888 Nerita turrita, TRYON, 10: 37, pl. 11, fig. 1, 2. Espece à trés large répartition. Aucune localisation précise à l’intérieur de l'île de Madagascar n'est donnée dans la littérature. De même, c'est avec la seule indication Madagascar” que se trouvent, dans la collection du Muséum, des lots au nombre de sept, venant de Liautaut, 1843; Amiral de Hell, 1847: Cloue, 1850; Texor de Ravisi, 1853; Ballot, 1887; Largentiere, 1887; Denis, 1945. Neritina (Vittina) gagates Lamarck 1822 Neritina gagates, LAMARCK, 6(2): 185. 1828 Neritina caffra, GRAY, In: WOOD, pl. 8, fig. 10. 1877 Nerita caffra, ANGAS, p 527. 1879 Neritina gagates, MARTENS, ed. 2, 2(10): 94, pl. 16, fig. 11, 12; pl. 10, fig. 18, 19; pl. 13, fig. 8. 1882 Neritina gagates, SMITH, p 387. 1882 Neritina fulgetrum, SMITH (non REEVE), p 387, pl. 22, fig. 23, 24. MOLLUSQUES DE MADAGASCAR 343 1888 Neritina gagates, TRYON, 10: 35, pl. 10, fig. 77-79, 97, 98; pl. 11, fig. 6. 1890 Neritina (Neritaea) gagates, BOETTGER, 22: 99. 1914 Neritina gagates, ROBSON, 32: 377. 1929 Neritina gagates, DAUTZENBERG, 3: 526. 1929 Neritina (Neritina) gagates, HAAS, 57: 427. 1969 Neritina (Vittina) gagates, STARMUHLNER, 8: 61, fig. 63-66. Cette espéce était connue des provenances suivantes: Tsararano, Dautzenberg; Nossi- Bé, Dautzenberg, Starmühlner; Nossi-Comba, Boettger; Marodasatia (baie d'Antongil), Robson; Antanambe, Haas; Tamatave, Robson, Haas, Smith; Ekongo, Angas; St. Augustin, Starmühlner. Les collections du Muséum permettent d ajouter les provenances suivantes: rivière des Caïmans (Decary); Пе Nosy-Lava, pres Ananalava (Waterlot); Virembina (H. Soula, 1969); Antsiafapiana, 8 km S.S.O. de Maromandia dans la vallée de la Sahefihitra (H. Soula, 1969), Androhofary, 2 km environ au N.-O. d’Ambohibe (H. Soula, 1969); Ат- bohivoangibe, 3 km au N.-E. d Ampohibe pres Antsirabato pres Mohatsara (H. Soula, 1969); riviere Manambolosy (H. Bertrand, 1970); embarcadére de Marovoay, eau saumátre (С. Petit, 1926); riviere Soanierana, pres Tamatave (С. Petit, 1927); riviere entre Soanierana et Maningory Manansatrana (G. Petit, 1927); Tamatave (G. Petit); Foulpointe, riviere Onibe (Decary, 1920); Andevoranto, estuaire du Zaroka (С. Petit, 1926); riviére Sandramanongy (Brygoo, 1957); village Manakambahiny, canton Vatoman- Nossi-Be Riviere des Caimans Nossi- Comba | ns Ambanja Maromandıa Androhibe wa ans Virembina Antsiafapiana Ambatofotsy Maroansetra Andranomavo—® Entre Tamatave et Andratambe la Baie d'Antoneil no Fenerive -Tamatave FIG. 2. Distribution de Neritina pulligera Linné. 344 FISCHER-PIETTE ET VUKADINOVIC dry (Brygoo, 1957); eau saumátre d'un petit lac pres d’ Andrahomana (Mission Grandidier, 1901) et Marovary. On voit que les provenances connues а ce jour sont toutes sur la cóte ou а faible dis- tance, et sur toute la longueur de l'île. L'intérieur de l’île n'en a pas donnée. Voir notre carte Fig. 4. Maroantsetra Mananara Maintinand ry Sandrano — 4 SE Augustin FIG. 3. Distribution de Neritina auriculata Lk. MOLLUSQUES DE MADAGASCAR 345 Septaria (Septaria) borbonica Bory 1803 Patella borbonica, BORY DE St. VINCENT, 1: 287, pl. 37, fig. 2. 1816 Navicella elliptica, LAMARCK, (Vers), Expl. pl. 456, fig. 1. 1832 Navicella depressa, LESSON, p 386. 1843 Navicella Cookii, RECLUZ, р 197. 1850 Navicella suborbicularis, SOWERBY, 2: 551, pl. 117, fig. 3; pl. 118, fig. 30, 31. 1856 Navicella Cookii, REEVE, 9: pl. 4, fig. 14. Riviere des Caimans Tsararano Nossi-Bé Nossi-Comba NOoSSi-Lava — Virembina Marovoay Ansiafapiana— Androhofary Ambohivoangibe Entre Tamatave et Manambolosy la Baie A'Antongil Antanambe Soanierana Manansatrana _ Tamatave Foulpointe aes ae -Andevoranto Vatomandry | Sandramanoney lac Andrahomana E kongo Marovary st AUQUStin .— FIG. 4. Distribution de Neritina gagates Lk. 346 1860 1860 1860 1876 1576 1876 1877 1878 1881 1581 1581 1882 1587 1588 1589 1590 1892 1921 1929 1938 1956 1969 FISCHER-PIETTE ET VUKADINOVIC Navicella Cookii, MORELET, 2: 126. Navicella porcellana L., MORELET, 2: 119, 126. Navicella suborbicularis, MORELET, 2: 126. Navicella elliptica, MARTENS, 3: 252. Navicella suborbicularis, MARTENS, 3: 253. Navicella Cookii, MARTENS, 3: 253. Navicella suborbicularis, MORELET, 25: 344. Navicella porcellana, KOBELT, 5: 180. Navicella bimaculata, CROSSE, 29: 207. Navicella borbonica, MARTENS, ed. 2, 2(10a): 10, pl. 1, fig. 4-18. Navicella junghuhni Herkl., MARTENS, p 23, pl. 1, fig. 13-15. Septaria borbonica, MORELET, 30: 200. Septaria borbonica, MORELET, 35: 291, pl. 9, fig. 5. Navicella (Cimber) borbonica, TRYON, 10: 78, pl. 27, fig. 2-12. Navicella bimaculata, BOETTGER, 21: 41. Navicella borbonica var. depressa, BOETTGER, 22: 98. Septaria (Elara) suborbicularis, BAKER, 2: 33, No. 208. Septaria borboniciensis, GERMAIN, p 398. Septaria borbonica, HAAS, 57: 428. Septaria (Septaria) borbonica, WENZ, p 429, fig. 1055. Septaria borbonica, FRANC, 13: 26, pl, 3, fig. 26. Septaria (Septaria) borbonica, STARMUHLNER, 8: 76; fig. 85, p 78. Espece а tres large répartition. En ce qui concerne Madagascar, les auteurs l'ont citée de Nossi-Bé (Crosse; Martens; Boettger; Starmühlner), de Nossi-Comba (Crosse; Boettger) et d Antanambe (Haas). Nous y ajoutons Analalava (Waterlot) et Ivontaka (Decary, 1920). Ces provenances sont portées sur notre carte Fig. 5. 1822 1822 1856 1877 1877 1881 1883 1888 1888 1938 1938 Septaria (Navicella) lineata Lamarck - Navicella lineata, LAMARCK, 6(2): 182 (Encycl. méth., pl. 456, fig. 2). Navicella tessellata, LAMARCK, 6(2): 182 (Encycl. méth., pl. 456, fig. 3, 4). Navicella eximia, REEVE, 10: pl. 6, fig. 26. Navicella lineata, ANGAS, p 527. Navicella eximia, ANGAS, p 527. Navicella tessellata, MARTENS, ed. 2, 2(10a): 37, pl. 7, fig. 8-17; pl. 8, fig. 1-9. Septaria tessellata, MORELET, 31: 204. Navicella tessellata, TRYON, 10: 81, pl. 29, fig. 57. Navicella lineata, TRYON, 10: 82, pl. 29, fig. 58. Septaria tessellaria, CONNOLLY, p 601, pl. 17, fig. 20, 21. Septaria (Navicella) tessellata, WENZ, p 430, fig. 1057. Espèce а tres large répartition. Elle n'avait été citée de Madagascar, à notre con- naissance, que par Angas, а Ekongo. Nos collections nous permettent d’ajouter d'autres provenances, toutes sur la cóte Est (carte No. 5): Maroansetra (Brygoo, 1957); embouchure de la riviere Mananara (Decary, 1920); Foulpointe, riviere Onibe (Decary, 1920); canal des Pangalanes (Gaud, 1951); Maintinandry, riviere Sakamila (Brygoo, 1957); riviere Sandramanongy (Brygoo, 1957). 1758 1827 1829 1841 1879 1879 1919 Smaragdia viridis Linné Nerita viridis, LINNE, 10: 778. Nerita viridis, var., RANG, In: FERUSSAC, 10: 412. Neritina viridis, RANG, p 193. Nerita Rangiana, RECLUZ, p 339. Nerita viridis, MARTENS, ed. 2, 2(10): 246, pl. 4, fig. 14-19. Nerita Rangiana, MARTENS, ed. 2, 2(10); 249, pl. 23, fig. 27, 28. Nerita rangiana, ODHNER, 12(6): 33. MOLLUSQUES DE MADAGASCAR 347 Lokoube —O Nossi- Comba: Analalava Maroansetra e—Ankasakasa POSES e_ Maintirano Demoka Foulpointe Miandriva3o Canal des Palangalanes b Menale Maintinandry 16 att, Sandramanongy Morondava " АПК 5 ао e—Marja vf Andranomanintsy Lac Thotry Ekongo—A e—Finerena Tulear e Lanistes OVUM Pos var. orasseti Morel. A Septaria(Navicella) lineata Lam. HO Septaria borbonica sory FIG. 5. Distribution de Septaria borbonica Bory, Septaria lineata Lk. et Lanistes ovum Peters var. grasseti Mor. 348 FISCHER-PIETTE ET VUKADINOVIC 1921 Smaragdia viridis, GERMAIN, p 395. 1929 Smaragdia (Smaragdia) Rangiana, DAUTZENBERG, 3: 527. 1930 Smaragdia viridis, GERMAIN, 21: 683. Espece а répartition extrêmement large. Elle est citée aussi bien par des auteurs s occu- pant de faune terrestre que par des auteurs s occupant de faune marine. A Madagascar elle est connue depuis fort longtemps (Rang). Les provenances données sont: Tamatave (Odhner); Hellville, Ankatsepe et Majunga (Dautzenberg). Les divers lots de Madagascar de nos collections sont dépourvus de provenances précises. Smaragdia souverbiana Montrouzier 1863 Мегита Souverbiana, MONTROUZIER, 11: 75; 175, pl. 5, fig. 5. 1881 Neritina (Smaragdia) Souverbiana, CROSSE, 29: 208. 1883 Neritina Souverbiana, MORELET, 31: 204. 1888 Neritina (Smaragdia) Souverbiana, TRYON, 10: 55, pl. 18, fig. 93. 1929 Neritina (Smaragdia) Souverbiana, DAUTZENBERG, 3: 527. Ce n'est que parce qu'elle a été citée de Madagascar (Nossi-Bé) par Crosse et des Comores par Morelet dans des listes de Mollusques terrestres, que nous mentionnons ici cette espece marine à trés large répartition. Nous en avons des échantillons de Nossi-Bé (Jousseaume) et de Tuléar (Geay). Neritilia consimilis Martens 1879 Neritina consimilis, MARTENS, ed. 2, 2(10): 243, pl. 23, fig. 25, 26. 1883 Neritina consimilis, MORELET, 31: 202. 1888 Neritina consimilis, TRYON, 10: 54, pl. 18, fig. 86. 1921 Neritina (Neritilia) consimilis, GERMAIN, p 394. Espéce décrite de Maurice, connue aussi des Comores et qui n avait pas encore été citée de Madagascar. M. Waterlot en a récolté plusieurs dizaines d'échantillons 4 Ananalava, dans le Nord-Ouest de l'île. Genre Lanistes Y a-t-il d Madagascar 2 espéces de Lanistes, ou une seule? Les 11 lots que nous possedons, faisant au total 70 échantillons, appartiennent tous à une seule forme qui a été décrite par Morelet sous le nom Ampullaria Grasseti, de Madagascar, puis 4 nouveau, de l'Afrique orientale par von Martens, sous le nom plicosus, variété de L. ovum (Peters) Troschel. Nous sommes tout-ä-fait d'avis que cette forme se rattache effectivement а L. ovum. Mais il faut remarquer que Germain (1909) et Haas (1929) rattachent grasseti, non pas а ovum, mais а L. olivaceus Sow. Starmühlner cite de Madagascar deux espéces, ovum Trosch., et une autre qu il appelle “Lanistes (Meladomus) olivaceus (Sowerby, 1825) grasseti (Morelet, 1863),” il se con- forme donc a Haas pour cette deuxiéme espéce. Starmühlner dit, а la page 15 (note infrapaginale relative а la р 14), n avoir pas eu d'exemplaires de ces espéces. De sorte qu'il ne fait (р 118) qu'en donner des listes de références et dire quelques notes de répartition basées sur cette littérature: pour ovum, région de Tuléar (Andranohinaly); pour olivaceus, région de Majunga (Menabe). Dans ces conditions il п’а pas dü consacrer de temps a ces Lanistes!. Nous pensons donc que la présence de deux espéces n'est pas prouvée; et nous nous contentons de donner des références, et la distribution, de la forme costulée de L. ovum. Puisque nous avons cité Germain, qui considérait striatus comme une forme représen- tative de olivaceus, notons que nous avons divers lots d'Afrique orientale déterminés par 'Autrement, dans la liste synonymique de olivacea, il n'aurait pas cité Reeve, Conch. Icon., fig. 3, qui représente une Ampullaria et non un Lanistes. MOLLUSQUES DE MADAGASCAR 349 Germain, que toutes ses étiquettes portent: Lanistes striatus Martens, et que les nom- breux échantillons de ces lots sont tous des L. ovum var. Grasseti (=striata). Deux de nos exemplaires de Madagascar sont des échantillons d'auteur de L. Grasseti (coll. des types du Journal de Conchyliologie). Tous nos exemplaires (comme d’ailleurs ceux d'Afrique orientale dont nous venons de parler) sont de taille médiocre: le moins petit a 35 x 30 mm. Ils sont tous peu étirés, et peu variables de forme. Les chiffres 35 x 30 et 32 x 32 donnent les limites des proportions de la hauteur et de la largeur. Les cótes, le plus souvent, sont aussi écartées que sur la figure de Grasseti, mais elles peuvent étre aussi serrées que sur celle de plicosus de Kobelt (voir plus loin), et il y a des intermédiaires. Lanistes ovum var. grasseti Morelet 1851 Ampullaria ovum Peters, PHILIPPI, ed. 2, 1(20): 22, pl. 6, fig. 2. 1863 Ampullaria (Lanistes) Grasseti, MORELET, 11: 267, pl. 10, fig. 2. 1896 Lanistes ovum var. plicosus, MARTENS, p 167. 1896 Lanistes grasseti, MARTENS, p 167. 1909 Lanistes grasseti, GERMAIN, (5) 1: 125, 162. 1911 Meladomus grasseti, KOBELT, ed. 2, 1(20): 13, pl. 23, fig. 8, 9. 1911 Meladomus ovum plicosus, KOBELT, p 12, pl. 29, fig. 1-3. 1929 Meladomus olivaceus grasseti, HAAS, 57: 422. 1950 Ampullaria (Lanistes) Grasseti, FISCHER-PIETTE, 90: 22. 1969 Lanistes (Meladomus) ovum Troschel, STARMUHLNER, 8: 118. 1969 Lanistes (Meladomus) olivaceus grasseti, STARMUHLNER, p 118. Distribution. Nous portons sur une carte (Fig. 5) celles des localités que nous pu situer. On voit que L. ovum п’а été trouvé jusqu ici que dans la région Ouest de part et d'autre de Morondava, et en un point de la côte Est à la latitude de Morondava. Pila cecillii Philippi 1848 Ampullaria Cecillii, PHILIPPI, 5: 191. 1848 Ampullaria Largillierti, PHILIPPI, p 192. 1851 Ampullaria Largillierti, PHILIPPI, ed. 2, 1(20): 46, pl. 13, fig. 5. 1851 Ampullaria Cecillei, PHILIPPI, p 47, pl. 13, fig. 6. 1856 Ampullaria simplex, REEVE, 10, pl. 21, fig. 98a, b. 1856 Ampullaria Largillierti, REEVE, 10, pl. 23, fig. 109. 1856 Ampullaria Hanleyi, REEVE, 10, pl. 23, fig. 113. 1860 Ampullaria Cecillei, MORELET, 2: 108, 125. 1863 Ampullaria adusta Rve, TRISTRAM, p 60. 1881 Ampullaria Cecillei, CROSSE, 29: 206. 1882 Ampullaria madagascariensis, SMITH, p 384, pl. 22, fig. 8, 9. 1882 Ampullaria subscutata, MOUSSON, 30: 46, pl. 3, fig. 6. 1884 Ampullaria hanleyi, NEVILL, 2: 8. 1889 Ampullaria Cecillei, BOETTGER, 21: 51. 1889 Ampullaria Largillierti, BOETTGER, р 51. 1890 Ampullaria cecillei, BOETTGER, 22: 95. 1890 Ampullaria largillierti, BOETTGER, p 96. 1911 Pachylabra subscutata, KOBELT, ed. 2, 1(20): 57, pl. 33, fig. 8. 1911 Pachylabra largillierti, KOBELT, 1(20): 59, pl. 33, fig. 9. 1911 Pachylabra hanleyi, KOBELT, 59, pl. 33, fig. 10. 1911 Pachylabra simplex, KOBELT, 67, pl. 36, fig. 3. 1911 Pachylabra madagascariensis, KOBELT, 68, pl. 36, fig. 4-6. 1914 Ampullaria madagascariensis, ROBSON, 32: 380. 1919 Ampullaria madagascariensis, ODHNER, 12(6): 43. 1925 Ampullaria madagascariensis, ALDERSON, p 83, pl. 17, fig. 1-3. 1925 Ampullaria Largillierti, ALDERSON, p 84, pl. 17, fig. 4. 1925 Ampullaria subscutata, ALDERSON, p 91, pl. 18, fig. 7. 09 50 FISCHER-PIETTE ЕТ VUKADINOVIC 1925 Ampullaria Cecillei, ALDERSON, p 92, pl. 18, fig. 8, 9. 1929 Pachylabra cecillei, HAAS, 57: 419. 1929 Pachylabra madagascariensis, HAAS, 57: 421. 1969 Pila (Pila) cecillei, STARMUHLNER, 8: 119, fig. 153-156; carte 205, р 157. Mananjeba Diego-Suarez Nossi-BÉ т 0 Nossi- Comba Montagne des Francais Ambilobe E Ampampamena. Ambanje Ankarana ~ Analamaho Andrakata D Farahalana Andapa: SEIN RS Marojala —, Ampohafana | Ambodiangezoka Ampahana Majunga Andranolava Ambohiovanoy-s Antsahanoro Lac kinkony ne ¢ _ Marolambo]\ Antsadrarana kapiloza US 14, Fort- Beros \_Ambchitralalana Marovoay tans Satie ' een Besalam PY laboha30 er Maevatananaf — Lac Alaotra Tsarasaotra — Imerimandrosa Maintirano Mangabe Ambatof otsy —» Lil e Tananarive in *—Imerina/ Lac Itasy% .— Moramanoa Miandrivazo Ambatolampy Sandramanoney -Antsirabe Saka fotsy. Mananjary Marovare—e FIG. 6. Distribution de Pila cecillei Philippi. MOLLUSQUES DE MADAGASCAR 351 Espece décrite de Madagascar. Starmühlner en a mis d'autres régions dans sa syn- onymie. Nous nous limitons ici а la forme de Madagascar. Cette derniére a elle-méme recu plusieurs noms, que Starmúhlner a mis en synonymie. Les exemplaires de Madagascar sont assez peu variables pour ce qui est de la forme générale. La plupart sont conformes a la figure de Largillierti donnée par Philippi (1851); certes il y en a qui sont plus étroits, comme sur la figure de Cecillei (sur la méme planche de Philippi), mais nous ne connaissons, de cette derniére forme, que des individus de taille faible, tandis que la forme plus gonflée se rencontre chez des exemplaires de toute taille. La forme de l'ouverture est un peu variable. L'ombilic l’est davantage: certains exemplaires sont imperforés; la plupart ont un ombilic ouvert mais de diametre assez fai- ble; mais nous avons un lot, récolté par Perrier de la Bathie 4 Majunga, dont un des in- dividus, de 38 mm de haut sur 36 de large, a un ombilic de 3,5 mm (tandis que chez d'autres exemplaires du méme lot, il peut étre peu ouvert). Au point de vue de la sculp- ture, ce lot, fait de 4 échantillons, est trés particulier: les lignes de croissance sont franche- ment saillantes, comme autant de côtes, tres visibles à l'oeil nu: elles sont aussi saillantes que celles des Lanistes ovum var. plicosa, tout en étant bien plus serrées. Ce trait peu faire penser а la description, par Reeve, de Ampullaria filosa. Mais cette espéce est imperforée, tandis qu ici l'ombilic est ouvert ou trés ouvert. Ces individus ne montrent pas de sculpture spirale. D'autres en ont une, qui peut étre bien moins saillante que la sculpture de croissance (elle-même trés peu marquée en général), ou aussi saillante, ou plus saillante sur les premiers tours rarement conservés in- tacts). Nous avons un exemplaire, de 51 mm de haut sur 48 de large, récolté par J. Millot a Moramanga (centre-Est de Madagascar), qui sur le dernier tour a une trés visible sculp- ture croisée, faite de nombreuses costules de croissance peu saillantes, et de cótes spirales, bien moins nombreuses mais bien plus saillantes, au nombre de 13, dont l’&cartement est assez variable. Le plus grand de nos échantillons de Madagascar récolté lui aussi par J. Millot а Moramanga, a 69 mm de haut sur 61 de large. Distribution. Nous portons sur une carte (Fig. 6) les localités que nous avons pu situer, tant celles que fournissait la littérature, que celles, bien plus nombreuses, qu y ajoutent nos collections (comparer avec la carte donnée par Starmühlner, 1969, р 157). On voit que les points de récolte connus à ce jour, sont assez nombreux sauf dans la partie Sud. Cleopatra amaena Morelet 1851 Melania amaena, MORELET, 2: 192, pl. 5, fig. 9. 1909 Cleopatra amoena, KOBELT, ed. 2, 1(21A): 396, pl. 76, fig. 15. La description de Morelet est suivie de ce renseignement sur l'habitat: “Palustria ad orientem insulae Madagascar.” En 1860, dans la Série Conchyliologique No. 2, Morelet, dans un article sur les Iles Orientales de l'Afrique, écrit (р 117): “La Melania amaena provient de Zanzibar et des Séchelles,” sans faire mention de Madagascar. Haas, 1929, p 425, aprés avoir rappelé que Morelet a décrit son espéce de Madagascar, écrit: “doch später (1860, р 117u.125) ändert er seine Angabe in Seychellen und Sansibar um, was nach v. Martens (Besch. Weicht. Dtsch. O.-Afr., 1898, p 187) für Sansibar richtig ist; weder auf den Seychellen noch auf Madagascar ist Cl. amoena wiedergefunden worden, wohl aber öfters auf Sansibar. Sie kann also endgültig als nicht zur madagassischen Tierwelt gehörig betrachtet werden.” Cette opinion de Haas pouvait passer a priori pour trop catégorique, pour les deux raisons suivantes. La premiére est que Morelet, en donnant en 1860 des provenances de Zanzibar et des Seychelles, n'a pas dit que cela annule la premiére provenance qu ‘il (we) | bo FISCHER-PIETTE ET VUKADINOVIC avait donnée, Madagascar. La seconde est que cette provenance de Madagascar était assortie de détails d'habitat du genre de ceux qui généralement impliquent l'authenticité. En tous cas, nous croyons pouvoir rapporter а cette espéce deux échantillons marqués de Madagascar, l'un sans autre précision, de Decorse (1900) dont nous avons beaucoup d'autres récoltes effectuées sans conteste à Madagascar, l’autre envoyé en 1901 par Petit, médecin а Morondava, dont les autres récoltes que nous avons viennent de la région méme de Morondava. On pourrait hésiter sur cette détermination, car les 2 specimens sont plus ou moins carénés, or nous n avons pas trouvé mention de caréne dans la littérature. Mais la forme générale correspond tres bien et les tours sont si peu bombés que nous ne voyons guere de quelle autre espéce il pourrait s'agir, et la ceinture colorée du dernier tour (visible en mouillant) est semblable. La caréne, sur l'échantillon du Dr. Petit, est une simple rup- ture de courbe de la surface, qui se voit sur le dernier tour et sur la fin de l'avant-dernier tour. Sur l'échantillon de Decorse elle se discerne sur tout l'avant-dernier tour, mais sur le dernier elle disparait rapidement. Etant donnée la grande variabilité de la sculpture chez certaines espéces de Cleopatra, nous ne pensons pas que ces faibles carénes constituent un obstacle а notre détermination. Nous donnons des figures de ces échantillons (Fig. 7, 8). Ainsi, l’espece est connue des marécages de l'Est, et de la côte Ouest, mais on peut penser qu elle est beaucoup plus rare à Madagascar que la plupart des autres formes fluviatiles. Cleopatra (Cleopatra) colbeaui Craven 1880 Paludina colbeaui, CRAVEN, p 216, pl. 22, fig. 5. 1880 Paludomus madagascariensis, BROT, (non Crosse & Fischer), ed. 2, 1(25): 48, pl. 8, fig. 7. 1881 Paludina Colbeaui, CROSSE, 29: 206. 1888 Paludina moniliata, PAETEL, p 424. 1889 Cleopatra colbeaui, BOETTGER, p 51. 1890 Cleopatra mangoroensis, ANCEY, 7: 344. 1929 Cleopatra colbeaui, HAAS, 57: 424, pl. 2, fig. 24. 1969 Cleopatra (Cleopatra) colbeaui, STARMÜHLNER, 8: 184, 185, 200, fig. 244. FIG. 7,8. Deux échantillons de Cleopatra amaena Mor. X 2. / FIG. 9. Distribution de Cleopatra colbeaui Craven. - MOLLUSQUES DE MADAGASCAR 353 Distribution. Cette espéce semble n'exister qu'à Madagascar. La littérature donne 4 provenances, Nossi-Bé (Craven, 1880); Périnet (Starmiihlner, 1969); Beforona (Star- mühlner, 1969); fleuve Mangoro (Апсеу, 1890). Les localités que nous permettent d'ajouter les collections du Muséum sont, du Nord au Sud: Diego-Suarez (Waterlot); Montagne des Francais (Waterlot); Nossi-Comba (G. Petit, 1920); Mizdioko (J. Millot, 1948); Mont Tsaratanana (Paulian, 1951); Antsiraka (Brygoo, 1957); Ankasakasa (Decary, 1930); Doany (H. Soula, 1969); riviére Kapiloza (G. Petit, 1926); Namoroko (Perrier de la Bathie); Iabohazo (Waterlot); Andonaka (Dr. Brygoo, 1957); ilot Anosy, lac Alaotra (Decary, 1921); Fenerive (Brygoo, 1957); Sahamany (Brygoo, 1957); Ifontsy (Brygoo, 1957); Bemaraha (Decary, 1921); Périnet (Brygoo, 1957); Manambolo (Brygoo, 1957); Beforona (Brygoo, 1957); Fananzanana (Brygoo, 1957); Anosibé (J. Millot, 1948); Ambodinonoka (Brygoo, 1957); Mangoro (Gaud, 1951); entre Anosibé et Moramanga (J. Millot, 1953); Volove (Brygoo, 1957); Mahanoro (Gaud, 1951); Onive (Brygoo, 1957); Andonabe (Brygoo, 1957); Mahabo (Brygoo, 1957); Ankilizato (Brygoo, 1957); Цотатру (Brygoo, 1957); Andasibe (Brygoo, 1957). Ces localités, avec celles de la littérature, sont portées sur notre carte Fig. 9. En plus, une provenance de la collection du Muséum п’а pu étre située par nous, c est: sommet Ihovika, 100 m altitude Est (Perrier de la Bathie). Cleopatra grandidieri Crosse & Fischer 1872 Paludomus Grandidieri, CROSSE & FISCHER, 20: 209. 1878 Paludomus Grandidieri, CROSSE & FISCHER, 26: 73, pl. 1, fig. 3, fig. 4 (var. submitica). 1880 Paludomus Grandidieri, BROT, ed. 2, 1(25): 45, pl. 8, fig. 3, 3a. 1914 Paludomus Grandidieri, ROBSON, p 378. 1929 Cleopatra grandidieri, HAAS, 57: 423. 1950 Paludomus Grandidieri, FISCHER-PIETTE, 90: 78, 150. 1969 Cleopatra (Cleopatra) grandidieri, STARMUHLNER, 8: 205, fig. 267. Distribution. Il semble que cette espéce ne se trouve qu à Madagascar. Les provenances connues, ou du moins celles que nous avons situées, se trouvent portées sur notre carte Fig. 10, qu il s'agisse des données de la littérature, ou de celles, plus nombreuses, que nos collections y ajoutent. Elles sont presque toutes dans la région moyenne des cótes Est, toutefois les provenances de Majunga et de Tuléar permettent de penser que nous n avons encore qu une documentation incomplete. Cleopatra (Cleopatra) madagascariensis Crosse & Fischer 1872 Paludina madagascariensis, CROSSE & FISCHER, 20: 210. 1882 Cleopatra trabonjiensis, SMITH, p 384, pl. 22, fig. 10, 11. 1894 Cleopatra carinulata, DAUTZENBERG, 42: 105, pl. 4, fig. 4. 1906 Cleopatra multilirata, ANCEY, 20: 45. 1914 Cleopatra trabonjiensis, ROBSON, 32: 377. 1929 Cleopatra madagascariensis, HAAS, 57: 423, pl. 2, fig. 21-23. 1950 Paludina madagascariensis, FISCHER-PIETTE, 90: 78; 180, pl. 5, fig. 75-77. 1969 Cleopatra (Cleopatra) madagascariensis, STARMUHLNER, 8: 201; fig. 263, 264, p 202; fig. 261, р 200. Il semble que cette espéce ne vive qu'à Madagascar. Les provenances données par la littérature étaient, du Nord au Sud: Ambohimarina (Dautzenberg, 1894); Nossi-Bé (Star- mühlner, 1969); Majunga (Haas, 1929); Trabonjy (Smith, 1882); Lac Alaotra (Robson, 1914); Vinaninony (Ancey, 1906). Les matériaux du Muséum nous permettent d'ajouter beaucoup d autres localités. Les unes et les autres sont portées sur notre carte de la Fig. 11. On voit que cette espéce, existe du Nord au Sud et de l'Est à l'Ouest, avec des provenances un peu plus nombreuses dans l'Ouest que dans | Est. 354 FISCHER-PIETTE ЕТ VUKADINOVIC FIG. 10. Distribution de Cleopatra grandidieri Crosse et Fischer. Majunga Manjakandriana Ansage Bie geal lig Vatomandr —89 Ambinanindrano—e ~ , Ambodiara Ivolo Ambohimanga—e Sakleony Ranomafana-e °— Masora Namorona Fort Carnot, ite.) == ananjar Y a Tulear lantara MOLLUSQUES DE MADAGASCAR 355 Ambilobe Anivorano Ambohimarina Tsararano Nossi- Be Nossi- Comba Ambanja | e < МЕ Tsaratanana Antohihy Beanoona : Sambirano Belambo Mariarano ma . + Ankijanibe | Pealan Maroala Marofinaritra Marovo cil as | Ankara! tantsika va = Trabony — Io 4 Ankarana Kapiloza a Tampolo Namoroka Boina ¢ Ankirihitra Lazafo Bekodoka Taboha30 ere Ambatondrazaka Mananoro AE Bemaraha Lac Alaotra RenEirans }. Miandriva3o Andreba e— lily Entre Anosibe Bekily -— et Moramanpa N р Marofandilia Vinaninony Vatomanary Morondava lac Andranomena Mahaloo e *—Fitampito Ankelizato' Ankotrofotsy Man akana *— Bemarivo Ifanadiana onto ve А Fianarantsoa MIN e-Ihosy Amloalavao Manombo 7 Fiherena _ betroka Tulear tiok Se ee e Tongobory Esira Tsivory Marontsiraka FIG. 11. Distribution de Cleopatra madagascariensis Crosse et Fischer (les points de récolte sans nom sont situés loin d'un village). 356 FISCHER-PIETTE ЕТ VUKADINOVIC Viviparus unicolor Olivier 1804 Cyclostoma unicolor, OLIVIER, 2: 39, pl. 31, fig. 9. 1852 Paludina biangulata, KUSTER, ed. 2, 1(21): 25, pl. 5, fig. 11, 12. 1909 Vivipara unicolor, KOBELT, ed. 2, 1(21A): 162, pl. 4, fig. 12, 13; pl. 5, fig, 11, 12. Nous avons trouvé dans les matériaux indéterminés du Muséum un exemplaire (Fig. 12) de Viviparus récolté еп 1900 par Decorse а Majunga. Nous le rapportons а У. unicolor Oliv. On sait que cette espéce est trés variable, dans sa forme générale et dans le fait qu'elle peut être pourvue d'une ou plusieurs carénes ou nen présenter aucune. Notre specimen est trés analogue а la figure de Paludina biangulata de Kiister (1852), que Kobelt (1909) a mis dans la synonymie de У. unicolor; cet auteur nous dit que biangulata, décrite d habitat inconnu, a été trouvée par Martens en Afrique orientale allemande. Madagascar est assez loin de cette région. Aussi pourrait-il y avoir doute sur la valeur de notre determination. Pour qu'on puisse en juger, nous décrirons notre échantillon en détail et nous le figurerons. Mais, а nos yeux, en ce qui nous concerne, cet habitat n'a rien d'anormal: nous sommes en effet persuadés que У. unicolor, décrit d'Egypte, se trouve jusqu'en Afrique du Sud, quels que soient les noms variés que cette espéce ait reçus en Afrique orientale. Hauteur 17 mm; largeur maxima 13 mm; ouverture ayant 8,5 sur 6,5 mm; couleur un- iformément verdatre; 5 tours, étagés par un aplatissement du haut de chacun. La bordure de cet aplatissement est une caréne bien individualisée en un cordon saillant. Une deuxième caréne apparaît à partir du sommet de | ouverture, de sorte que le dernier tour a un aspect bi-anguleux. Cette deuxiéme caréne est bien moins individualisée que I autre, et s atténue beaucoup en arrivant à | ouverture. A mi-distance entre ces deux carénes se voit une faible côte spirale. Avec une forte loupe, on constate l'existence d'une fine striation spirale de toute la surface, un peu plus forte sur la base, qui croise les irréguliéres cótes de croissance. I] n'y а pas d ombilic. Melanatria fluminea Gmelin 1767 Buccinum flumineum, GMELIN, 13: 3503. 1822 Pirena spinosa, LAMARCK, 6: 172. 1838 Melanopsis spinosa, POTIEZ & MICHAUD, p 351. 1838 Melanopsis Lamarckii, POTIEZ & MICHAUD, p 351. 1840 Melania madagascariensis, GRATELOUP, 11: 167, pl. 4, fig. 7. 1840 Melania duisabonis, GRATELOUP, 11: pl. 4, fig. 8. 1840 Melania bicarinata, GRATELOUP, 11: pl. 4, fig. 9. 1842 Pirena spinosa, SGANZIN, 3: 19. 1851 Pirena sinuosa, PHILIPPI, p 91. 1859 Pirena (Melanatria) spinosa, CHENU, 1: 298, fig. 2082. 1859 Pirena (Melanatria) granulosa Lk., CHENU, 1: 298, fig. 2081. 1859 Pirena spinosa, REEVE, 12: pl. 2, fig. 9. 1859 Pirena fluminea, REEVE, 12: pl. 2, fig. 10. 1859 Pirena maura, REEVE, 12: pl. 2, fig. 6. 1859 Pirena plicata, REEVE, 12: pl. 2, fig. 11. 1859 Pirena lingulata, REEVE, 12: pl. 2, fig. 7. 1860 Pirena fluminea, MORELET, 2: 118, 126. 1860 Melania bicarinata, MORELET, 2: 125. 1860 Melania Duisabonis, MORELET, 2: 126. 1860 Pirena Lamarckii, MORELET, 2: 126. 1860 Pirena madagascariensis, MORELET, 2: 126. 1860 Pirena sinuosa, MORELET, 2: 126. 1862 Pirena Debeauxiana, CROSSE, p 402, pl. 13, fig. 6. 1863 Pirena (Melanatria) spinosa, TRISTRAM, р 60. 1867 Melanatria fluminea, GRAY, 3: 330. MOLLUSQUES DE MADAGASCAR 357 ЕТС. 12. Viviparus unicolor Oliv. X 2. 1868 Pirena aspera, BROT, p 49, pl. 1, fig. 6. 1874 Melanatria spinosa, BROT, ed. 2, 1(24): 401, pl. 42, fig. 1, la-c. 1874 Melanatria fluminea, BROT, 1(24): 402, pl. 42, fig. 2, 2a, 2b, 3; pl. 43, fig. 1, la, 2, 2a-c, 3. 1874 Melanatria Debauxiana, BROT, 1(24): 404, pl. 43, fig. 4. 1874 Melanatria Goudotiana, BROT, 1(24): 405, pl. 44, fig. 1, la. 1874 Melanatria Madagascariensis, BROT, 1(24): 406, pl. 43, fig. 5, 5a-c. 1882 Doryssa (Melania) Audeberti, MOUSSON, 30: 47, pl. 3, fig. 7. 1882 Melanatria fluminea, MOUSSON, 30: 183. 1882 Melanatria johnsoni, SMITH, p 383, pl. 22, fig. 6, 7. 1890 Melanatria madagascariensis, BOETTGER, 22: 97. 1894 Melanatria madagascariensis, DAUTZENBERG, 42: 104. 1902 Pirena spinosa, DAUTZENBERG, 27: 199. 1908 Melania madagascariensis, FULTON, 8: 43, 44. 1914 Melanatria fluminea, ROBSON, 32: 378. 1914 Melanatria Johnsoni, ROBSON, 32: 378. 1919 Melanatria spinosa, ODHNER, 12: 43. 1928 Melanatria fluminea, THIELE, 55: 385. 1929 Pirena fluminea, HAAS, 57: 425. 1929 Pirena spinosa, HAAS, 57: 425. 1929 Pirena madagascariensis, HAAS, 57: 425. 1950 Pirena debeauxiana, FISCHER-PIETTE, 90: 20. 1969 Melanatria fluminea, STARMUHLNER, 8: 159, fig. 206-208; fig. 241, p 182. 1969 Melanatria madagascariensis, STARMUHLNER, 8: 182, fig. 241-243. Le grand nombre d'échantillons dont nous disposons, nous a permis de nous rendre compte qu'il n'existe à Madagascar qu'une seule Melanatria, tres variable, en particulier pour les côtes, longitudinales ou spirales et qui souvent sont d'un systeme а un âge et d'un 358 FISCHER-PIETTE ЕТ VUKADINOVIC autre à un autre âge, pour la convexité des tours, le degré d'épaulement des tours, les pointes que cet épaulement peut porter, et aussi pour la forme de | ouverture, dont le bord externe peut étre peu sinueux ou trés sinueux. Sur un méme individu, а ouverture tres sinueuse, on peut constater а peu de distance en arriére le tracé peu sinueux qui a précédé. Les noms dús а Reeve laissaient un doute du fait des provenances données par lui, en Сар dAmbre Diego- Suarez Nossi-Be | Montagne des Francais Virembina Andranomaiaza(Maromandia) N Ambohianoibe h Doan Ampampamena Andapa* re Ambato \ Analantsoa , A \ ohafana Antalaha Tsitampiky Amp lias «\ Andranonakcho > Ankarafantsika Ambohivoangy Hort & Beronono Ranolalina laboha3o Marovoay Mananara Ankirihitra Ivontaka Somoromahitra ste Marie Antsinjy Lac Alaorra? Sahatavy $ Fostimano—®* Ivoloina vondahy ——e Andravondahy » betampona Vohibary Antsalova а Ambila Manjakandriana * Andratambe vatomandry .—® belo u Moramanga Ambinanindrano-* Manampotsy —Mahnanoro Fort-Carnot Inosy Mananjary $ Manambia Marovary Ankotofotsy Ranomafana Тъака Fort- Dau phin Manambaro FIG. 13. Distribution de Melanatria fluminea Gmelin (les points de récolte sans nom sont situés loin d'un village). MOLLUSQUES DE MADAGASCAR 359 Afrique occidentale. Mais il s agissait d'exemplaires de Cuming, ог cet excellent récolteur, tres peu lettré, n'indiquait souvent les provenances qu aprés-coup, et les erreurs d'origine sont ainsi fort courantes en ce qui le concerne. C'est aussi de Cuming que Crosse tenait l’exemplaire (que nous avons en mains, coll. des types de Journal de Conchyliologie) qu il a décrit comme Pirena Debeauxiana: il était, lui aussi, censé venir d’ Afrique occidentale. Distribution. La littérature donne les provenances suivantes: Nossi-Bé (Philippi, 1851); Ranomafana (Tristram, 1863); Tamanarivo (Brot, 1874); riviere Kamony (Smith, 1882); Montagne des Francais (Dautzenberg, 1894); riviére Fanjahira (Dautzenberg, 1902); en- tre Matilasy et Mangoro; source de la riviére Ihovika; Belolondyi et Tandrahu (Robson, 1914); Tamatave (Odhner, 1919); Ivohibé, Karimbela; Anharimbelo; Marinabo; Sakana (Haas, 1929); ruisseau Sakanofa et ruisseau Isaka (Starmühlner, 1969). Ces diverses provenances ont été réunies par Starmiihlner sur une carte (fig. 241, p 182), pour l'ensemble de М. fluminea et М. madagascariensis qu'il considérait comme deux espéces distinctes. Elles sont situées dans le Sud-Est; dans la région de Tamatave; a Tananarive; et ä la pointe Nord y compris Nossi-Bé. Les collections du Muséum nous ont procuré beaucoup d autres provenances dont nous donnons les emplacements (ceux, du moins, que nous avons pu situer) sur notre Fig. 13. On constate que Гезрёсе est présente aussi bien à l'Ouest qu'à | Est; qu à l'Est elle se trouve jusque dans le Nord-Est compris; et qu il n y a que la région axiale de Vile qui jusqu ici est presque en blanc, ne contenant que quelques provenances. Thiara (Thiara) amarula L. 1758 Helix amarula, LINNE, ed. 10: 774. 1822 Melania thiarella, LAMARCK, 6: 166. 1850 Melania cornuta, LEA, p 194. 1860 Melania amarula, MORELET, 2: 111. 1874 Melania amarula Brug., BROT, ed. 2, 1(24): 289, pl. 29, fig. 1, la-g. 1874 Melania thiarella, BROT, 1(24): 291, pl. 29, fig. 3, 3a, b. 1877 Melania amarula, ANGAS, p 527-530. 1877 Melania amarula Brug., MORELET, 25: 343. 1879 Melania thiarella, MORELET, 27: 312. 1881 Melania thiarella, CROSSE, 29: 207. 1882 Melania amarula Brug., MORELET, 30: 199. 1889 Melania (Tiara) tiarella, BOETTGER, 21: 53. 1890 Melania (Thiara) tiarella, BOETTGER, 22: 98. 1910 Melania amarula, KOBELT, 32: 92 1910 Melania cornula, KOBELT, 32: 92. 1914 Melania amarula Brug., ROBSON, 32: 379. 1919 Melania cybele Gould, ODHNER, 12: 43. 1921 Melania amarula, GERMAIN, p 358. 1928 Melania amarula, THIELE, 55: 397. 1929 Melania amarula, HAAS, 57: 426. 1929 Melania coacta Meusch., HAAS, 57: 427. 1938 Thiara vouamica Bgt., CONNOLLY, p 564. 1956 Melania amarula Brug., FRANC, 13: 57, fig. 74. 1969 Thiara (Thiara) amarula, STARMUHLNER, 8: 208: fig. 272-275, p 209; carte p 182. Espece répandue de | Afrique du S.-O. à l'Australie. Pour ce qui concerne Madagascar, la bibliographie donne les provenances suivantes: Ekongo (Angas, 1877); Nossi-Bé (Crosse, 1881; Starmühlner, 1969); Nossi-Comba (Boettger, 1890); entre Tamatave et la baie d'Antongil (Robson, 1914); Androhibe (Odhner, 1919); Tamatave (Haas, 1929); Karimbela (Haas, 1929). Les lots de la collection du Muséum permettent Фу ajouter les provenances suivantes: Diego-Suarez (Ballot, 1887); riviere des Caimans (Decary); Bas-Sambirano (J. Millot, 1945); Maromandia (Decary, 1922); Andaribé (Mme. Bouchard, 1969); Maroansetra 360 FISCHER-PIETTE ET VUKADINOVIC Die go- Suarez Nossi-Be ? Riviere desCaimans Nossi-Comba & | ine e————Bas-Ssambirano Maromandia Andaribe Maroansetra Bndronibe == S een Tamatave et Lvontaka Baie d’Antongil Y Mahambo Andreba —e Tamatave Canal des Palangalanes Sand ramanongy ЕКОМОО Karimbela FIG. 14. Distribution de Thiara amarula L. MOLLUSQUES DE MADAGASCAR 361 (Brygoo, 1957); Ivontaka (Decary, 1920); Mahambo (С. Petit, 1920); Andreba (Brygoo, 1957); canal des Pangalanes (Gaud, 1951); Sandromangy riviére (Brygoo, 1957). Ces diverses localités, celles qui étaient connues et celles que nous ajoutons, sont portées sur une carte (Fig. 14). Ces lieux de récoltes sont bien moins nombreux que ceux de l’espéce indigéne Melanatria fluminea: ils sont répartis sur le pourtour de [Ге dans ses parties Nord et Est. Melanoides tuberculatus Miller 1774 Nerita tuberculata, Müller, р 191. 1786 Nerita tuberculata, CHEMNITZ, 9: 189, pl. 136, fig. 1261, 1262. 1860 Nerita commersoni, MORELET, 2: 116, pl. 6, fig. 4. 1860 Nerita tuberculata, MORELET, 2: 126. 1864 Nerita psorica, MORELET, 12: 287. 1889 Nerita (Striatella) tuberculata, BOETTGER, 21: 52. 1914 Nerita tuberculata, ROBSON, 32: 379. 1929 Melanoides tuberculatus, HAAS, 57: 427. 1935 Melania (Melanoides) tuberculata, GERMAIN, (10), 18: 445. 1958 Melanoides tuberculata, BRYGOO, 26: 86. à 1969 Melanoides (Melanoides) tuberculatus, STARMUHLNER, 8: 224; fig. 293-294, p 209: carte 319, p 242. Cette espéce est une de celles qui sont les plus répandues dans le monde. Pour Madagascar la carte publiée par Brygoo et reproduite par Starmühlner ne donne de nom- breuses localités que dans le Sud. Nous avons des récoltes qui nous montrent que cette es- péce est trés abondante dans toute l’île. Nous jugeons inutile de traduire ce renseignement sur une carte, et méme de donner la liste de ces localités. Cerithidea decollata Brug. 1842 Cerithium decollatum Brug., KIENER, p 96, pl. 28, fig. 2 1855 Cerithium decollatum L., SOWERBY, 2: 886, pl. 186, fig. 274. 1860 Melania decollata Lk., MORELET, 2: 116, 125. 1866 Cerithidea decollata, L., REEVE, 15: pl. 2, fig. 14. 1881 Melania decollata Lk., CROSSE, 29: 207. 1887 Potamides (Cerithidea) decollatus L., TRYON, 9: 161, pl. 32, fig. 54. 1890 Cerithidea (Pirenella) decollata Lk., BOETTGER, 22: 97. 1894 Cerithidea decollata L., DAUTZENBERG, 42: 91. 1929 Potamides (Cerithidea) decollatus L., DAUTZENBERG, 3: 489 1929 Cerithidea decollata Brug., HAAS, 57: 427. 1969 Cerithidea decollata, Brug., STARMUHLNER, 8: 243. Nous ne nous sommes pas chargés d'essayer de résoudre la question, fort difficile, de savoir quel est l’auteur de Гезрёсе de Cerithidea qui habite les côtes de Madagascar (et se trouverait jusqu en Australie). Nous nous sommes contentés de donner les références aux figures auxquelles ressemblent les exemplaires que nous avons en collection et d'en représenter un Fig. 15. Pour cette raison, nous n avons pas indiqué, bien que Starmühlner la cite, la figure de Brot (Conch. Cab., pl. 7, fig. 10), qui ne représente certainement pas Гезрёсе digurée par Kiener (ce serait plutöt Melanatria fluminea). Les provenances malgaches trouvées dans la littérature sont les suivantes: Nossi-Bé (Morelet, 1860); Diego-Suarez (Dautzenberg, 1894); Amboaniva (Dautzenberg, 1929); riviere des Catmans (Id.); Tuléar (Id. ). Les collections du Muséum permettent d'ajouter: Ambanja (Paulian, 1951); Bas- Sambirano (J. Millot, 1945); Ananalava (Waterlot, 1925); Ambongo (J. Millot, 1948); Besalampy (Decary, 1938); Morondava et Morombé (Brygoo, 1957). On voit sur notre carte (Fig. 16) que cette espéce des eaux saumátres a surtout été récoltée sur la cóte Nord-Ouest et Ouest. 362 FISCHER-PIETTE ET VUKADINOVIC FIG. 15. Cerithidea decollata, X 1, 5. _Diego-Suares s Gé |- Бе Е = NOSSI-B Riviere des Caımans Ambanja Amboaniva Bas-Sambirano — 7 Besalampy Morondava Tulear- FIG. 16. Distribution de Cerithidea decollata. MOLLUSQUES DE MADAGASCAR 363 Radix (Radix) hovarum Tristram 1863 Limnaea hovarum, TRISTRAM, p 61. 1882 Limnaea hovarum, SMITH, p 385. 1882 Limnaea electa, SMITH, 385, pl. 22, fig. 12, 13. 1894 Limnaea suarensis, DAUTZENBERG, 42: 100, pl. 4, fig. 3. 1914 Limnaea hovarum, ROBSON, 32: 280. 1920 Limnaea hovarum, GERMAIN, p 160. Ambilobe Ampotsihy /_Diego-Suarez Ambanje (27 & baie cles Amis Bas E Ankatafa Nossi-Be Analalava à |///-Ankarana Ambondrona MW epi Mahabo Tsinjomitondraka $* Mont. Tsaratanana Manaratsandra e à Ambalavelona Amparangidro Mohakibokely R Ankaboka Ankazombrona| A DN мым]. I jure || Antsohiny N Bemarivo Soalala a. er ge Jang Ankasakasa NS $ Mandritsara Manakana Marovoay Antsirabe Ambato-Boeni*\ \Tsararano Maevatanana-, befotoana р à с Alaotr: anna ES otra : Marovato Ikopa eo Tamatave 5 Ambatondrasaka Miandrivazo N e- Miarinarivo Ambila Ankavandra- Manak ambahiny er Bekily Anosibe Vatomandry Maintinandr Morondava e-Mananjaka Mahanoro Analafaly У bande ana e— Andrianombo Ambila \anonhony- Betroka Betioky Tsivory Manaravolo-——e Marohotro Amboasary Ambovombe FIG. 17. Distribution de Bulinus mariei Crosse. 364 FISCHER-PIETTE ET VUKADINOVIC 1957 Lymnaea hovarum, RANSON, (34): 25 1958 Lymnaea hovarum, BRYGOO, 26: 75 1969 Radix (Radix) hovarum, STARMUHLNER, 8: 244-268; fig. 321, 322, р 246; carte, р 267. Aux trés nombreuses provenances qui étaient connues, les collections de Paris et Bruxelles en ajoutent un si grand nombre, qu il devient inutile de donner une nouvelle carte de localités. Il suffit de savoir maintenant que Гезрёсе existe dans toute l'île. Bulinus (Bulinus) liratus Tristram 1863 Physa (Ameria) lirata, TRISTRAM, p 60, text-fig. 1877 Physa madagascariensis, ANGAS, p 528, pl. 54, fig. 2. 1882 Physa madagascariensis. SMITH, p 386, pl. 22, fig. 18, 19. 1882 Physa lamellata, SMITH, p 386, pl. 22, fig. 14, 15. 1882 Physa obtusispira, SMITH, p 386, pl. 22, fig. 16, 17. 1886 Physa madagascariensis, CLESSIN, ed. 2, 1(17): 282, pl. 40, fig. 6. 1886 Physa Hildebrandti, CLESSIN, 1(17): 351, pl. 49, fig. 9. 1920 Bullinus (Isidora) liratus, GERMAIN, p 161, fig. 8-11. 1920 Bullinus (Isidora) madagascariensis, GERMAIN, p 163. 1953 Bulinus liratus, GRJEBINE € MENACHE, 8: 87. 1957 Bulinus liratus, RANSON, (34): 16. 1958 Bulinus liratus, BRYGOO, 26: 60. 1969 Bulinus (Bulinus) liratus, STARMUHLNER, 8: 268-288; He 353, p 270; fig. 386, p 288. Distribution. Les cartes publiées par Brygoo, Ranson et Starmühlner sont déjà assez fournies. Nous aurions encore beaucoup d autres localités а faire connaitre, qu il nous semble inutile de les énumérer. Qu il nous suffise de dire que cette espéce se trouve en abondance dans toute l'île. Bulinus (Pyrgophysa) mariei Crosse 1879 Pyrgophysa Mariei, CROSSE, 27: 209. 1880 Pyrgophysa Mariei, CROSSE, 28: 141, pl. 4, fig. 5. 1881 Pyrgophysa Mariei, CROSSE, 29: 202. 1889 Pyrgophysa Mariei, CROSSE & FISCHER, In: GRANDIDIER, 14: pl. 24, fig. 5. 1889 Pyrgophysa Mariei, BOETTGER, 21: 41. 1894 Pyrgophysa Bavayi, DAUTZENBERG, 42: 103, pl. 3, fig. 7. 1950 Pyrgophysa Bavayi, FISCHER-PIETTE, 90: 161. 1957 Bulinus mariei, RANSON, 34: 21, fig. 5a. 1958 Bulinus mariei, BRYGOO, 26: 56. 1964 Pyrgophysa Mariei, CHEVALLIER, 104: 33. 1969 Bulinus (Pyrgophysa) mariei, STARMUHLNER, 8: 288-306; fig. 387, p 290; carte, p 306. Les types de P. Mariei et P. Bavayi sont tous deux au Muséum, le premier dans la collection de l'Atlas de Madagascar et le second dans la collection des types du Journal de Conchyliologie. Ranson a montré que В. mariei est une espéce uniquement malgache, distincte de В. forskalii Ehr. Les provenances connues, ou du moins celles que nous avons situées, se trouvent portées sur notre carte Fig. 17, qu'il s'agisse des données de la littérature, ou de celles que nos collections y ajoutent. Anisus (Anisus) crassilabrum Morelet 1860 Planorbis crassilabrum, MORELET, 2: 96, pl. 6, fig. 8. 1860 Planorbis trivialis, MORELET, p 97, pl. 6, fig. 7. 1863 Planorbis (Nautilina) caldwelli, TRISTRAM, р 61. 1876 Planorbis crassilabrum, MARTENS, 3: 253. 1878 Planorbis crassilabrum, KOBELT, 5: 180. MOLLUSQUES DE MADAGASCAR 365 1878 Planorbis trivialis, KOBELT, 5: 180. 1879 Planorbis trivialis, MORELET, 27: 311. 1879 Planorbis crassilabrum, MORELET, 27: 312. 1881 Planorbis crassilabrum, CROSSE, 29: 202. 1883 Planorbis hildebrandti, MARTENS, 10: 83. 1886 Planorbis crassilabrum, CLESSIN, ed. 2, 1(17): 150, pl. 22, fig. 6. 1886 Planorbis crassilabrum, CLESSIN, 1(17): 196, pl. 29, fig. 7. 1894 Planorbis alluaudi, DAUTZENBERG, 42: 101, pl. 4, fig. 2. 1894 Planorbis simpliculus, DAUTZENBERG, 42: 101, pl. 4, fig. 1. 1918 Planorbis (Planorbis) Hildebrandti, GERMAIN, p 46. 1918 Planorbis (Tropidiscus) trivialis, GERMAIN, p 48. 1918 Planorbis (Tropidiscus) simpliculus, GERMAIN, p 49. 1918 Planorbis (Tropidiscus) alluaudi, GERMAIN, p 50. 1918 Planorbis (Gyraulus?) crassilabrum, GERMAIN, p 50. 1921 Planorbis (Propidiscus) trivialis, GERMAIN, 10: 39, pl. 5, fig. 9-14. 1929 Planorbis (Planorbis) trivialis, HAAS, p 413, pl. 2, fig. 14, 15. 1935 Planorbis (Planorbis) trivialis, GERMAIN, (10), 18: 442. 1935 Planorbis (Gyraulus) crassilabrum, GERMAIN, (10) 18: 442, fig. 5-7. 1953 Planorbis trivialis, GRJEBINE & MENACHE, (A), 8: 87. 1953 Planorbis crassilabrum, GRJEBINE € MENACHE, 8: 87. 1957 Anisus crassilabrum, RANSON, 34: 6. 1958 Anisus crassilabrum, BRYGOO, 26: 66. 1969 Anisus (Anisus) crassilabrum, STARMUHLNER, 8: 307-328; fig. 420, 421, p 309. Distribution. Les cartes publiées par Brygoo et par Ranson sont déja trés fournies. Nous aurions encore tant d'autres localités à faire connaître, qu'il nous semble inutile de les énumérer. Qu'il nous suffise de dire que cette espéce se trouve en abondance dans toute l’île. Gyraulus (Caillaudia) apertus Martens 1897 Planorbis apertus, MARTENS, p 149, pl. 6, fig. 17. 1969 Gyraulus (Caillaudia) apertus, STARMUHLNER, 8: 328, fig. 452, 453; p 344, fig. 481. Espéce décrite du Lac Albert-Edouard qui était sa seule provenance connue, et que Starmühlner a citée récemment de Madagascar, en deux provenances du centre Sud, le ruisseau Andranomaria, et le ruisseau Amborompotsy (et un de ses affluents). Nous y ajoutons 14 autres provenances. L'une d elles est due à Waterlot Diego-Suarez (Baie des Amis). Toutes les autres sont dues au Dr. Brygoo. Ce sont, du Nord au Sud: Vohemar, Ambilobe, Bemapaza, Bandabe, Ambodiamontana, Mandritsara, Am- balabongo, Ambalatany, Bekodoka, Antsirasitra, Bevato, Miarina rivo et Ambano (voir notre carte Fig. 18). Nous avons comparé nos échantillons avec un lot du Lac Albert Edouard étudié par Germain (1912, Bull. Muséum, p 80). Segmentorbis (Segmentorbis) angustus Jickeli 1874 Segmentina angusta, JICKELI, р 220, pl. 7, fig. 24. 1904 Segmentina chevalieri, GERMAIN, p 468. 1918 Segmentina chevalieri, GERMAIN, p 51. 1935 Segmentina angusta, GERMAIN, (10), 18: 444. 1969 Segmentorbis angustus, STARMUHLNER, 8: 345. Distribution. Les cartes publiées par Brygoo et par Ranson sont déjà tres fournies. Nous aurions encore tant d'autres localités а faire connaítre, qu'il nous semble inutile de les énumérer. Qu il nous suffise de dire que cette espéce se trouve en abondance dans toute Vile. 366 FISCHER-PIETTE ET VUKADINOVIC Diego- Suarez Ambilobe — Ветараза Vohemar | FIG. 18. Distribution de Gyraulus apertus Martens. Ambalabongo | Ambodiamontana Ambalatany Bandabe — \ 4 Mandritsara | Bekodoka —Antsirasitra Miarinarivo Antsampandrano et Amborompotsy E / e—Andranomaria Espece décrite du Lac Albert-Edouard qui était sa seule provenance connue, et que Starmiihlner a citée récemment de Madagascar, en deux provenances du centre Sud, le ruisseau Andranomaria, et le ruisseau Amborompotsy (et un de ses affluents). Nous y ajoutons 14 autres provenances. L'une d'elles est due à Waterlot Diego-Suarez (Baie des Amis). Toutes les autres sont dues au Dr. Brygoo. Ce sont, du Nord au Sud: Vohemar, Ambilobe, Bemapaza, Bandabe, Ambodiamontana, Mandritsara, Ambalabongo, Am- balatany, Bekodoka, Antsirasitra, Bevato, Miarina rivo et Ambano (voir notre carte Fig. 18). Nous avons comparé nos échantillons avec un lot du Lac Albert Edouard étudié par Germain (1912, Bull. Muséum, p 80). Espece africaine а trés large répartition, dont on trouvera davantage de références dans Germain (1935) et dans Starmiihlner (1969). Pour Madagascar, les provenances connues sont Majunga (Germain, 1918) et lac Manampetsa (Germain, 1935). Nous y ajoutons 12 autres provenances. Du Nord au Sud: Ambanja (Waterlot); Antsohihy (Brygoo, 1957); Ambodiamontana (Brygoo, 1957); An- dohajango (Brygoo, 1957); Marovoay (Waterlot); Tampolo (J. Millot, 1949); Fenerive (J. Millot, 1949); Manambolo (Brygoo, 1957); Morondava (Perrier de la Bathie); Vondrove (Brygoo, 1957); Fiherana (Grandidier); Tuléar (G. Petit, 1925). Les diverses provenances sont portées sur notre carte Fig. 19. Ferrissia (Ferrissia) modesta Crosse 1880 Ancylus modestus, CROSSE, 28: 150. 1881 Ancylus modestus, CROSSE, 29: 203, pl. 8, fig. 6. 1882 Ancylus modestus, CLESSIN, ed. 2, 1(6): 73, pl. 9, fig. 10. 1889 Ancylus modestus, CROSSE & FISCHER, In: GRANDIDIER, pl. 24, fig. 6. 1964 Ancylus modestus, CHEVALLIER, 104: 33. 1969 Ferrissia (Ferrissia) modesta, STARMUHLNER, 8: 362, fig. 506. Nous avons le type dans la collection de |’Atlas de Madagascar. Cette espéce a été décrite de Nossi-Bé. Starmühlner Га citée en plus de Tananarive, de la riviére Lily а 100 km de Tananarive, des environs du lac Froid et pres de la voie ferrée d Antsirabe. — MOLLUSQUES DE MADAGASCAR 367 Nos collections y ajoutent: (J. Millot, 1946 et 1947): Marais du lac Alaotra, lac Tsim- bazaza, Ambositra. Les diverses provenances sont portées sur notre carte Fig. 19. Biomphalaria madagascariensis Smith 1882 Planorbis madagascariensis, SMITH, p 387, pl. 22, fig. 20-22. 1905 Planorbis madagascariensis, ANCEY, 53: 320. 1918 Planorbis madagascariensis, GERMAIN, p 45. Ambanja Antsohihy | Majunga Ambodiamontana Marovoay \ Ambohajango Г Tampolo Fenerive Manamloolo Lil = Tananarive Tone x Lac Tsimloazaza E Lac Froid Ligne d'Antsirabe | Morondava A Ambositra Vondrove_e Tulear e—Fiherena Lac а : p- Man mpetsa e Segmentorbis angustus Jick. NTercissia, Mmoeleska cross= FIG. 19. Distribution de Segmentorbis angustus Jickeli et de Ferrissia modesta Crosse. 368 FISCHER-PIETTE ET VUKADINOVIC 1953 Biomphalaria pfeifferi, GRJEBINE & MENACHE, 8: 87. 1957 Biomphalaria madagascariensis, RANSON, (34): 1, fig. 2, 3A. 1958 Biomphalaria madagascariensis, BRYGOO, 26: 49, carte, p 51. 1969 Biomphalaria madagascariensis, STARMUHLNER, 8: 345; fig. 482, p 349; fig. 505, p 361. Distribution. Les cartes publiées par Brygoo et par Ranson sont déja trés fournies. Nous aurions encore tant d'autres localités а faire connaitre qu il nous semble inutile de les énumérer. Qu'il nous suffise de dire que cette espéce se trouve en abondance dans toute Vile. Caelatura (Zairia) geayi Germain 1911 Unio (Nodularia) Geayi, GERMAIN, p 137, pl. 1, fig. 1, 2, 6, 7. 1918 Nodularia Geayi, GERMAIN, p 36. 1969 Caelatura geayi, HAAS, 88: 187. La localisation de cette espéce dans l’île est inconnue. Nous sommes tombés par hasard, dans des matériaux non-classés du Muséum, sur un lot de 4 Unionidae dépourvus de nom et dont l'étiquette portait seulement * Mission Geay 1911.” Cette indication prouvant que la provenance était Madagascar nous avons constaté, avec la plus grande facilité, que 3 des 4 specimens étaient ceux que Germain (1911) avait figurés sous les noms Unio (Nodularia) Geayi et Unio (?) malgachensis.? Tous les détails des taches etc. . . se reconnaissent. HAAS a affirmé que | Unio geayi n'était pas une Caelatura, sans proposer d’ailleurs une autre affectation. Il п’а pas expliqué les raisons de son affirmation. Nous ne comprenons pas ce qui Гу a conduit, et nous confirmons pleinement la position de Germain. Faisons connaître que l'échantillon non-figuré est une valve gauche de 42 mm sur 23. Caelatura (?) malgachensis Germain 1911 Unio (?) malgachensis, GERMAIN, р 139, pl. 1, fig. 3-5. La localisation de cette espéce dans l’île est inconnue. Comme nous venons de le dire (voir Caelatura (Zairia) geayi), | exemplaire sur lequel est basée la description de Germain est entre nos mains. De méme que Germain, nous ne voulons pas l'ouvrir pour ne pas le casser plus que ne le montre la figure 3, de sorte qu il n'est toujours pas possible de lui assigner une place dans la classification. Certes, Haas af- firme que c’est un jeune d’ Unio geayi. Nous devons faire remarquer que son sommet n'est séparé de l'extrémité antérieure que par un septième de la longueur totale de l’exemplaire, alors que chez Caelatura geayi il est au quart ou entre le quart et le tiers. Nous savons que le sommet peut s'éloigner de l'avant au cours de la vie, mais nous pen- sons qu'avant de prendre une décision il faudrait attendre d’avoir а sa disposition des in- dividus de tous âges. Unio madagascariensis Sganzin 1841 Unio madagascariensis, SGANZIN, 3: 8. 1918 Unio (?) madagascariensis, GERMAIN, p 37. 1969 Caelatura madagascariensis, HAAS, 88: 187. 2Germain ne prenait vraiment aucun soin des matériaux qu'il avait étudiés. ne leur mettant bein souvent pas d'étiquettes, ou encore les mélangeant ainsi que leurs étiquettes ou les dispersant dans bien des cas, non seule- ment n'importe où au Muséum, mais aussi bien dans son appartement de Paris, sa villa d'Angers ou le Musée d'Angers. Il en résulte que beaucoup de ses types passent maintenant inaperçus, et il se pourrait qu un certain nombre soit définitivement perdu. Le professeur Fischer-Piette tient à faire connaître clairement cette situation pour ne pas en être tenu responsable. MOLLUSQUES DE MADAGASCAR 369 Espece non-figurée et qu on пе peut guere dire avoir été décrite, le texte étant: Cette coquille, que je crois inédite, est de la grandeur de la mulette littorale; elle est vert et d'une contexture trés fragile; elle se trouve abondamment dans le Mahoupa, riviere pres de Tamatave, ile de Madagascar.” Il conviendrait de rechercher cette espéce dans la région d'où elle était signalée. Etheria elliptica Lamarck 1807 Etheria elliptica, LAMARCK, 10: 401, pl. 29; pl. 31, fig. 1. 1907 Aetheria elliptica, GERMAIN, p 225. 1945 Aetheria elliptica, FISCHER-PIETTE, p 41. La provenance indiquée en 1907 et les 2 provenances qui ont été ajoutées en 1945 sont portées sur notre carte Fig. 20. Jusqu ici il ne s agit donc que du Nord-Est et du Nord- Ouest. Betsieka e-Beandrarezona sahondra A-Mahavavy Fah arantSana-e, ropa Tananarive—e : e- Ambohitraimanitra if Onive—e Tsinjoarivo Antsirabe . — Manshiatra e— Fianarantsoa Mananara—e E 4 vanganidrano Itomam Befotaka=e PY Amboasary —e eCorbicula madagascariensis smith A Etheria elliptica Lr FIG. 20. Distribution de Etheria elliptica Lk. et de Corbicula madagascariensis Smith. 370 FISCHER-PIETTE ET VUKADINOVIC Corbicula madagascariensis Smith 1882 Corbicula madagascariensis, SMITH, p 388, pl. 22, fig. 25-27. 1918 Corbicula madagascariensis, GERMAIN, p 37. Cette espece n était connue jusqu ici que par le travail de Smith, qui a donné comme provenance “Twenty miles from Antananarivo.” Nous en avons un grand nombre d'échantillons de diverses provenances, qui vont nous permettre de faire connaître le degré de variabilité de l'espece. Voir la charniére de l'un d'eux, Fig. 21. Smith a donné les dimensions suivantes: longueur 14 mm; hauteur 11 mm; épaisseur 7 mm. Le plus grand de nos échantillons a: 19 mm; hauteur 16 mm; épaisseur 12 mm (récolté par Decary dans la riviere Itomampy). Les rapports des dimensions montrent quelque variabilité. Nous les donnons pour un certain nombre d'individus de tailles diverses dans le Tableau No. 1. TABLEAU 1. Dimensions de 20 individus de Corbicula madagascariensis Rapport Rapport Longueur Hauteur Epaisseur longueur épaisseur en mm en mm en mm sur hauteur sur largeur 19 16 12 152 0,60 18 14 8 1,3 0,45 17 15 Ih! 1,1 0,65 17 14 8 12 0,45 16 15 8,5 1,03 0,53 16 14 10 I 0,62 16 13 7,9 1.2 0,47 16 13 8 1,1 0,44 15 13 9,5 11 0,63 15 13 8 1,13 0,44 14 12 7,9 1413 0,53 14 11 6 1:25 0,43 14 10,5 5,5 1,4 0,40 13 10 6 1,3 0,46 12 10 6 1,3 0,46 11 9 5 1,2 0,45 10 8 5,5 1,25 0,55 10 8 5 1,3 0,50 9 7 4 1,3 0,44 8 6,5 4 1,2 0,50 FIG. 21. Corbicula madagascariensis Smith. MOLLUSQUES DE MADAGASCAR 371 On voit par ce tableau que le rapport de la longueur а la hauteur, varie de 1,1 а 1,4, et que le rapport de l'épaisseur а la longueur varie davantage de 0,49 à 0,65. Ce tableau ne montre pas d’evolution nette des rapports des dimensions avec l’äge des individus. Distribution. A la provenance qui était connue, Tananarive, nous ajoutons (voir carte Fig. 20): Beaudrarezona (Brygoo, 1957); rivière Кора à Faharantsana; riviere Кора pres de Tananarive; Ambohitraimanitra canal (Brygoo, 1957); Tsinjoarivo (J. Millot, 1949); Onive (J. Millot, 1949); Antsirabe (Waterlot); Manshiatra (Perrier de la Bathie); Fianarantsoa; Mananara (Decary, 1926 et Perrier de la Bathie); Vanganidrano (Decary); Itomampy (Decary, 1926); Befotaca (Brygoo, 1957); Amboasary (G. Petit, 1932). Corbicula sikorae Ancey 1890 Corbicula sikorae, ANCEY, 7: 347. 1918 Corbicula sikorae, GERMAIN, p 38. Cette espece n'est connue que par la description d’Ancey (du fleuve Mongoro) et n’a jamais été figurée. Germain a seulement dit qu'elle semble bien voisine de С. madagascariensis. C'est tout-d-fait notre opinion, et nous voulons faire ressortir la similitude des caracteres. Voici la description donnée par Ancey: “Concha pro genere tenuis, deplanata, subaequilatera, ovalis, nitida, lutea, epidermide ad nates praecipue decidua. Nates submediani, obtusati, vix prominentes. Pagina interna livide alba. Area an- tica ovalis, postica haud angulata nec truncata, subovalis. Basis regulariter lateque ar- cuata. Superficies sulcis concentricis ad marginem vix tenuiorbus sculpta. Diam. antero- post., 11%; alt. (e natibus ad basin), 8/2; crass., 5 п.” Ancey dit que son espece differe “tres notablement” de С. madagascariensis, mais il n'exprime pas des différences. Nous supposons qu elles consistent dans la taille, petite; dans le fait que les stries de croissance, dans la région ventrale, s atténuent à peine alors que Smith avait écrit: “The concentric striae are deep and regular upon the umbones; but towards the ventral margin they become less regular and finer.” Mais il se pourrait bien que la petitesse de la coquille d'Ancey soit due ä un Аве moin- dre, et il serait alors normal que l’affaiblissement des côtes, qui, faisons le remarquer, est exprimé dans les deux cas, ne fasse que commencer. Nous supposons aussi ач’еп disant ач’а l’arriere la coquille n était ni anguleuse ni tronquée, Ancey a voulu apposer ces caractères à “squarish and subtruncate posteriorly qu exprime et figure Smith. Mais, au sein d'un même lot, nous trouvons avec la plus grande facilité. aussi bien des contours réguliérement arrondis а | arriére que des aspects tronqués, et avec tous les intermédiaires. Nous sommes donc persuadés que C. sikorae est synonyme de C. madagascariensis. Mais n ayant pas vu d échantillons d'Ancey, nous n opérons pas la suppression de son es- ресе. Pisidium casertanum Poli 1791 Cardium casertanum, POLI, p 65, pl. 15, fig. 1. 1906 Pisidium planatum, ANCEY, 20(4): 46, No. 3. 1918 Pisidium planatum, GERMAIN, p 40. 1953 Райт edouardi, KUIPER, р 26, pl. 1; fig. 1, 2, p 27. 1966 Pisidium casertanum, KUIPER, pl. 10, fig. 1-3; pl. 11, fig. 1-5; pl. 12, fig. 1, 2; pl. 15, fig. 13. Kuiper (1966), a placé dans la synonymie de |’ espéce cosmopolite P. casertanum le P. edouardi qu'il avait décrit en 1953, et aussi le P. planatum. Ce dernier n est connu que par la description d'Ancey qui ne Га jamais figuré. Ancey le dit plus plat que P. madagascariensis Smith. Germain a fait remarquer qu il n'y a jamais eu de P. madagascariensis Smith. Nous supposons qu Ancey voulait parler, en fait, de P. johnsoni, qui d’apres les dimensions données est en effet plus gonflé. 372 FISCHER-PIETTE ET VUKADINOVIC Nous avons au Muséum le type de P. edouardi, ses paratypes, les échantillons sub- fossiles d’Antsirabe cités par Kuiper (1966, р 50), ainsi qu une vingtaine d'exemplaires récoltés par Waterlot äTananarive. Voir la carte Fig. 22. Pisidium johnsoni Smith 1882 Pisidium johnsoni, SMITH, p 389, pl. 22, fig. 28-29. 1918 Pisidium johnsoni, GERMAIN, p 40. 1953 Pisidium pauliani, KUIPER, 93: 28, pl. 2, fig. 1-5. 1960 Pisidium pauliani, KUIPER, 89: 74; fig. 24-29. 1966 Pisidium johnsoni, KUIPER, p 54, pl. 14, fig. 1-6; pl. 15, fig. 16. Espece décrite des environs de Tananarive. Connue aussi de Betafo (centre de l’île, voir notre carte Fig. 22) par la description que Kuiper a faite de P. pauliani qu il a ensuite placée dans la synonymie de P. johnsoni. Le Muséum ne possede pas d'échantillons de cette espece. ePisidium casertanum poli APisidium reticulatum ruipr Nossi-Be_A Ankirihitra k Andriba_ , Ambatolaona Tananarive_, Perinet Betafo Antsirabe % Namokely 1 Antsampandrano /l FIG. 22. Distribution de Pisidium casertanum Poli et de Pisidium reticulatum Kuiper. Pisidium betafoense Kuiper 1953 Pisidium betafoense, KUIPER, 93: 30; pl. 3, fig. 1-5, p 31. 1966 Pisidium betafoense, KUIPER, р 55, pl. 15, fig. 17. Espece décrite sur un seul échantillon, de Betafo (Paulian, 1949). Betafo est au centre de l'île (voir carte Fig. 22). Pisidium (Parapisidium) reticulatum Kuiper 1966 Pisidium (Parapisidium) reticulatum, KUIPER, 95: 16, text-fig. 1-4. Espece décrite de Nossi-Bé et de Rhodésie. Nous en avons deux échantillons dont un jeune, récolté par Waterlot 4 Ankarihitra pres Maevatanana (Madagascar Nord-Ouest). Voir notre carte Fig. 22. MOLLUSQUES DE MADAGASCAR 373 Namoroka e——Tananarive Morondava Antsirabe FIG. 23. Distribution de Eupera ferruginea Krauss. Sphaerium madagascariense Tristram 1863 Cyclas (Sphaerium, Scop.) madagascariensis, TRISTRAM, p 61. 1878 Sphaerium Madagascariense, SOWERBY, In: REEVE, 20: pl. 3, fig. 22. 1882 Sphaerium madagascariense, SMITH, p 388. 1918 Sphaerium madagascariense, GERMAIN, p 39. Cette forme dont nous n'avons pas d'exemplaires sous les yeux, a été décrite de la région de Tananarive, et trouvée aussi а Betsileo (Smith). Germain en commentant ces données, émet la supposition qu ‘il n'y a avec Sphaerium capense Krauss, 1848, largement répandue en Afrique, qu une difference de provenance et qu une mise en synonymie devra se faire. Eupera ferruginea Krauss 1848 Cyclas ferruginea, KRAUSS, p 7, pl. 1, fig. 7. 1879 Limosina ferruginea, CLESSIN, ed. 2, 9(3): 247, pl. 46, fig. 1-4. 1882 Limosina ferruginea, SMITH, p 388. 1918 Sphaerium ferrugineum, GERMAIN, p 38. 1929 Eupera ferruginea, HAAS, 57: 429. 1954 Byssanodonta ferruginea, KUIPER, 94: 47; fig. 6-10, p 46. Cette espéce décrite d'Afrique du Sud a été signalée à Madagascar par Smith de Tananarive, par Haas de Majunga et par Kuiper de Morondava et Namoroko. Nous y ajoutons: Antsohihi (Dr. Gaud, 1951); Antsirabe (Perrier de la Bathie). Voir la carte Fig. 23. Eupera degorteri Kuiper 1954 Byssanodonta degorteri, KUIPER, 94: 42-47; fig. 1-5, р 43. Cette espéce a été décrite sur des matériaux du Muséum ayant les provenances suivantes: Cap St. André; riviere Kapiloza; riviere Maningoza; Sahondra; Andravodahy (dont le type); Morondava. Toutes ces provenances sont de l'Ouest. Nous у ajoutons une provenance du Nord: Diego-Suarez (Waterlot). Voir notre carte Fig. 24. 374 FISCHER-PIETTE ET VUKADINOVIC FIG. 24. Distribution de Eupera degorteri Kuiper. LITERATURE CITED ALDERSON, F., 1925, Studies in Ampullaria: xx + 102 p, 19 pl., W. Heffers & Sons Ltd., Cambridge. ANCEY, C. F., 1890, Mollusques nouveaux de l'archipel d' Hawai, de Madagascar et de l'Afrique équatoriale. Bull. Soc. Malacol. 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WENZ, W., 1938, Gastropoda, In: Handbuch der Paläozoologie, 6(1), Prosobranchia: xii + 948 p, Borntraeger, Berlin. 378 FISCHER-PIETTE ET VUKADINOVIC ABSTRACT ON THE FRESHWATER MOLLUSKS OF MADAGASCAR E. Fischer-Piette and D. Vukadinovic This work is a complement to that of Starmühlner which appeared in MALACOLOGIA in 1969. It completes his study by also mentioning lamellibranchs and by giving additional locations for many gastropods. AG ZUSAMMENFASSUNG ÜBER DIE SÜSSWASSERMOLLUSKEN MADAGASKARS E. Fischer-Piette und D. Vukadinovic Diese Arbeit ist eine Ergänzung zu der in 1969 in MALACOLOGIA erschienenen von Starmühlner. Sie vervollständigt seinen Bericht insbesondere dadurch, dass ausser Gastropoden auch Lamellibranchier erwähnt werden, und indem für die Gastropoden zusätzliche Fundorte angeführt sind. A.G. RESUMEN SOBRE LOS MOLUSCOS DE AGUA DULCE DE MADAGASCAR E. Fischer-Piette y D. Vukadinovic Este trabajo es complementario al de Starmühlner publicado en MALACOLOGIA en 1969. Completa su estudio mencionando tambien lamelibranquios y dando ubicaciones adicionales para muchos gaströpodos. JE. ABCTPAKT ) ПРЕСНОВОДНЫХ МОЛЛЮСКАХ МАДАГАСКАРА Е. ФИШЕР-ПЬЕТТ И Д. ВУКАДИНОВИЧ Эта работа служит дополнением к исследованию Штармюльнера, напечатанного ологии" в 1969 г. Она выполнена на тех же видах Bivalvia и в ней указываются дополнительные места нахождения многих Gastropoda. Z.A.F. MALACOLOGIA, 1973, 12(2): 379-399 SUBSTRATUM AS A FACTOR IN THE DISTRIBUTION OF PULMONATE SNAILS IN DOUGLAS LAKE, MICHIGAN!,? Philip T. Clampitt Cranbrook Institute of Science, Bloomfield Hills, Michigan 48013 USA ABSTRACT Study has been made of substratum as a factor in the distribution of 5 species of pulmonate snails in Douglas Lake, Cheboygan County, Michigan. Quantitative field sampling, together with laboratory experiments, revealed that adult Physa integra Haldeman prefer hard substrata such as stones; adult Helisoma antrosa percarinata (Walker), in contrast, prefer a substratum of sand. When food (algae or detritus) was pre- sent on both stones and sand in the laboratory, the average distribution of P. integra was 58% on the stones and 8% on the sand (a highly significant difference), while in separate equivalent experiments an average of 24% of the H. antrosa were on the stones and 39% on the sand (also significant). Physa parkeri “Currier” DeCamp, Stagnicola emarginata angulata (Sowerby) and Helisoma campanulata smithi (Baker) all exhibited more com- plex and varied patterns of distribution as to substratum in the field. In the laboratory, P. parkeri showed a preference for a stony substratum very similar to that of P. integra when food was present. The average distribution of H. campanulata was 29% on stones and also 29% on sand when food was present on both. Relationships in the 5 species between sub- stratum, on the one hand, and depth, wave action, food, oviposition sites, and respiratory needs, on the. other, are discussed. INTRODUCTION Substratum is a significant ecological factor in the distribution of freshwater snails. After a comparative study of 2 species of aquatic pulmonate snails in Iowa (Clampitt, 1970) and a review of the pertinent literature, I have concluded that this factor deserves more study than it has so far received. Hyman (1967), in her summary of the literature on habits and behavior in pulmonate snails, makes no special mention of substratum with reference to most freshwater forms; she states only that the freshwater limpets, family Ancylidae, inhabit rock surfaces in streams and lakes. Boycott (1936), while giving considerable information on the habitats of British freshwater mollusks, does not describe substratum types in most instances. Macan (1950) gives some information on substratum and vegetation in relation to the numbers of gastropod mollusks in Lake Windermere and other bodies of water in the English Lake District. Elsewhere, Macan (1963) comments more generally both on the importance of substratum to most freshwater animals, and on the lack of data on the sub- ject. A recent study of Harman (1972) confirms the importance of substratum in the dis- tribution of aquatic mollusks. In a lake well-populated with a variety of species of snails, some reside primarily on the bottom, others on vegetation, and still other species move freely from one to the other. In the study cited above (Clampitt, 1970), some populations of Physa integra Haldeman (Pulmonata: Physidae) were concentrated on stones close to shore, while others were 1 A contribution from the University of Michigan Biological Station and Cranbrook Institute of Science. 2 The work was supported by Cranbrook Institute of Science. (379) 380 Р. T. GLAMPITT contined largely to off-shore vegetation; the species appeared to avoid substrata of sand or mud. P. gyrina Say, an inhabitant of small ponds as well as shallow areas of lakes, was much less selective as to substratum, being found on living and dead vegetation, stones, mud and sand. The substratum on which a snail moves provides food and oviposition sites, and may afford protection against such physical and biological factors as wave action and preda- tion. For pulmonate snails dependent on atmospheric oxygen, the ‘substratum’ —whether it be stones, fallen logs, vegetation, or some other material—may provide a surface on which the snails can crawl upward to reach the air- water interface. It is reasonable to assume that different snail species will have different behavior patterns and ecological requirements, and can therefore be expected to show different patterns of distribution with respect to substratum. The study described here was undertaken to test this assumption. Douglas Lake, Cheboygan County, Michigan, (45°35’ N. lat., 84°40’ W. long.) was chosen as the site of the study. This lake has a rich molluscan fauna, including several pulmonate snail species which are widely distributed in the lake. Although a review of the considerable background in- formation available on the lake and on various of its molluscan inhabitants 15 beyond the scope of this paper, the following studies are pertinent: H. B. Baker (1912, 1914), Welch (1927), Eggleton (1931, 1935), Cheatum (1934), Cort (1936a,b), Moore (1939), Cort, et al., (1940, 1941), Moffett (1943), Wilson (1944), Young (1945), Neel (1948), Gan- non & Brubaker (1969), Gannon & Fee (1970), and Bazin & Saunders (1971). Five species of pulmonate snails were chosen to receive major emphasis in this study. These are Physa integra Haldeman? and Р. parkeri “Currier” DeCamp in the family Physidae; Stagnicola emarginata angulata (Sowerby) (=Lymnaea e. angulata Say), Lymnaeidae; and Helisoma antrosa percarinata (Walker) (=H. anceps percarinata (Menke)) and H. campanulata smithi (Baker), Planorbidae. These species are the most common of the larger pulmonate snails in Douglas Lake. The study consisted of 2 major parts: (1) distribution of each species in the field—related to substratum characteristics, depth, and distance from shore—as revealed by quantitative sampling at selected locations, and (2) sub- stratum “preference” as revealed by laboratory experiment. The work reported here is the first of a series of investigations on the ecology, life history and behavior of Douglas Lake pulmonate snails, being done at the University of Michigan Biological Station. QUANTITATIVE FIELD SAMPLING METHODS Quantitative sampling of snails was done directly by hand. А circular “sampling loop, constructed of heavy steel wire and enclosing a М m? area, was set on the substratum and the enclosed area was searched carefully for snails. A face mask and snorkel were used regularly to aid collecting; SCUBA gear was used at depths of 2 m or more. Adult snails of the 5 species studied could be seen and collected readily using this method, as could juveniles 5 mm or more in greatest shell dimension. The sampling was done along transects at carefully selected sites positive for snails, at locations in Douglas Lake in- dicated in Fig. 1. Quantitative sampling was confined for purposes of this study to 3 The Douglas Lake forms which I have designated as Physa integra were apparently mis-identified by Goodrich (1932) and Cheatum (1934) as P. зауй crassa Walker. 1 was able to collect a few living P. зауй crassa from Higgins Lake, Roscommon County, Michigan, the type locality, on July 2, 1970. Examination of characteristics of both shells and male genitalia clearly establishes that the Higgins Lake forms and those from Douglas Lake are different entities, belonging not only to different species but to different subgenera (for criteria, see Clam- pitt, 1970, p. 119-121). In contrast, the lowa P. integra studied earlier (Clampitt, 1970) and those of Douglas Lake are very similar forms which I believe to be conspecific. SUBSTRATUM AND FRESHWATER SNAILS 381 М. Fishtail Bay b с БОЕ, que Пе В М Grapevine d Parc ad a km Si. 0 0. РО Fishtail и Вау 0 ORS UM Biol. mi A ESfiatiion FIG. 1. Douglas Lake, Cheboygan County, Michigan: approximate location with respect to Great Lakes region of North America (inset) and of transects (a-d) used for quantitative field sampling of snail populations. the eastern part of the lake—i.e., the North and South Fishtail Bay areas. Furthermore, only fairly open parts of the lake, exposed at times tofairly heavy wave action and characterized by a substratum of cobbles, gravel, or sand, and with slight to moderate growth of vegetation, were in- cluded; data were not collected from the few more sheltered and pond-like portions of the lake with heavy vegetative growth and substrata of silt. Each transect chosen showed fairly con- sistent substratum characteristics at any given depth. These are described below under “Results.” The transects ran perpendicular to the lake shore, and extended usually from the shore to maximum depths (distances) positive for snails. A series of stations along each transect was sampled; the several stations reflected changes in substratum with in- creased depth and distance from shore. Sampling at each station was along a narrow strip totalling 10 sq. m, running parallel to shore. Each sample, in turn, contained snails from a 1 m? area. The data are presented graphically in this paper as the average number of snails per m2, of each of the dominant species, at each station along the transect. Data were recorded at each station not only on sub- stratum, but also on depth and distance from shore. Temperature data, and data on shell sizes—reflecting life history stages—were also collected, and are to be reported in a later paper. 382 РТ. CLAMPITE RESULTS the shallow water adjacent to shore, to Transect “a,” South Fishtail Bay: sand (with scattered stones and pebbles) The substratum along this transect (Fig. | overlain by a thin layer of flocculent 2c) changed from algae-covered cobblesin organic detritus. The detritus layer 25 a June 30 - July 9, 1969 Transect a. N = > п —| < Z п NO. b 25 Physa Stagnicola May 18 - 21, 1970 integra emarg. angul. N = 20 Ph SS (Q ysa Helisoma m м parkeri antr.. peras =. < Z п O 72 DEPTH, DISTANCE, | 3 - 4 12 19 24 M SUBSTRA= 13 TUM I \ \ 0 / 7 р \ \ с > DS E = ee 10 a FROM DISTANCE SHORE, FIG. 2. Quantitative sampling data from transect “a,” South Fishtail Bay. a € b, numbers of adult snails per m? in July 1969 and May 1970, respectively; average numbers shown in cross-hatched or shaded bars, range of numbers per m? by vertical lines. c, bottom profile and substratum characteristics. SUBSTRATUM AND FRESHWATER SNAILS 383 became gradually thicker with increased depth and distance from shore. Rooted vegetation along this transect was sparse to absent. Beginning at about 30 m from shore (depth 2 m when the data were collected), the slope of the bottom in- creased, so that at about 45 m from shore the water depth was 5 m. At the times of sampling most of the snails were confined to water little more than 1 т deep, and the data in Fig. 2 are limited to these areas. Snail density data are shown in Fig. 2 for June 30-July 9, 1969, and May 18-21, 1970. In 1969 (Fig. 2a) there was a rather definite zonation for 2 species: Physa in- tegra were found in greatest numbers on the cobbles adjacent to shore, averaging 5/т? here. Helisoma antrosa were decidedly most abundant in the detritus- covered sand, in water 0.9 m deep, 12 m from shore; they averaged up to 18/m? in this area. Again in May, 1970 (Fig. 2b), P. integra showed much the highest den- sity—averaging 20/m2—in the cobble area adjacent to shore. Sampling done later in 1970 revealed heavy mortality of P. integra adults during June and July; by mid-July the adults had been almost entirely replaced by tiny juvenile snails. The other 3 species were fewer in number and showed less clear zonation. Stagnicola emarginata, for example, ex- hibited a more scattered distribution pattern through both cobble and sand sub- stratum areas in July 1969 (Fig. 2a); in 1970, this species was quite rare, not only along this transect but elsewhere in the lake. Both Physa parkeri and Helisoma campanulata (the latter not shown in Fig. 2) were low in numbers and rather scattered in distribution along transect “a” during both seasons. Transect “b,” North Fishtail Bay: The substratum adjacent to shore at transect “b” (Fig. 3c) was sand, with a limited amount of detritus and growth of algae. At about 10 m from shore, at a depth of 0.9 m, was a sharp drop-off. Below the drop-off were gradually т- creasing amounts of detritus upon the sand; a dense growth of rooted vegetation (Potamogeton, Myriophyllum, Vallisneria, etc.) at 2-3 m; a gentler slope at a depth of 5-6 m, on which was deposited a very fine, dark-colored layer of detritus; coarser detritus at 7 m; and increasing amounts of silty detritus at 9 m depth and slightly below, where the bottom again leveled off. Snail density data are shown in Fig. 3 (a & b) for July 12, 1969, and July 22-24, 1970. As at transect “a, the snail density and distribution data differed greatly in the 2 years. In July 1969, numbers of Helisoma antrosa averaged 12 or more per m? in water 0.1 m deep, within 1 m of shore; their numbers dropped off sharply to 0 in water 0.9 m deep, 10 m from shore. The few Physa integra which were present were also in very shallow water. In 1970, few snails of any species were found above the drop-off area. The numbers of Н. cam- panulata on the fine silty substratum at 5.5 m depth—average 5/m?—was something of a surprise; this species elsewhere seem- ed to be most prevalent (e.g., see Fig. 5) on sand in water less than 1.0 m deep. Transect “c,” North Fishtail Bay: Characteristics of the substratum along transect “с” аге summarized, together with bottom profiles, in Fig. 4. A broad shoal, mostly of sand but containing varia- tions which could make considerable dif- ference in the lives of snails populating the area, extended from shore outward to a distance of about 150 m. At the edge of the shoal, at about 2 m deep, was a steep drop- off extending to a depth of more than 10 m. Snail density data from July 1969 are shown in Fig. 5. Helisoma antrosa pop- ulations averaging 7-9 snails/m? were pre- sent on a substratum of soft sand overlain by an algae-covered “crust” of con- solidated sand grains (Fig. 4) at a depth of 0.9-1.1 m, 65-100 m from shore. Densities of this species were much lower at other stations with different substratum condi- tions. H. campanulata were present in greatest numbers, averaging 2-3/m?, on fine sand 0.7 m deep and 40 m from shore; the presence of ripple marks indicated that the bottom was disturbed by periodic wave 384 action here. Physa integra and Sıugnicola emarginata were more scattered in their aistribution. On July 30, 1969, juvenile P. parkeri (not shown in Fig. 5) were found in fair numbers—up to 5 or 6/m2—all along the transect between 6 and 160 m from shore, at depths ranging from 0.5 to 5.0 m. а Transect b. HT. CLAMEPEITT Juvenile and some adult H. antrosa were similarly widely distributed, but with highest densities—10 or more/m? —between 1.0 and 2.0 m depth. A few adult H. campanulata were found below the drop-off at 2, 6 and 9 m depth, and some juveniles were collected at 2 and 3 т Physa integra 15 Helisoma = m July iZ 1969 = ants) spiere : = Helisoma I 5 IM) campanulata < Z n 0 b o 25 0 DEPTH, M DISTANCE, 4 8 Il 12 14 22 30 M SUBSTRA- =] Tun AY С 0 2 = Y dE = a us 6 = 8 10 20 30 № DISTANCE FROM SHORE, М FIG. 3. Transect “b” quantitative data, North Fishtail Bay. a € b, numbers (average and range) of adult snails per m? in July 1969 and July 1970, respectively. c, bottom profile and substratum characteristics. SUBSTRATUM AND FRESHWATER SNAILS 385 DISTANCE FROM SHORE, METERS 0 20 40 60 80 100 120 140 160 180 à \ AE — АЕ = + — 1 / / soft sand,,” 4 и а | дае -соуеге 4 3 fine sand, crust, patches ripple marks, of rooted plants u slight surface œ 4 wu crust EE uy = 18 ЕЕ = 6 a us a Transect c. soft sand, Е flocculent _- 7 organic 3 debris sand,” 7 debris / / fairly clean some organic sand, organic increasing debris, „I rooted plants 24 . Y still more debris h sand, organic Y sand, silty, grayish- flocculent debris Zi green, organic very silty sand 2 FIG. 4. Transect “c”, North Fishtail Bay area—bottom profile and substratum characteristics. depth, on the same date. During the spring and summer of 1970 transect “с” was again sampled. The numbers of most species in this area were greatly reduced from those of 1969. However, on July 22, 1970, the numbers of Helisoma antrosa averaged 2-3 / пл? at 7 т depth and about 1/m? at both 5 and 9 m depth below the drop-off. On August 14, 1970, Physa integra juveniles were found in numbers averaging 7/m? at 0.5 m depth, 50 m from shore, on soft sand, at that time covered with an algae crust; these numbers decreased gradually both closer to and farther from the shore where substratum changes also occurred. Transect “d,” Big Shoal: The “Big Shoal” extends from the east shore of Douglas Lake westward across the mouth of South Fishtail Bay nearly to Grapevine Point (Fig. 1). The substratum was mostly sand, with variations from shore outward (Fig. 6b) which could affect the snail populations inhabiting the area. At 0.45 m depth (at the time of sampling), 15 m from shore, the substratum was clean sand with distinct ripple marks, indicating frequent disturbance by wave action. The ripple marks faded out and a sparse mix- ture of Chara and a small Potamogeton sp. appeared between 30 and 50 m from shore at a depth of 0.5-0.55 m. The sand became very soft under foot at 60 m from shore, 0.65 m deep, then much firmer again at 90 m out, 0.8 m deep. At about 130 m from shore, where the water depth was 1.2 m, the substratum was fine sand with a slight ‘crust’ forming on the surface, and a very small amount of loose organic detritus. The slope of the bottom increased tem- porarily from a depth of 1.2 m at 132 m to 1.5 m at 147 m from shore. Along with this more rapid change in depth were changes in the amounts of loose organic detritus, dead clam shells and stones, all of which increased in quantity. Snail densities at transect “d” on July 9- 11, 1970, are shown in Fig. 6a. Most notable were the high densities—reaching more than 50/m? at 1.4 depth—of Helisoma antrosa in a relatively narrow 386 Р. T. CLAMPITT a 15 Physa integra 3 Stagnicola emarg. angul. N >= 10 Helisoma > anfr-perc. п — < Не! 15 ота zZ campanulata un © 5 Z FROM Transect c. July 12 - 16, 1969 65 100 150 SIHIORE, LS METERS Ss FIG. 5. Transect “c” quantitative data, North Fishtail Bay area. a, numbers (average and range) of adult snails per m? in July 1969. b, bottom profile and substratum characteristics (see also Fig. 4). zone, 132 to 147 m from shore at depths of 1.2-1.5 m. As indicated above, the sand was covered with increasing amounts of loose organic detritus, dead clam shells and stones as depth increased from 1.0 to 1.6 m. Also, in what was otherwise a flat shoal area, the zone of greatest abundance of snails of this species was in the area which sloped downward relatively rapidly. In contrast, H. campanulata was dis- tributed rather evenly and much more sparsely along transect “4.” The соп- trasting distributions of these 2 congeneric species suggests that they may differ con- siderably in their behavior and ecological requirements. LABORATORY EXPERIMENTS METHODS The procedures described here were designed to test experimentally the behavior of the snail species on which quantitative field data had been obtained, as this behavior pertained to the character of the substratum and to potential sources of food associated with different sub- stratum types. The basic experimental chamber was an oval-shaped plastic container, 50 x 30 cm; the bottom of one half was covered with a layer of stones and the other with a layer of sand 2 cm deep (Fig. 7). Space was left in SUBSTRATUM AND FRESHWATER SNAILS 387 the center of the chamber for insertion of a dish 8 cm in diameter; this would contain the snails released at the beginning of an experiment. The chamber was filled to a total depth of 10 cm with lake water. Water temperatures averaged 21.3°C (range, 19°-24°C). Overhead fluorescent lights provided continuous, uniform il- lumination of moderate intensity (averag- a 60 Transect d. 50 S Helisoma = = antr. erc. ~ 40 Р п > Helisoma O campanulata Zz п о 20 7 10 0 DEPTH»; 0.45 0105. 058 Ir M er 15 60 90 120 en 2 50 DISTANCE оу 9 = Pl FROM ing 100 footcandles) in the experimental chamber. At the beginning of each experiment, a dish containing water and 20-50 snails of a single species—the number depending on the size of the species—was placed in the center of the chamber. After Y hour, locations of all snails—whether on stones, sand, or elsewhere—were recorded at 15- 1970 100 150 SHORE, М FIG. 6. Transect “d’ quantitative data, Big Shoal. a, numbers (average and range) of adult snails per m2. b, bottom profile and substratum characteristics. 388 Pt. CLAMPITT Rete STONES SAND K 50 cm А FIG. 7. Experimental chamber for substratum preference experiments. minute intervals for a 14-hour period, after which the experiment was ter- minated. From these data on locations of snails at different time intervals, computations were made of the average numbers of snails located on stones and on sand during the course of an experiment. Enough replicate experiments were done on each species so that experimental data from at least 200 snails of that species—yielding some 1200 position recordings in all—were obtained in a particular set of experiments. Individual snails were used only once in a set of experiments. To test the response of the snails to sub- strata including as well as excluding a potential source of food (similar to that available in the lake), 4 sets of experiments were done on each species, as described above, with the following variations: (1) washed stones vs. washed sand (no food on either); (2) algae-covered stones vs. sand (food on stones only); (3) washed stones vs. sand with an algal crust or layer of organic detritus (food on sand only); (4) algae-covered stones vs. sand with algal crust or organic detritus (food on both stones and sand). The washed stones were obtained initially from dry land above the lake; other sub- washed stratum materials—with and without food—were collected from the lake itself, in areas where 1 or more of the species un- der study also lived successfully. RESULTS The data from these experiments are presented in Fig. 8 as follows: in “a,” the snails were given a “choice” between washed stones and washed sand; in “b,” between algae-covered stones and washed sand; in “c, between washed stones and sand with an algal crust or layer of organic detritus; and in “d,” between algae- covered stones and sand with an algal crust or layer of organic detritus. Fig. 8a reveals, in Physa integra, a decidedly more positive orientation toward the stones than toward the sand when food was absent from both—21% compared with 8%, on the average. Helisoma antrosa percarinata, in contrast, showed an average distribution of 28% on the sand and 15% on the stones. The dif- erences within both species were signifi- cant; for P. integra, p<.01 and for H. an- trosa, p<.05.* It will be noted that well over 50% of the snails of all 5 species were neither on the stones nor on the sand in this experimental situation. Some of these snails—here and in other sets of ех- periments—moved along the sides of the experimental chamber, some crawled on the water surface film, some crawled on the backs of other snails, and some remain- ed in or returned to the central dish from which they had been “released.” Fig. 8b reveals rather clearly the tendency of most of the species to concen- trate most heavily on stones when food was present there but lacking from the sand. This tendency was most pronounced in the 2 Physa species; the average distribution of P, integra was 56% on stones and only 2% on sand, and in P. parkeri, 61% on stones and 5% on the sand. In both species, the differences were highly significant; p<.001. In contrast, an average of 32% of the Helisoma antrosa were on the algae- covered stones as compared with 25% on 4 Tests of significance were done using the t distribution. SUBSTRATUM AND FRESHWATER SNAILS the washed sand. This difference was of doubtful significance; .4>p>.3. When food was present on the sand, but not on the stones (Fig. 8c), only Physa in- tegra continued to show a“ preference’ for the stones, averaging 27% as compared with 17% on sand; this preference was of 389 responding figures for P. parkeri were 18% and 24% (of borderline significance, .2>p>.1). Those for Helisoma antrosa were 16% on stones and 42% on sand, and for H. campanulata, 15% and 39%, respec- tively. Both of these latter were signifi- cant; p<.005 for H. antrosa and p<.001 doubtful significance; .3>p>.25. The cor- for H. campanulata. (No data were STONES SAND Year oft total аи» 80 60 40 20 0 20 40 60 80 ol T | И pied iid) CRC Pee: AG HTT + wn О ея. ES food food Het ars pos Ss Н. с. A Pls i NE Pos COR СС СС es Ев АА 23 food H. a. p. food К ES Н. с. ES Pha Für, HER PAGE no HI food C H. a. p. food A He EAU eee UE d Bi tp); UC food H. p. food К Е. SMC let total population 80 60 80 20 FIG. 8. Substratum preference, as revealed by laboratory experiment, in 5 species of snails (in- dicated by initials: P. i. = Physa integra, etc.). Data are given as percentages of the total population situated on stones (to left of heavy vertical line) and on sand (to right of this same line); horizontal bars represent mean distribution, and horizontal lines—extending into and from the bars—the range of distribution within a set of experiments. No population totals 100% because some snails, at any one time, were neither on stones nor on sand, but were located elsewhere in the experimental chamber (see text). Each bar represents the collective distribution of 200 snails over a 12-hour period, involving some 1200 position recordings. Numbers of snails used in a single experimental replicate were: Physa integra, 50; P. parkeri, 20; Stagnicola emarginata, 25; Helisoma antrosa, 40; Н. campanulata, 40. Four sets of experiments (a through d) were done, using stones and sand with or without food in 4 combinations. 390 P. T. CLAMPITT STONES SAND a EE | | = | т | | 1 T T T a] PHYSA INTEGRA no food food KKK Boe i ATT по food food ЕО HELISOMA ANTR. РЕКЕ. по food food КК по food tl: food KE a E A eS he GR à LR |! sa WLW LON mye к] по 80 60 40 20 % of total population FIG. 9. Substratum preference, in the laboratory, of the 2 most common and abundant of the larger pulmonate snails of Douglas Lake, Physa integra and Helisoma antrosa percarinata (the same data, differently grouped, as given for these 2 species in Fig. 8). collected for 5. emarginata in this or the following set of experiments because living specimens were unavailable. ) The most meaningful comparisons among species are provided in Fig. 8d, where food was present both on the stones and on the sand. This probably best reflects the usual situation in nature where both substratum types are available. Both Physa species exhibited a clear preference for the algae-covered stones even when food was also present on the sand; for P. integra, the averages were 58% of the snails on stones, 8% on sand; in P. parkeri, 55% and 12%, respectively. Both “ preferences’ were highly significant; p<.001. Under these same conditions equal numbers of Helisoma campanulata gathered on stones and on sand—29% on each. On the other hand, 39% of H. antrosa gathered on the sand, as compared with 24% on the stones. This difference was significant; p<.02. Results of the substratum “preference” experiments on Physa integra and Helisoma antrosa are presented separately as Fig. 9, which shows the contrasting behavior of these 2 species over substrata of stones and sand. In all 4 sets of experiments P. integra showed а “pref- erence for stones over sand, especially in experiments where food was present in the stones. Helisoma antrosa showed “‘pref- erence for the stones over the sand (32% to 25%) only when food was present on the stones and absent from the sand, and even this behavior was subject to considerable variation (and is of doubtful significance; .4>p>.3). The apparent preference by P integra for stones and of H. antrosa for sand was consistent with the patterns of distribution of these species in the field (Figs. 2-6). The other 3 species studied all SUBSTRATUM AND FRESHWATER SNAILS 391 appeared to have somewhat more varied patterns of distribution in the field rela- tive to substratum, and their behavior in these laboratory experiments (Fig. 8) was similarly variable. DISCUSSION The data presented in this study show that Douglas Lake populations of Physa integra and Helisoma antrosa percarinata present contrasting distributions as to sub- stratum; adult P. integra prefer stones, while sand is preferred by H. antrosa. Laboratory experimental data confirm these findings. These 2 species are “specialists, to a greater degree than are the other 3 species studied, in utilizing 2 types of substratum—stones and sand, respectively,—both of which are amply available in Douglas Lake. Not surprising- ly, therefore, these 2 species are the most common and abundant of the larger pulmonate snails in the lake. Physa parkeri, Stagnicola emarginata angulata, and Helisoma campanulata are also widespread in their distribution in Douglas Lake, but their numbers are fewer, and they are less clearly identifiable with particular substratum types. P. parkeri was widely dispersed over both stones and sand in the field; in the laboratory, however, it revealed a strong preference (closely paralleling that of P. integra) for stones when food was present there. From field and laboratory data taken together, I conclude that all 3 of the above species are more “generalists” in their behavior with regard to substratum. Broad sandy shoal areas, frequently inter- spersed with stones and other hard sur- faces, again provide very suitable habitats for these 3 species at widespread locations in Douglas Lake. It is beyond the scope of this paper to review the literature as it relates to the various habitats and substratum types oc- cupied in other bodies of water by the species studied here. A few examples will suffice to illustrate the difficulty of generalizing on the subject. Physa integra, for example, has been reported from a variety of types of habitats—creeks, rivers, brooks, and lakes—on boulders, gravel, sand, clay, mud and on vegetation (F. C. Baker, 1928; Goodrich, 1932; Goodrich & van der Schalie, 1939, 1944; Dawley, 1947; Clampitt, 1970). P. parkeri has been reported only from Michigan and only from a few lakes, inhabiting both sheltered bays and open or exposed areas (Baker, 1928; Goodrich, 1932; Cheatum, 1934). Stagnicola emarginata has been found (in Lake Huron at Mackinac Island) “in numbers on stones, weedy boards, and wharf supports close to the surface” (Goodrich, 1932). Stagnicola emarginata angulata, according to Cheatum (1934), is “ordinarily found in exposed littoral regions, clinging tightly to rocks, or buried in the sand or mucky bottom.” Helisoma antrosa, according to F. C. Baker (1928), is “primarily a river and creek species, not living in the large lakes’; Dawley (1947), however, reports that it is very common in both lakes and rivers in all parts of Minnesota, and Goodrich (1932) reports similar habitats for the species all over Michigan. Goodrich € van der Schalie (1939) report that this species occurs in brooks, creeks, rivers, lakes and ponds in Michigan's Upper Peninsula. Goodrich (1932) adds: “It may be found clinging to sticks and stones. In the Great Lakes, it has exploited a feeding ground of diatoms and algae on concrete piers and pine spiles. It can endure the heavy pressure of water in swift rapids.” Baker (1928) describes H. antrosa percarinata as “a form of large, deep lakes or bays of larger lakes. On the shore of Sturgeon Bay [Wisconsin] it oc- curs in deep water on rocks near shore.” Of the same form, Cheatum (1934) states that it “occurs widely in lakes,’ and is “found in sheltered vegetation zones and in exposed littoral regions. ” Baker (1928) describes typical H. campanulata in Wisconsin as a species of lakes, with habitat situations including rock bottom, sand bottom with vegetation, submerged logs, and mud bottom in a marshy area, in water varying from .3 to 1 m deep. Goodrich & van der Schalie (1944) state that this species is “apparently intolerant of domestic sewage and in course of dis- 392 P. T. CLAMPITT appearance in Indiana. Cheatum (1934) says of H. campanulata smithi that it is “commonly found in exposed areas of Douglas Lake; frequently in sheltered situations. | From the above, it can be concluded that there is considerable adaptive plastici- ty in most of these species which, as emphasized by Hunter (1961, 1964), is characteristic of freshwater snails general- ly. Therefore, what applies for a particular species in one aquatic situation may not necessarily apply for the same species in other situations. Conclusions from this study pertain specifically to Douglas Lake, and are likely to be generalizable only in part to other bodies of water. Some anatomical and behavioral peculiarities—as these pertain both to sub- stratum and depth distribution—of certain of the Douglas Lake species should be noted. The shells of Helisoma cam- panulata smithi in Douglas Lake are characterized by a “sculpture of coarse riblets”” (Е. С. Baker, 1928). As a result of this structural reinforcement, the shell of adult specimens is extremely durable; this is evidenced by the large proportion of dead shells of this species which remain unbroken when washed ashore, in con- trast with the broken fragments of shells left behind by most other species. Fair numbers of living H. campanulata (e.g., at transects “с” and “d,” Figs. 5 & 6) were often found in very shallow water on a sand substratum; when wave action was heavy, the living animals often could be seen to be buffeted about by the waves, without any apparent ill effects. In con- trast, the shells of H. antrosa percarinata are rather fragile and easily broken, es- pecially during periods of rapid growth of the animals. The densest, and apparently healthiest, populations of this species were in areas protected in 1 of 2 ways: either (1) wave action was usually slight (as at transect “b,” Fig. 3), or (2) in the more ex- posed areas (such as the Big Shoal, transect “d,” which was often disturbed by heavy wave action generated by the prevailing westerly winds), the snails were in water 1 m or more deep where the substratum suf- fered little disturbance even on the win- diest days. Another contrast between the 2 Helisoma species concerns their behavior. Helisoma antrosa frequently exhibited a tendency to burrow into the sand, demonstrated both in the laboratory and in the field. Burrowing at times of es- pecially heavy wave action could confer survival value on this species by pre- venting the snails from being tossed about by the waves and thereby damaged. None of the other snails studied showed any pro- nounced tendency to burrow. Adult Physa parkeri appeared to survive successfully in shallow water zones which were at least occasionally subject to fairly heavy wave action, even though their shells are rather thin and fragile for such a large snail. At transect “а” in South Fishtail Bay, fair numbers of adult P. parkeri were present on the stones near shore and in adjacent sandy areas in late spring and early summer, where they laid large numbers of eggs. Few young of this species appeared to develop in these areas, however, in contrast to P. integra. The shells of young P. parkeri are extremely thin and fragile and are probably unable to withstand the frequently heavy wave ac- tion on this and similar shores. On the other hand, many individuals of this species were seen to develop very rapidly in off-shore sandy areas where the water was deep enough so that the effects of wave action were slight. Such populations of juveniles were found at transect “c” during the summer of 1969 (water depth 1 m or more), and at transect “d” on the Big Shoat (water depth about 1.5 m), both in 1970 and 1971. In contrast, juvenile pop- ulations of the much smaller, slower- growing and less fragile P. integra seemed to thrive best on the rocks adjacent to shore (e.g., at transect “a” in South Fishtail Bay), even though exposed fre- quently to moderately heavy wave action. Brief consideration should be given to the relationship between substratum and food in the Douglas Lake snails. The clas- sification by Fox (1960) of marine detritus feeders into “filterers,” “scrapers” and “shovelers” is pertinent. Physa integra, as SUBSTRATUM AND FRESHWATER SNAILS 393 an inhabitant of stones and other hard sur- faces, could be expected to feed primarily by scraping edible materials—algae and associated SAufwuchisi and detritus— from these surfaces. Helisoma antrosa, on the other hand, with its preference for a sandy substratum, might be more adapted to “shoveling” in the loose detritus—with its contained nutrients— which is more characteristic of its habitat. However, laboratory observa- tions suggest that both species are capable of both “scraping” and “shoveling. Furthermore, examinations of the crop and stomach of 20 or 30 snails of each of the 5 species, collected from various locations, fail to give a clear picture of selective feeding in any of the species.? It is not clear whether the slight anatomical differences in the jaw and radula of these and other freshwater pulmonate snails (F. C. Baker, 1928) are significant in feeding. Also it remains unclear whether the type of substratum is of greater importance nutritionally or for reasons relating to other aspects of the ecology of the various species. The problem of the relationship between substratum and food merits further study. As for the role of the substratum in pro- viding oviposition sites, some kind of solid surface is required by all 5 species for the deposition of eggs. In both Physa species and in Stagnicola, stones, sticks, dead leaves, clam shells, and the shells of other living snails were all found to be accept- able sites. Somewhat surprisingly, an addi- tional acceptable site was the “crust” of consolidated sand grains, overlain by alee) growth, which appeared at transect (Fig. 4) at about 1 m depth during ve summer of 1969, and which has been observed during the summer months in ex- tensive zones on the Big Shoal and else- where. The 2 Helisoma species utilize sites similar to those used by the other species, except that stones with rough surfaces seem to be unacceptable. On the other hand, both Helisoma species were es- pecially prone to deposit their eggs on the shells of other living snails, of their own or other species. In sandy areas with few other sites appropriate for oviposition—a type of habitat where both the Helisoma species were frequently found—this behavior could have adaptive value for the species, providing a stable surface on which the embryonic snails can develop successfully to the hatching stage. Distribution both as to substratum and depth has a bearing on the supposed respiratory requirements of aquatic pulmonate snails. Hyman (1967, p 625) repeats the widely held view that freshwater pulmonates ‘‘or- dinarily .. . require access to air and die if kept submersed.” If this were true generally of lake pulmonates, they could probably live only in areas where stones, emergent plants, or other stable surfaces were available on which they could crawl upward periodically to reach the water sur- face for breathing air. None of the 5 species of this study was so restricted in its distribution. I therefore conclude that the supposed need for atmospheric oxygen is greatly exaggerated. There is good evidence that many lake pulmonates are well-adapted for remaining submerged, and that the mantle cavities of these snails may often be filled with water, rather than air, throughout their life cycles (Cheatum, 1934; Hunter, 1953, 1964; Clampitt, 1970). I found that Douglas Lake pop- ulations of adult Helisoma antrosa and H. campanulata, living in water either 0.5 or 5.5 m deep, had the mantle cavities filled with water. The same was true of adult Physa integra living on vegetation at 3 m depth in an Iowa lake (Clampitt, 1970). It is undoubtedly true also of many Douglas Lake populations of P. integra, P. parkeri, and Stagnicola emarginata, although further study is required to confirm this. This is not to say that pulmonate snails from lakes will not come to the surface and 5 The stomach contents of each species included sand grains (1% to more than 90%), algae (including diatoms, blue-greens, various unicellular and colonial green algae), moss leaflets, pine pollen, animal material (rotifers, parts of small crustaceans and insects, oligochaete annelids, etc.) and organic detritus. 394 Р. T. СБАМРИТ take on atmospheric oxygen when placed in the shallow water and restricted space of a laboratory aquarium, or in the field when they occur on stones which protrude out of water adjacent to shore, as at transect “a” along the shore of South Fishtail Bay. Few situations in lakes, however, provide such convenient access to the water surface. There is little evidence that lake-dwelling populations of pulmonates (except those living in very shallow water adjacent to shore or on emergent vegetation) make periodic trips to the surface for breathing air. As long as the dissolved oxygen supply is adequate, the snails can apparently ob- tain adequate oxygen for their respiratory needs by direct diffusion through the in- tegument. In planorbid snails, such as the Helisoma species, the development of a pseudobranch aids the process of aquatic breathing (Е. С. Baker, 1945; Hunter, 1957). Large annual variations in densities of certain species, notably Helisoma antrosa and Stagnicola emarginata, are evident from the study. Helisoma antrosa showed a dramatic decline in numbers at transects “a, “b” and “ce between 1969 and 1970; unpublished data from the spring and summer of 1971 reveal a partial reversal of this trend at transect “a.” At transect “d” on the Big Shoal, the very high densities of Н. antrosa (up to 50 per m?) in a well- defined zone in 1970 (Fig. 6) were not maintained in that zone in 1971, although numbers of this species apparently did in- crease greatly during 1971 in areas 230 to 300 m from shore at the same transect (un- published data). The drop in population density of H. antrosa along transect “d” between 1970 and 1971 was accompanied by increases in densities particularly of Physa parkeri, but also of P. integra and H. campanulata, in the same area. Stagnicola emarginata was a common species at transects ‘а’ and “с” in 1969, with den- sities of from 1-5 snails/m? not being un- common. In 1970, this species could be characterized as very rare not only in these areas but apparently throughout the lake. During the 1971 season, numbers of S. emarginata were again on the increase. The causes of these fluctuations in popula- tion density are not clear. The fact that in H. antrosa they were local in extent, in- volving only limited areas in the lake at any | time, while in S. emarginata they ex- tended throughout the lake, suggests different causes for the fluctuations in these 2 species. A 10-year study by Hunter (1961) of annual variations in growth and density of natural populations of fresh- water snails in Scotland indicates that short-term fluctuations in density are not uncommon even in stable populations, and also that such variations are useful as an in- dex of benthic productivity. Hunter at- tributed the fluctuations in 3 pulmonate snail species to the severity of winter con- ditions. In Douglas Lake, changes in lake level (relating to precipitation) and the oc- casional occurrence of severe storms which could so disturb the substratum as to cause considerable mortality among certain snail species, are among the climatic factors which must be considered. Biological fac- tors, including life histories of the various species (on which studies are now in progress), possible seasonal movements (also being studied), predation, parasitism, and intra- and interspecific competition must also be considered. There is evidence that long-range changes in the molluscan fauna of Douglas Lake have occurred, although earlier quantitative data are largely lacking. H. B. Baker (1914) reported on the mollusks of lake pools and in Douglas Lake itself, giv- ing descriptive terms such as ‘abundant, ” “common, “frequent” and “rare to in- dicate relative densities. The species of the present study were apparently among the more common and abundant species of Baker s studies in similar habitats. A proso- branch snail, Goniobasis livescens, former- ly absent from Douglas Lake but native to nearby lakes (Baker, 1912), was sub- sequently introduced and is now abundant and ubiquitous; this species, through in- terspecific competition, could have had a depressing effect on the numbers of some pulmonate species. Moffett (1943) made a quantitative study of the bottom fauna of the Big Shoal, which included data on SUBSTRATUM AND FRESHWATER SNAILS 395 pulmonate snails. His findings that both Helisoma species were “not typical” and “very rare” in this area do not correlate with those reported here, especially in the case of H. antrosa (Fig. 6). This could in- dicate either that during the particular year of his studies the numbers of these particular species were unusually low, or that the Big Shoal has changed dramatical- ly in the intervening 28 years. This appears quite probable in the light of a recent report by Bazin & Saunders (1971) which, on the basis of a gradual but steady in- crease in the hypolimnetic oxygen deficit in Douglas Lake during the past 50 years, indicates that the lake has very gradually become more eutrophic. Such а trend could be expected to involve an increase in littoral benthic productivity, reflected (in part) by an increase in biomass of pulmonate snails (Hunter, 1961) in the Big Shoal area and elsewhere. - А comparison of the distributions of Physa integra in Douglas Lake and in Lake West Okoboji (and other lakes nearby) in Iowa (Clampitt, 1970) is of considerable interest and of possible significance. In both lakes, populations of this species were concentrated in summer in a zone of cobbles adjacent to shore. Other pop- ulations in Lake Okoboji, away from shore, were found almost exclusively on sub- merged vegetation—Ceratophyllum, Myriophyllum, various species of Potamogeton, etc.; the snails appeared to avoid substrata of sand and silt. In Douglas Lake, in contrast, nearly all of the P. in- tegra which were found in somewhat deeper water (0.5 to 5.0 m deep) away from shore were on the bottom—on stones, submerged logs, dead shells, dead leaves and often on sand—and very few on living vegetation. This species illustrates what appears to be a more general con- trast between the distributions as to sub- stratum of Lake Okoboji and Douglas Lake snails. In Lake Okoboji, nearly all snails of all species living in deeper water—0.5 m or more—were on vege- tation whereas in Douglas Lake, they were nearly all on the bottom. This contrast was observed independently by a colleague, Dr. Eugene Stoermer (personal com- munication) who has done extensive SCUBA diving in both lakes. I believe that the relative progress of cultural (i.e., man- caused) eutrophication in the 2 lakes gives at least a partial explanation for this con- trast. Lake Okoboji gives evidence of be- ing much more eutrophic. Bovbjerg € Ulmer (1960) reported a drastic decline in species diversity among gastropod mol- lusks over a 45-year period in Lake Okoboji. These investigators noted par- ticularly the apparent elimination of a number of species of lymnaeid snails and of planorbids of the genus Helisoma, since earlier studies in the area by Shimek (1915, 1935). Among some 11 species of gas- tropods found in Lake Okoboji in 1960, only Physa gyrina and P. integra were pre- sent in really large numbers at widespread locations in the lake. The decline of the gastropod fauna was attributed to the progressive pollution and eutrophication of this very popular and heavily used lake. A similar but less drastic decline in the molluscan fauna of Oneida Lake, New York, has been reported recently by Har- mon & Forney (1970), and attributed to similar causes. Douglas Lake has been much less subject to human influence dur- ing the same interval of time, and if cultural eutrophication has been oc- curring, as suggested by the work of Bazin & Saunders (1971), it has been much more gradual and subtle in its effects. Certainly the gastropod fauna of Douglas Lake has not suffered the kind of depletion which it has undergone in Lake Okoboji. As has been already suggested, some species, such as H. antrosa, may actually have in- creased in biomass in certain areas such as the Big Shoal, reflecting increased benthic productivity associated with the very gradual eutrophication. It seems reason- able to suppose that the more rapid eutrophication of Lake Okoboji has led to changes in the substratum through in- creased growth of submerged vegetation, increased quantities of silt in vegetated zones, reduced productivity by microflora on the bottom, a corresponding increase in organic decomposition and consequent 396 reduction in the dissolved oxygen supply on the bottom. With such changes oc- curring in more and more of the littoral regions of the lake, only those species of snails which are already adapted to living on the vegetation, or are able to success- fully make the transition from the bottom to the vegetation, or are adapted to con- tinued life under anoxic conditions on the bottom, will survive. All others will be- come locally extinct. It seems reasonable to speculate that P. integra successfully made the transition from the bottom to the vegetation in Lake Okoboji, whereas most of the larger lymnaeid and planorbid species which were formerly represented in the lake did not. The questions which this idea raises warrant further descriptive and experimental studies on mollusks in a variety of lake habitats. ACKNOWLEDGEMENTS I am grateful to Dr. Warren L. Wittry, Director of Cranbrook Institute of Science, and the Board of Trustees of the same in- stitution, not only for their encouragement and support of this work, but also for their generosity in allowing me time away from the Institute. I wish to thank Dr. Frederick K. Sparrow, Jr., recently retired as Direc- tor of the University of Michigan Biological Station, for providing me with the opportunity to do research there. Mr. Michael Gambel, Mr. Marc Harrison and Mr. Thomas Pinson all gave valuable assistance with the field work. I am in- debted to others, notably Dr. Bruce Z. Lang (University of Michigan Biological Station and Eastern Washington State College) and Dr. Henry van der Schalie (University of Michigan), for their un- failing interest and encouragement. Dr. V. Elliott Smith, Cranbrook Institute of Science, kindly read and offered helpful criticism of the manuscript. LITERATURE CITED BAKER, F. C. 1928. The fresh water Mollusca of Wisconsin, Part 1, Gastropoda. Wisc. Geol. & Nat. Hist. Survey Bull., 70(1): 507 p. P. T. CLAMPITT BAKER, F. С. 1945. The molluscan family Planorbidae. Univ. Illinois Press, Urbana, Ill., 530 р. BAKER, H. B. 1912. A few notes on the Mollusca of the Douglas Lake region. Mich. Acad. Sci., 14th Report: 209-211. BAKER, H. B. 1914. Physiographic and molluscan succession in lake pools. Mich. Acad. Sci., 16th Report: 18-45. BAZIN, M. & SAUNDERS, G. W. 1971. The hypolimnetic oxygen deficit as an index of eutrophication in Douglas Lake, Michigan. Mich. Academician, 3(4): 91-106. BOVBJERG, R. V. & ULMER, M. J. 1960. An ecological catalogue of the Lake Okoboji gas- tropods. Proc. Iowa Acad. Sci., 67: 569-577. BOYCOTT, А. Е. 1936. Habitats of freshwater Mollusca in Britain. J. anim. Ecol., 5: 116- 186. СНЕАТОМ, Е. P. 1934. Limnological in- vestigations on respiration, annual migratory cycle, and other related phenomena in freshwater pulmonate snails. Trans. Amer. microsc. Soc., 53: 348-407. CLAMPITT, P. T. 1970. Comparative ecology of the snails Physa gyrina and Physa integra (Basommatophora: Physidae). Malacologia, 10: 113-151. CORT, W. W. 1936a. Studies on schistosome dermatitis. I. Present Status of the subject. Amer. J. Hyg., 23: 349-371. CORT, W. W. 1936b. Studies on schistosome dermatitis. IV. Further information on dis- tribution in Canada and the United States. Amer. J. Hyg., 24: 318-333. CORT, W. W., McMULLEN, D. B.,OLIVIER, L. € BRACKETT, S. 1940. Studies on schistosome dermatitis. УП. Seasonal in- cidence of Cercaria stagnicolae Talbot, 1936, in relation to the life eycle of its snail host, Stagnicola emarginata angulata (Sowerby). Amer. J. Hyg., 32(Sec. D): 33-69. CORT, W. W., OLIVIER, L. & McMULLEN, D. B. 1941. Larval trematode infection in juveniles and adults of Physa parkeri Currier. J. Parasitol., 27: 123-141. DAWLEY, C. 1947. Distribution of aquatic molluscs in Minnesota. Amer. Midl. Natur., 38: 671-697. EGGLETON, F. E. 1931. A limnological study of the profundal bottom fauna of certain fresh-water lakes. Ecol. Monogr., 1: 231-332. EGGLETON, F. E. 1935. A comparative study of the benthic fauna of four northern Michigan lakes. Pap. Mich. Acad. Sci. Arts & Lett., 20(1934): 609-644. SUBSTRATUM AND FRESHWATER SNAILS 397 FOX, D. L. 1960. Perspectives in marine bio- chemistry. Ann. N.Y. Acad. Sci., 90: 617-621. GANNON, J. E. & BRUBAKER, D. C. 1969. Sub-surface circulation in South Fishtail Bay, Douglas Lake, Cheboygan County, Michigan. Mich. Academician, 2(2): 19-35. GANNON, J. E. & FEE, E. J. 1970. Surface seiches and currents in Douglas Lake, Michigan. Limnol. Oceanogr., 15: 281-288. GOODRICH, C. 1932. The Mollusca of Michigan. Univ. Mich. Press, Ann Arbor, Mich., U.S.A. 120 p. GOODRICH, C. € van der SCHALIE, H. 1939. Aquatic mollusks of the Upper Penin- sula of Michigan. Misc. Publs. Mus. Zool., Univ. Mich. No.-43, 45 р. GOODRICH, C. € van der SCHALIE, H. 1944. A revision of the Mollusca of Indiana. Amer. Midl. Natur., 32: 257-326. HARMON, W. N. 1972. Benthic substrates: their effects on fresh-water Mollusca. Ecology, 53: 271-277. HARMON, W.N. & FORNEY, J. L. 1970. Fif- ty years of change in the molluscan fauna of Oneida Lake, New York. Limnol. Oceanogr., 15: 454-460. HUNTER, W. R. 1953. The condition of the mantle cavity in two pulmonate snails living in Loch Lomond. Proc. Roy. Soc. Edinb. 65B(11): 143-165. HUNTER, W. R. 1957. Studies on freshwater snails at Loch Lomond. Glasgow Univ. Publ., Stud. Loch Lomond, 1: 56-95. HUNTER, W. R. 1961. Annual variations in growth and density in natural populations of freshwater snails in the West of Scotland. Proc. zool. Soc. London, 136: 219-253. HUNTER, W. R. 1964. Physiological aspects of ecology in nonmarine molluscs. In: K. M. Wilbur & C. M. Yonge (eds.), Physiology of Mollusca 1: 83-126, Academic Press, N.Y. & London. HYMAN, L. H. 1967. The Invertebrates VI. Mollusca 1. McGraw-Hill Book Co., N.Y., 792 p. MACAN, T. T. 1950. Ecology of fresh-water Mollusca in the English Lake District. ]. anim. Ecol., 19: 124-146. MACAN, T. T. 1963. Freshwater Ecology. John Wiley & Sons, N.Y., 338 p. МОЕЕЕТТ, J. W. 1943. A limnological in- vestigation of the dynamics of a sandy, wave- swept shoal in Douglas Lake, Michigan. Trans. Amer. microsc. Soc., 62: 1-23. MOORE, G. M. 1939. A limnological investiga- tion of the microscopic benthic fauna of Douglas Lake, Michigan. Ecol. Monogr., 9: 937-082. NEEL, J. K. 1948. A limnological investigation of the psammon in Douglas Lake, Michigan, with especial reference to shoal and shoreline dynamics. Trans. Amer. microsc. Soc., 67: 1- 53. SHIMEK, В. 1915. The Mollusca of the Okoboji region. Bull. U. Iowa, 7(2): 70-88. SHIMEK, B. 1935. The effect of pollution on the mollusks in Iowa. Nautilus, 48(4): 109- RTE WELCHMPEMNSMM927 “Limnological «me vestigations on northern Michigan lakes. 1. Physical-chemical studies on Douglas Lake. Pap. Mich. Acad. Sci. Arts & Lett., 8: 421- 451. WILSON, I. T. 1944. A study of the sediment in Douglas Lake, Cheboygan County, Michigan. Pap. Mich. Acad. Sci. Arts & Lett., 30: 391-419. YOUNG, O. W. 1945. A limnological investiga- tion of periphyton in Douglas Lake, Michigan. Trans. Amer. microsc. Soc., 64: 1- 20. ZUSAMMENFASSUNG DAS SUBSTRAT ALS VERBREITUNGSBESTIMMENDER FAKTOR FUR LUNGEN-SCHNECKEN IM DOUGLAS LAKE, MICHIGAN Р. Т. Clampitt Dem Substrat als verbreitungsbestimmendem Faktor fiir 5 Lungenschnecken-Arten aus dem Douglas Lake, Cheboygan County, Michigan, wurde eine Studie gewidmet. Quantitative Aufsammlungen am natürlichen Standort, zusammen mit Laborversuchen, ergaben, daß adulte Physa integra Haldeman Hartsubstrate wie Steine bevorzugen; im Gegensatz dazu bevorzugen adulte Helisoma antrosa percarinata (Walker) sandiges Substrat. Wenn im Laborversuch Nahrung (Algen oder Detritus) sowohl auf Steinen als 398 P/ T° CLAMPITT auch auf Sand vorhanden war, war die durchschnittliche Verteilung von P. integra: 58% auf Steinen und 8% auf Sand (Unterschied hoch signifikant), während in entsprechenden weiteren Experimenten mit H. antrosa sich im Durchschnitt 24% auf dem Steinsubstrat und 39% auf dem sandigen einfanden (Unterschied ebenfalls signifikant). Physa parkeri “Currier” DeCamp, Stagnicola emarginata angulata (Sowerby) und Helisoma cam- panulata smithi (Baker) zeigten in der Natur komplexere und unterschiedlichere Ver- breitungsmuster, was das Substrat betrifft. Im Labor zeigte P. parkeri, sehr ähnlich wie P. integra, eine Präferenz für steiniges Substrat, wenn Nahrung vorhanden war. H. cam- panulata war im Durchschnitt zu 29% auf Steinen und zu 29% auf Sand verteilt, wenn beide Substrate Nahrung enthielten. Beziehungen bei den 5 Arten zwischen Substrat zum einen und Tiefe, Wellenschlag, Nahrung, Ablaichsubstrat und respiratorischen An- forderungen zum anderen werden diskutiert. C.M.-B. RESUME LE SUBSTRAT, FACTEUR DE DISTRIBUTION DES MOLLUSQUES PULMONES DANS LE LAC DOUGLAS, MICHIGAN P. T. Clampitt On a réalisé une étude sur le substrat considéré comme facteur de distribution pour 5 espéces de pulmonés du lac Douglas, Cheboygan County, Michigan. Des échantillon- nages dans la nature, en méme temps que des expériences au laboratoire ont révélé que les adultes de Physa integra Haldeman preferent les substrats durs tels que les pierres; au contraire, les adultes d’Helisoma antrosa percarinata (Walker) préférent un substrat sableux. Quand de la nourriture (algues et détritus) était présente а la fois sur le sable et sur les pierres, au laboratoire, la moyenne de P. integra a été de 58% sur les pierres et de % sur le sable (différence hautement significative), tandis que dans une experience équivalente mais séparée, une moyenne de 24% de H. antrosa se trouvait sur les pierres et de 39% sur le sable (significatif aussi). Physa parkeri “Currier” Decamps, Stagnicola emarginata angulata (Sowerby) et Helisoma campanulata smithi (Baker) ont tous montré des types de distribution plus complexes et plus variés vis-à-vis du substrat dans la nature. Au laboratoire, P. parkeri a montré une préférence pour le substrat pierreux trés similaire а celle de P. integra quand la nourriture était présente. La distribution moyenne de H. campanulata était de 29% sur les pierres et aussi de 29% sur le sable quand la nourriture était présente sur chacun d'eux. On aussi discuté, pour les 5 especes, des relations entre, d'une part le substrat et d’autre part: la profondeur, l'action des vagues, la nourriture, les lieux de ponte et les besoins respiratoires. A.L. RESUMEN EL SUBSTRATO COMO FACTOR EN LA DISTRIBUCION DE CARACOLES PULMONADOS, EN EL LAGO DOUGLAS, MICHIGAN P. T. Clampitt Se estudiö el substrato en el Lago Douglas, condado de Cheboygan, Michigan, como un factor en la distribuciön de cinco especies de pulmonados. Muestras cuantitativas y experimentos en laboratorio revelaron que los adultos de Physa integra Haldeman, prefieren substratos duros, de piedra; contrariamente, Helisoma antrosa percarinata SUBSTRATUM AND FRESHWATER SNAILS (Walker) prefieren fondos de arena. La presencia de alimento (algas o detritos) sobre las piedras о arena mostró, en el laboratorio, un promedio de 58% en la distribución de P. in- tegra en piedras y 8% en la arena (diferencia muy significativa), mientras que en otros experimentos, equivalentes pero separados, H. antrosa mostró solamente 24% de preferencia por piedras, y 39% de arena. Р. parkeri “Currier” DeCamp, Stagnicola emarginata angulata (Sowerby) y Helisoma campanulata smithi (Baker) tienen patrones de distribución más complejos y variados con respecto a los substratos naturales. En el laboratorio P. parkeri mostró preferencia por un substrato de piedra, muy similar al de P. integra cuando habia alimento presente. El promedio de distribución de H. campanulata fue de 29% en piedras y tambien 29% en arena cuando ambos ofrecian alimento. Relaciones de las cinco especies entre substratos por una parte, y produndidad, acción de oleaje, alimento, sitios de ovoposición y necesidades respiratorias por la otra, se discuten en el trabajo. J.J.P. ABCTPAKT CYBCTPAT, КАК ФАКТОР, ВЛИЯЮ НА РАСПРОСТРАНЕНИЕ МОЛЛЮСКОВ PULMONATA В ОЗЕРЕ ДУГЛАС, МИУИГАН П.Т. KISMIMT Изучался субстрат, как фактор, влияющий на распространение 5 видов моллюсков из Pulmonata (озеро Дуглас, Чебойган, Мичиган). Сбор количественных проб, вместе с лабораторными экспериментами показал, что взрослые Physa integra Haldeman предпочитают твердый субстрат (камни); взрослые Helisoma ат тоза percarinata (Walter), напротив, предпочитют песок. Если пища (водоросли или детрит) имелись в лабораторных условиях или на песке, среднее распространение P. integra составляло 58% на камнях и 8% Ha песке (очень значительное различие), в то время как в отдельных эквивалентных экспериментах, в среднем 24% Н. antrosa были на камнях и 30% - на песке (различия также значительные). Physa parkeri “Currier”? DeCamp, Stagnicola emarginata angulata (Sowerby) и Нейзота campanulata smithi (Baker) все имеют более сложное и изменчивое распространение, связанное не только с природным субстратом. В лабораторных условиях Р. parkeri предпочитает каменный субстрат, подобно Р. integra (если пища имеется). В среднем, распространение H. campanulata на 29% связано с камнями и на 29% - ec песком, если пища имеется тут и там. В статье обсуждается отношение 5 видов моллюсков к субстрату, глубине, действию волн, пище, местам откладки яиц и потребностям дыхания. ZERS ER 399 Y PT OVATE. 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INDEX TO SCIENTIFIC NAMES abbreviata, Coralliophila, 315, 329 Abra, 6, 47, 77 aequalis, 47, 77 abyssicola, Volutocorbis, 309, 310 Achatina, 168, 189, 206, 207 Actinonaias, 97-113 cavinata, 97-113 ligamentina, 100 acuta, Paludomus, 134 adamsi, Seila, 27, 30, 39, 40 Adula, 269, 272, 273, 274, 277 adusta, Ampullaria, 349 adustus, Penion, 314, 321 aequalis, Abra, 47, 77 Aequipecten, 39, 40 irvadians, 39, 40 Aetheria, 369 elliptica, 369 Aforia, 310 goodei persimilis, 310 Agriolimax, 206 albula, Maoritomella, 305 Alcithoe, 301, 310, 315, 316, 318, 319, 321 arabica, 301, 310, 315, 316, 319, 321 Alectrion, 313 aoteanus, 313 alexandrina, Biomphalaria, 115-122 alexandrina watsoni, Biomphalaria, 115-122 alluaudi, Planorbis, 365 alluaudi, Tropidiscus, 365 alternatum, Bittium, 24-30, 39, 40 amaena, Cleopatra, 351, 352 Amalda, 304, 310, 313 australis, 310, 313 amarula, Helix, 359 amarula, Melania, 359 amarula, Thiava, 359, 360 ambiguus, Xymene, 310 Amblema, 97-113 plicata, 97-113 Ameria, 364 lirata, 364 americanus, Modiola, 284, 291 amouretta, Harpa, 310 Ampelisca, 21, 38 Amphipholis, 39, 40 squamata, 39, 40 Ampullariidae, 123, 124, 175, 186, 187, 188, 189, 206, 207 Ampullaria, 124, 125, 146, 147, 168, 186-189, 205-207, 348-350 adusta, 349 canaliculata, 124, 125, 146, 147, 168, 189, 205 cecillii, 349, 350 depressa, 124, 205, 206 filosa, 350 gigas, 147, 187-189, 205, 206 gvasseti, 348, 349 hanleyi, 349 largillierti, 349 madagascariensis, 349 ovum, 349 polita, 124, 147, 186, 188 simplex, 349 subscutata, 349 urceus, 187, 189 Amygdalum, 50, 51, 54, 64, 65, 88, 91 papyrid, 50, 51, 54, 64, 65, 88, 91 (401) Anachris, 13-46 avara, 22, 26-29, 36, 39, 40 avara similis, 13-46 translivata, 36, 37 Anadara, 13-46, 51, 54, 59, 60, 61, 88, 91 ovalis, 51, 54, 59, 61, 62, 88, 91 transversa, 13-46, 51, 54, 59, 60, 62, 88, 91 anceps percarinata, Helisoma, 380 Ancilla, 304 Ancillista, 304 cingulata, 304 Ancylidae, 379 Ancylus, 366 modestus, 366 angulata, Lymnaea emarginata, 380 angulata, Stagnicola emarginata, 379-399 angusta, Segmentina, 365 angustus, Segmentorbis, 365, 367 Anisus, 364, 365 crassilabrum, 364, 365 annulata, Nucula, 25 Anodonta, 97, 100, 104, 109, 110 cygnea, 97, 100, 109, 110 Anodontinae, 97 Anodontoides, 110 ferrussacianus, 110 Anomia, 24, 27, 29, 39, 40, 51, 54, 67, 68, 88 simplex, 24, 27, 29, 39, 40, 51, 54, 67, 68, 88 antiqua, Neptunea, 310, 313 antrosa percarinata, Helisoma, 379-399 aoteanus, Alectrion, 313 aoteanus, Nassarius, 313 apertus, Caillaudia, 365 apertus, Gyraulus, 365, 366 apertus, Planorbis, 365 apiculata, Chaetopleura, 13-46 arabica, Alcithoe, 310, 315, 316, 319, 321 Arbacia, 39, 40 punctulata, 39, 40 Archaeogastropoda, 186-188, 206, 295-297, 299, 301 Architaenioglossa, 123 Arcidae, 59 Arcuatula, 283, 291 arcuatula, Modiola, 283 avenaria, Mya, 47, 48, 83, 88, 90 argentea, Thuiaria, 51 Argopecten, 24, 26, 27, 29, 47, 67, 88, 90 irvadians, 24, 26, 27, 29, 47, 67, 88, 90 Arion, 206, 207 Ariophanta, 188, 206 Artemia, 109 aspera, Pirena, 357 Aspidobranchia, 186 Asprella, 310 mucronatus, 310 Asterias, 39, 40 forbesi, 39, 40 Astrangia, 39, 40 danae, 39, 40 Atrina, 291 rigida, 291 audeberti, Doryssa, 357 aurea, Venerupis, 225-245 auricularia, Lintricula, 309, 318 auricularia, Olivancillaria, 309, 318 auriculata, Neripteron, 342 auriculata, Neritina, 342, 344 402 MALACOLOGIA Busycon, 24, 26, 27, 30, 39, 40, 309, 321 canaliculatum, 24, 26, 27, 30, 39, 40, 309 australiensis, Peristernia, 310 australis, Amalda, 310, 313 australis, Baryspira, 310, 313 contrarium, 309 australis, Microvoluta, 310 Byssanodonta, 373 Austrofusus, 314, 321 degorteri, 373 glans, 314, 321 ferruginea, 373 Austromitra, 302, 309, 320 Caelatura, 368 rubiginosa, 309 geayi, 368 avara, Anachris, 22, 26-29, 36, 39, 40 madagascariensis, 368 avara similis, Anachris, 13-46 malgachensis, 368 Babylonia, 313 Caenogastropoda, 296 balthica, Macoma, 1, 52, 55, 74-76, 88, 90 caffra, Nevita, 342 Bankia, 85, 88 caffra, Neritina, 342 gouldi, 85, 88 Caillaudia, 365 Barnea, 51, 54, 83, 84, 88, 90, 91 apertus, 365 truncata, 51, 54, 83, 84, 88, 90, 91 calcitrans, Chaetoceros, 226 Baryspira, 310, 313 caldwelli, Nautilina, 364 australis, 310, 313 caldwelli, Planorbis, 364 bavayi, Pyrgophysa, 364 californianus, Tagelus, 1-11 Bedeva, 310 Calyptraea, 188 hanleyi, 310 camerunensis, Biomphalaria, 115-122 camerunensis manzadica, Biomphalaria, 115 bengalensis, Neritina, 340 campanulata smithi, Helisoma, 379-399 betafoense, Pisidium, 372 canaliculata, Ampullaria, 124, 125, 146, 147, biangulata, Paludina, 356 168, 189, 205 bicarinata, Melania, 356 canaliculata, Pomacia, 188, 189 biconica, Microvoluta, 314 canaliculatum, Busycon, 24, 26, 27, 30, 39, 40, bimaculata, Navicella, 346 309 Biomphalaria, 115-122, 214, 367, 368 Cancellaria, 299, 310, 321 alexandrina, 115-122 Cancellariacea, 295, 300, 304, 307, 323, 324 alexandrina watsoni, 115-122 Cancellariidae, 299, 304, 306, 308, 309, 310, camerunensis, 115-122 311, 315, 317, 323 bengalensis, Nerita corona, 340 camerunensis manzadica, 115 madagascariensis, 367, 368 pfeifferi, 115-122, 368 sudanica tanganyicensis, 115-122 Bithynia, 188, 214 Bittium, 24-30, 39, 40 alternatum, 24-30, 39, 40 Bivalvia, 1, 109, 265, 283 boothi, Philbertina, 305 borbonica, Cimber, 346 borbonica depressa, Navicella, 346 borbonica, Navicella, 346 borbonica, Patella, 345 borbonica, Septaria, 345-347 borboniciensis, Septaria, 346 Borsonia, 305 Borsoniinae, 305 Botula, 273 Brachidontes, 64, 88, 91 recurvus, 64, 88, 91 brevispina, Clithon, 339 brevispina, Neritina, 339 brevispina, Ophioderma, 39, 40 Buccinacea, 295, 296, 302, 308, 315, 325, 330 Buccinidae, 295-331 Buccinulidae, 325 Buccinulum, 314 Buccinum, 299, 307, 309, 310, 312, 313, 316, 321, 356 flumineum, 356 undatum, 309, 310, 313 Bullia, 302 Bulinus, 119, 363, 364 liratus, 364 madagascariensis, 364 mariei, 363, 364 cancellata, Daphnella, 305 cancellata, Tevebra, 305 Cancilla, 310 capense, Sphaerium, 373 Cardiidae, 70 Carditidae, 67 Cardium, 371 casertanum, 371 carinata, Actinonaias, 97-113 carinulata, Paludina, 353 cavoliniana, Polymesoda, 68, 88 casertanum, Cardium, 371 casertanum, Pisidium, 371, 372 caudata, Eupleura, 13-46 cecillei, Pachylabra, 350 cecillii, Ampullaria, 349, 350 cecillii, Pila, 349, 350, 351 celata, Cliona, 39, 40 Cenodagreutes, 305, 306 Cephalopoda, 188 ceramicum, Vasum, 310 Cerastoderma, 27, 30, 39, 40 pinnulatum, 27, 30, 39, 40 Ceratodes, 124 Ceratophyllum, 395 Cerithidea, 361, 362 decollata, 361, 362 Cerithiopsis, 27, 30, 39, 40 subulata, 27, 30, 39, 40 Cerithium, 361 decollatum, 361 Chaetoceros, 226 calcitrans, 226 Chaetopleura, 13-46 apiculata, 13-46 Chama, 90 INDEX, VOL. 12 403 congregata, 90 Chara, 385 chevalieri, Segmentina, 365 Chione, 7 Chlorella, 58 Cimber, 346 borbonica, 346 cinerea follyensis, Urosalpinx, 247-249, 253, 256, 257, 259 cinerea, Hastula, 305 cinerea, Urosalpinx, 26, 27, 29, 39, 40, 247-263 cingulata, Ancillista, 304 clausa, Natica, 24, 27, 30, 36, 38-40 Clavatulinae, 305 Clavinae, 300, 305, 308, 319 Cleopatra, 350, 352, 353, 354 amaena, 351, 352 colbeaui, 352 grandidieri, 353, 354 mangoroensis, 352 cleopatra, Melania, 350 Cliona, 39, 40 celata, 39, 40 Clithon, 339-341 brevispina, 339 longispina, 340 madecassina, 340, 341 rhyssodes, 340 spiniperda, 340, 341 Clypeolum, 340, 341 pulligera knorri, 340, 341 coacta, Melania, 358 coerulescens, Hastula, 310 coerulescens, Impages, 310 colbeaui, Cleopatra, 352 colbeaui, Paludina, 352 Colubraria, 304, 327, 328 maculosa, 327 muricata, 327 sowerbyi, 327 Colubrariidae, 302-331 Columbariidae, 307 Columbarium, 305, 310, 329 pagodum, 310 Columbellidae, 328 Colus, 314 gracilis, 314 Coluzea, 305, 306, 329 mariae, 329 spiralis, 329 Cominella, 307, 314 Cominellidae, 325 Comitas, 305 onokeana, 305 onokeana vivens, 305 commersoni, Nerita, 361 Conacea, 295-331 Concholepas, 303 peruviana, 303 Congeria, 47, 51, 54, 68, 69, 88, 90 leucophaeta, 47, 51, 54, 68, 69, 88, 90 congregata, Chama, 90 Conidae, 299, 305, 310, 311 Conorbiinae, 305 consimilis, Neritilia, 348 consimilis, Neritina, 348 contrarium, Busycon, 309 conularis, Imbricaria, 319 Conus, 307, 310, 313, 318, 319 lividus, 307 mediterraneus, 312, 318, 319 mucronatus, 310 convexa, Crepidula, 24, 27, 29, 39, 40 cookii, Navicella, 345, 346 Coralliophila, 303, 307, 315, 329 abbreviata, 315, 329 Coralliophilidae, 329 Corbicula, 265-281, 369-372 madagascariensis, 369, 371, 372 manillensis, 265-281 sikorae, 371 Corbiculidae, 68 cornuarietis, Marisa, 123-210 cornula, Melania, 359 cornuta, Melania, 359 corona bengalensis, Nerita, 340 corona, Melongena, 309 costata, Cyrtopleura, 52, 55, 84, 85, 88, 91 crassa, Physa sayi, 380 crassa, Pseudoliva, 310 crassilabrum, Anisus, 364, 365 crassilabrum, Gyraulus, 365 crassilabrum, Planorbis, 364, 365 Crassinella, 27-29, 32, 34, 35, 39, 40 mactracea, 27-29, 32, 34, 35, 39, 40 Crassostrea, 48, 65, 66, 88, 247-249 virginica, 48, 65, 66, 88, 247-249 crennularis, Inquisitor, 310 crenulata, Pterygia, 310 Crepidula, 13-46, 146, 168, 206, 214, 215, 219 convexa, 24, 27, 29, 39, 40 fornicata, 13-46 plana, 24, 26-29, 39, 40 cretaceus, Plesiotriton, 328 cuneata, Rangia, 47, 53, 56, 82, 83, 88, 90 cuneiformis, Martesia, 47, 84 cybele, Melania, 359 Cyclas, 372, 373 ferruginea, 373 madagascariensis, 373 Cyclope, 302, 310, 313 neritea, 310, 313 Cyclostoma, 356 unicolor, 356 cygnea, Anodonta, 97, 100, 109, 110 Cyllene, 310 lyrata, 310 Cymatiidae, 304, 327 Cyrtopleura, 52, 55, 84, 85, 88, 91 costata, 52, 55, 84, 85, 88, 91 dalei, Liomesus, 310 danae, Astrangia, 39, 40 Daphnella, 305 cancellata, 305 Daphnellinae, 305 debauxiana, Melanatria, 357 debeauxiana, Pirena, 356, 357 debilis, Splendrillia, 305 decollata, Cerithidea, 361, 362 decollata, Melania, 361 decollata, Pirenella, 361 decollatum, Cerithium, 361 decollatus, Potamides, 361 degorteri, Byssanodonta, 373 degorteri, Eupera, 373, 374 demissus granosissimus, Mytilus, 284, 286, 290 404 MALACOLOGIA demissus, Modiolus, 64, 88, 91, 283-293 demissus, Mytilus, 283, 284 Dentalium, 213-215, 219 depressa, Ampullaria, 124, 205, 206 depressa, Navicella, 345 depressa, Navicella borbonica, 346 desetangsii, Scabricola, 310 Diluculum, 310, 311, 315 inopinatum, 310 Diotocardia, 186 Diplomeriza, 310 duplicata, 310 Diplothyra, 84 smithii, 84 directus, Ensis, 22, 27, 30, 39, 40, 52, 55, 79, 88 discus, Dosinia, 47, 71 divisus, Tagelus, 27, 30, 79 Domiporta, 310 Donacidae, 77 Donax, 47, 52, 55, 77, 78, 88-90 gouldi, 1, 7 variabilis, 47, 52, 55, 77, 78, 88-90 Doryssa, 357 audeberti, 357 Dosinia, 47, 71 discus, 47, 71 Dreissena, 265-281 polymorpha, 265-281 siamensis, 266 Dreissenidae, 68 Drillia, 310 umbilicata, 310 Drupa, 307 dubius, Taron, 314, 318 duclosiana, Pseudanachis, 310 duisabonis, Melania, 356 duplicarinata, Proneptunea, 310 duplicata, Diplomeriza, 310 duplicatus, Polinices, 26, 30, 39, 40 edouardi, Pisidium, 371 edulis, Mytilus, 47, 48, 63-65, 88, 90, 247, 268, 269, 273, 284-288 Egeria, 4 radiata, 4 Elara, 346 suborbicularis, 346 electa, Limnaea, 363 elliptica, Aetheria, 369 elliptica, Etheria, 369 elliptica, Navicella, 345, 346 emarginata angulata, Lymnaea, 380 emarginata angulata, Stagnicola, 379-399 Ensis, 22, 27, 30, 39, 40, 52, 55, 79, 88 directus, 22, 27, 30, 39, 40, 52, 55, 79, 88 Epidirona, 305 gabensis, 305 erinaceus, Ocenebra, 308, 313, 316 Etheria, 369 elliptica, 369 Eupera, 373, 374 degorteri, 373, 374 ferruginea, 373 Eupleura, 13-46 caudata, 13-46 eximia, Navicella, 346 fasciata, Venus, 225-245 Fasciolaria, 206 Fasciolariidae, 295-331 Ferrissia, 366, 367 modesta, 366, 367 ferruginea, Byssanodonta, 373 ferruginea, Cyclas, 373 ferruginea, Eupera, 373 ferruginea, Limosina, 373 ferruginea, Sphaerium, 373 ferrussacianus, Anodontoides, 110 filosa, Ampullaria, 350 flava, Fusconaia, 97-113 Florimetis, 1-11 obesa, 1-11 fluminea, Melanatria, 356-358, 361 fluminea, Pirena, 356, 357 flumineum, Buccinum, 356 follyensis, Urosalpinx cinerea, 247-249, 253, 256, 257, 259 forbesi, Asterias, 39, 40 fornicata, Crepidula, 13-46 fortunei, Limnoperna, 265-281 fortunei, Modiola, 266 fortunei, Volsella, 266 Fulgerca, 328 fulgetrum, Neritina, 342 Fulgur, 206 Fungiacava, 268 Fusconaia, 97-113 flava, 97-113 Fusidae, 327 Fusinidae, 327, 329 Fusinus, 327 gabensis, Epidivona, 305 gagates, Neritaea, 343 gagates, Neritina, 342, 343, 345 gagates, Vittina, 342, 343 galbana, Isochrysis, 226 Galeodidae, 302, 305, 307, 309, 321, 325-327 Gastropoda, 109, 124, 213 geayi, Caelatura, 368 geayi, Nodularia, 368 geayi, Unio, 368 geayi, Zairia, 368 Gemma, 50, 52, 55, 72, 88 gemma, 50, 52, 55, 72, 88 gemma, Gemma, 50, 52, 55, 72, 88 Geukensia, 283, 284 gibberula, Pyrene, 310 gibberula, Strombina, 310 gigas, Ampullaria, 147, 187, 188, 189, 205, 206 glans, Austrofusus, 314, 321 globosa, Pila, 124, 125, 128, 146, 147, 168, 169, 187-189, 205 Goniobasis, 394 livescens, 394 goodei persimilis, Aforia, 310 goudotiana, Melanatria, 357 gouldi, Bankia, 85, 88 gouldi, Donax, 1, 7 gouldiana, Pandora, 22, 24, 26, 27, 29, 39, 40 gracilis, Colus, 314 gvandidieri, Cleopatra, 353, 354 grandidieri, Paludomus, 353 gvanosissimus, Mytilus demissus, 284-286, 290 Granulifusus, 310 niponicus, 310 granulosa, Pirena, 356 gvasseti, Ampullaria, 348, 349 gvasseti, Lanistes, 349 INDEX, VOL. 12 405 gvasseti, Lanistes olivaceus, 348, 349 johnsoni, Pisidium, 371, 372 grasseti, Lanistes ovum, 347 junghuhni, Navicella, 346 gvasseti, Meladomus, 349 junonia, Scaphella, 310 gvasseti, Meladomus olivaceus, 349 knorri, Clypeolum pulligera, 340, 341 Gyraulus, 365, 366 knorri, Nerita, 341 apertus, 365, 366 knorri, Neritina, 341 crassilabrum, 365 knorrit, Neritina pulligera, 340 gyrina, Physa, 380, 395 knorrii, Neritina, 341 Haedropleuva, 319 lacustris, Modiola, 266 septangularis, 319 Laevicardium, 22, 24-29, 32, 35, 39, 40, 52, 55, Haliotis, 146, 186, 206, 297, 299 70, 88, 90 Haloginella, 310 mortoni, 22, 24-29, 32, 35, 39, 40, 52, 55, 70, philippinarum, 310 88, 90 hanleyi, Ampullaria, 349 lamarckii, Melanopsis, 356 hanleyi, Bedeva, 310 lamarckii, Pirena, 356 hanleyi, Pachylabra, 349 lamellata, Physa, 364 Harpa, 310, 313, 330 Lampsilinae, 100 amouretta, 310 Lampsilis, 97-113 Harpidae, 303-331 ovata ventricosa, 99 Hastula, 305, 310, 320 radiata luteola, 100 cinerea, 305 radiata siliquoidea, 97-113 coerulescens, 310 Lanistes, 347, 348, 349 hedleyi, Peculator, 314 gvasseti, 349 Helisoma, 379-399 olivaceus grasseti, 348, 349 anceps percarinata, 380 ovum, 349 antrosa percarinata, 379-399 ovum gvasseti, 347 campanulata smithi, 379-399 ovum plicosus, 349 Helix, 207, 359 ovum striata, 349 amarula, 359 plicosus ovum, 348 Heterodontida, 67 striatus, 349 Heterogastropoda, 296 lapillus, Nucella, 308, 313, 315, 316 hildebrandti, Physa, 364 lapillus, Thais, 258, 259 hildebrandti, Planorbis, 365 largillierti, Ampullaria, 349 Hindsia, 303 largillierti, Pachylabra, 349 Hivudo, 108 latevalis, Mulinia, 26, 30, 52, 56, 81, 82, 88 medicinalis, 108 Leptodesma, 38 Hormospira, 310 leucophaeta, Congeria, 47, 51, 54, 68, 69, 88, 90 maculosa, 310 Leucozonia, 314, 316, 318 hovarum, Limnaea, 363, 364 nassa, 314 hovarum, Radix, 363, 364 leufroyi, Philbertina, 305 hyalina, Lyonsia, 22, 26, 27, 30, 39, 40, 52, 55, ligamentina, Actinonaias, 100 86, 88, 90 limatula, Yoldia, 13-47, 59, 88 Ilyanassa, 213-223, 310, 313 Limax, 168, 188, 207 obsoleta, 310, 313 Limnaea, 363, 364 Imbricaria, 319 electa, 363 conularis, 319 hovarum, 363, 364 Impages, 310 Limnoperna, 265-281 coerulescens, 310 fortunei, 265-281 incisa, Nephtys, 21, 38 Limosina, 373 inconstans, Xenostrobus, 269, 276 ferruginea, 373 incrassatus, Nassarius, 318 lineata, Navicella, 346 inopinatum, Diluculum, 310 lineata, Septaria, 346, 347 Inquisitor, 310 lingulata, Pirena, 356 crennularis, 310 Lintricula, 309, 318, 320 integra, Physa, 379-399 auricularia, 309, 318 Iredalula, 310, 327 Liomesus, 310 striata, 310, 327 dalei, 310 ivvadians, Aequipecten, 39, 40 lirata, Ameria, 364 irradians, Argopecten, 24, 26, 27, 29, 47, 67, 88, lirata, Physa, 364 90 livatus, Bulinus, 364 Ischadium, 283, 284, 285, 289, 291 livatus, Isidora, 364 recurvum, 283, 284, 285, 289, 291 Lithophaga, 268, 269, 273 Isidora, 364 Littorina, 146, 168, 188, 299 livatus, 364 Littorinacea, 320 madagascariensis, 364 livescens, Goniobasis, 394 Isochrysis, 226 lividus, Conus, 307 galbana, 226 longispina, Clithon, 340 johnsoni, Melanatria, 357 longispina, Neritina, 340 406 MALACOLOGIA longispina, Paranerita, 340 Marginellidae, 295-331 Lora, 316, 320 mariae, Coluzea, 329 travelliana, 316 mariei, Bulinus, 363, 364 turricula, 320 mariei, Pyrgophysa, 364 Loxonematacea, 302 marina, Zostera, 58, 90 Lucina, 47, 52, 55, 68, 69, 88, 90 Marisa, 123-210 multilineata, 47, 52, 55, 68, 69, 88, 90 cornuarietis, 123-210 luhdorffi, Parabathytoma, 305 martensi, Meteutria, 310 Lunarca, 24, 26, 27, 30, 39, 40 Martesia, 47, 84 ovalis, 24, 26, 27, 30, 39, 40 cuneiformis, 47, 84 lunata, Mitrella, 22, 24, 26, 27, 29, 39, 40 masoni, Schistosoma, 115, 119 luteola, Lampsilis radiata, 100 maura, Pivena, 356 lutheri, Monochrysis, 226 medicinalis, Hivudo, 108 Lunatia, 27, 30 mediterraneus, Conus, 312, 318, 319 triseriata, 27, 30 Meladomus, 349 Lymnaea, 109, 214, 219, 380 grasseti, 349 emarginata angulata, 380 olivaceus grasseti, 349 Lymnaeidae, 380 ovum plicosus, 349 Lyonsia, 22, 26, 27, 30, 39, 40, 52, 55, 86, 88, 90 Melanatria, 356-361 hyalina, 22, 26, 27, 30, 39, 40, 52, 55, 86, 88, debauxiana, 357 90 fluminea, 356, 357, 358, 361 Lyonsiidae, 86 goudotiana, 357 lyrata, Cyllene, 310 johnsoni, 357 Macoma, 1, 4, 6-8, 13-46, 47, 52, 55, 74-76, 77, madagascariensis, 357 88, 90 Spinosa, 356, 357 baltica, 7, 52, 55, 74-76, 88, 90 Melania, 168, 350, 356, 359, 361 mitchelli, 47, 52, 55, 56, 76, 77, 90 amarula, 359 nasuta, 1, 4, 6-8 bicarinata, 356 phenax, 88 cleopatra, 350 secta, 6-8 coacta, 359 tenta, 13-46, 77, 88, 90 cornula, 359 mactracea, Crassinella, 27-29, 32, 34, 35, 39, 40 cornuta, 359 Mactridae, 80 cybele, 359 maculata, Terebra, 306 decollata, 361 maculosa, Colubraria, 327 duisabonis, 356 maculosa, Hormospira, 310 madagascariensis, 356 madagascariense, Sphaerium, 373 thiarella, 359 madagascariensis, Ampullaria, 349 tuberculata, 361 madagascariensis, Biomphalaria, 367, 368 Melanoides, 361 madagascariensis, Bulinus, 364 tuberculatus, 361 madagascariensis, Caelatura, 368 Melanopsis, 356 madagascariensis, Corbicula, 369, 371, 372 lamarckii, 356 madagascariensis, Cyclas, 373 Spinosa, 356 madagascariensis, Isidora, 364 Melongena, 309, 313, 327, 328 madagascariensis, Melanatria, 357 corona, 309 madagascariensis, Melania, 356 melongena, 309 madagascariensis, Pachylabra, 349, 350 melongena, Melongena, 309 madagascariensis, Paludina, 353 Melongenidae, 295, 310, 311, 314, 327 madagascariensis, Paludomus, 352, 353 Mercenaria, 27, 30, 70, 71, 88 madagascariensis, Physa, 364 mercenaria, 27, 30, 70, 71, 88 madagascariensis, Pirena, 356, 357 mercenaria, Mercenaria, 27, 30, 70, 71, 88 madagascariensis, Pisidium, 371 Mesogastropoda, 123, 175, 186, 187, 295-298, madagascariensis, Planorbis, 367 301, 327 madagascariensis, Unio, 368 mestayerae, Ratifusus, 305, 327 madecassina, Clithon, 340, 341 Meteutria, 310 madecassina, Neritina, 339 martensi, 310 Magilidae, 302, 303, 306-309, 314-316, 321, 326, Metula, 328 329 Microciona, 39, 40 Magilus, 303, 329 prolifera, 39, 40 malgachensis, Caelatura, 368 Microvoluta, 310, 314 malgachensis, Unio, 368 australis, 310 Mangelia, 316, 319 biconica, 314 Mangeliinae, 305 Microvolutidae, 301, 307, 330, 331 mangoroensis, Cleopatra, 352 mitchelli, Macoma, 47, 52, 55, 56, 76, 77, 90 manillensis, Corbicula, 265-281 Mitracea, 325 manzadica, Biomphalavia camerunensis, 115 Mitrella, 22, 24, 26, 27, 29, 39, 40 Maoritomella, 305 lunata, 22, 24, 26, 27, 29, 39, 40 albula, 305 Mitridae, 299-331 INDEX, VOL. 12 modesta, Fervissia, 366, 367 modestus, Ancylus, 366 Modiola, 266, 283-293 americanus, 284, 291 arcuatula, 283 demissus, 64, 88, 91, 283-293 fortunei, 266 lacustris, 266 modiolus, 27, 30 plicatula, 283 squamosus, 284, 291 modiolus, Modiolus, 27, 30 Mohnia, 310 mohnia, 310 mohnia, Mohnia, 310 moniliata, Paludina, 352 Monochrysis, 226 lutheri, 226 Monodonta, 300 Monotocardia, 186 morio, Pugilina, 310 morio, Semifusus, 310 morrhuana, Pitar, 22, 26, 27, 29, 39, 40 mortoni, Laevicardium, 22, 24-29, 32, 35, 39, 40, 52, 55, 70, 88, 90 Morula, 307 mucronatus, Asprella, 310 mucronatus, Conus, 310 Mulinia, 26, 30, 52, 56, 81, 82, 88 lateralis, 26, 30, 52, 56, 81, 82, 88 multilineata, Lucina, 47, 52, 55, 68, 69, 88, 90 multilivata, Paludina, 353 Murex, 303, 308, 310, 313, 329 pecten, 310 tenuispina, 310 trunculus, 308 Muricacea, 295, 296, 300, 312, 314, 324, 325, 328, 329 muricata, Colubraria, 327 Muricidae, 299-331 Muricinae, 328 musica, Voluta, 310 Mya, 47, 48, 83, 88, 90 avenaria, 47, 48, 83, 88, 90 Myacidae, 83 Myobarbum, 331 Myriophyllum, 383, 395 Mytilacea, 265 Mytilidae, 63, 276, 283, 291 Mytilopsis, 276 Mytilus, 47, 48, 63-65, 88, 90, 214, 215, 219, 247, 268, 269, 273, 274, 283 demissus, 283 demissus demissus, 284 demissus granosissimus, 284, 286, 290 edulis, 47, 48, 63-65, 88, 90, 247, 268, 269, 273, 284-288 Nacella, 299, 319 nassa, Leucozonia, 314 Nassariidae, 213, 295-331 Nassarius, 13-46, 215, 301, 307, 313, 316, 318 aoteanus, 313 incrassatus, 318 obsoletus, 36, 215, 313 pygmaeus, 318 reticulatus, 301, 313, 318 trivittatus, 13-46 vibex, 24, 30, 39, 40 nasuta, Macoma, 1, 4, 6-8 Natica, 24, 27, 30, 36, 38-40 clausa, 24, 27, 30, 38-40 Nautilina, 364 caldwelli, 364 navalis, Teredo, 85, 86, 88 Navicella, 345, 346 bimaculata, 346 borbonica, 346 borbonica depressa, 346 cookii, 345, 346 depressa, 345 elliptica, 345, 346 eximia, 346 junghuhni, 346 lineata, 346 porcellana, 346 suborbicularis, 345, 346 tessellata, 346 Nematoglossa, 323 Neogastropoda, 295-338 neozelanicum, Scrinium, 305 Nephtys, 21, 38 incisa, 21, 38 Neptunea, 310, 313, 321 antiqua, 310, 313 Neptuniidae, 325 Nereis, 214 Nerineacea, 296 Neripteron, 342 auriculata, 342 Nerita, 340-342, 346 caffra, 342 commersoni, 361 corona bengalensis, 340 knorri, 341 psorica, 361 pulligera, 341 vangiana, 346 Yubella, 341 tuberculata, 361 turrita, 342 viridis, 346 Neritacea, 297, 320 Neritaea, 343 gagates, 343 neritea, Cyclope, 310, 313 Neritidae, 297 Neritilia, 348 consimilis, 348 Neritina, 339-344, 345, 346, 348 auviculata, 342, 344 bengalensis, 340 brevispina, 339 caffra, 342 consimilis, 348 fulgetrum, 342 gagates, 342, 343, 345 knorri, 341 knorrü, 341 longispina, 340 madecassina, 339 pulligera, 341, 343 pulligera knorri, 340 vhyssodes, 340 rubella, 341 souverbiana, 348 spiniperda, 340 407 408 stumpffi, 341 truncata, 341 turrita, 342 viridis, 346 niponicus, Granulifusus, 310 nitida, Parasmittina, 39, 40 Nodularia, 368 geayi, 368 Noetia, 52, 56, 62, 63, 88, 91 ponderosa, 52, 56, 62, 63, 88, 91 norwegicus, Volutopsis, 321 Nucella, 308, 312, 313, 315, 316, 317 lapillus, 308, 313, 315, 316 Nucula, 13-46, 58 annulata, 25 proxima, 13-46, 58, 88 Nuculanidae, 59 Nuculidae, 58 obesa, Florimetis, 1-11 obsoleta, Ilyanassa, 310, 313 obsoletus, Nassarius, 36, 215, 313 obtusa, Retusa, 22, 24, 30, 39, 40 obtusispira, Physa, 364 Ocenebra, 308, 313, 316 erinaceus, 308, 313, 316 Ocenebrinae, 328, 329 Oenopota, 316 travelliana, 316 Oliva, 304, 309, 310, 313, 318, 319 sayana, 309, 310, 313, 318, 319 tehuelchana, 304 Olivacea, 325 olivaceus grasseti, Lanistes, 348, 349 olivaceus grasseti, Meladomus, 349 Olivancillaria, 309, 316, 318, 320 auricularia, 309, 318 Olivella, 307, 308, 310, 313, 318, 319, 330 verreauxü, 310, 313 Olivellinae, 308 Olividae, 299-331 onokeana, Comitas, 305 onokeana vivens, Comitas, 305 Ophioderma, 39, 40 brevispina, 39, 40 Opisthobranchia, 308 Ostreidae, 65 ovalis, Lunarca, 24, 26, 27, 30, 39, 40 ovata ventricosa, Lampsilis, 99 ovoideus, Turbinella, 310 ovum, Ampullaria, 349 ovum grasseti, Lanistes, 347 ovum, Lanistes, 349 ovum, Lanistes plicosus, 348 ovum plicosus, Lanistes, 349 ovum plicosus, Meladomus, 349 ovum striata, Lanistes, 349 Pachylabra, 349, 350 cecillei, 350 hanleyi, 349 largillierti, 349 madagascariensis, 349, 350 simplex, 349 subscutata, 349 pagodum, Columbarium, 310 Paladmetidae, 323 Paludina, 124, 146, 206, 352, 353 biangulata, 356 carinulata, 353 MALACOLOGIA colbeaui, 352 madagascariensis, 353 montliata, 352 multilirata, 353 trabonjiensis, 353 Paludomus, 352, 353 grandidieri, 353 madagascariensis, 352, 353 Pandora, 22, 24, 26, 27, 29, 39, 40 gouldiana, 22, 24, 26, 27, 29, 39, 40 papyria, Amygdalum, 50, 51, 54, 64, 65, 88, 91 Parabathytoma, 305 luhdorffi, 305 Paradmete, 310 typica, 310 Paranerita, 340 longispina, 340 Parapisidium, 372 reticulatum, 372 Parasmittina, 39, 40 nitida, 39, 40 Paratrophon, 310 quoyi quoyi, 310 parkeri, Physa, 379-399 Patella, 146, 148, 345 borbonica, 345 Patellacea, 297 pauliani, Pisidium, 372 paupercula, Strigatella, 319 paxillus, Paxula, 310 Paxula, 310 paxillus, 310 pecten, Murex, 310 Pectinidae, 67 Pectinobranchia, 186 Peculator, 314 hedleyi, 314 Penion, 314, 321 adustus, 314, 321 percarinata, Helisoma anceps, 380 percarinata, Helisoma antrosa, 379-399 Peristernia, 310 australiensis, 310 Perna, 273 Persicula, 310 persicula, 310 persicula, Persicula, 310 persimilis, Aforia goodei, 310 peruviana, Concholepas, 303 Pervicacia, 306 tristis, 306 Pervicaciidae, 325 Petricola, 53, 56, 73, 88, 272 pholadiformis, 53, 56, 73, 88 Petricolidae, 73 pfeifferi, Biomphalaria, 115-122, 368 Phenatoma, 305, 310 rosea, 305, 310 bhenax, Macoma, 88 Philbertina, 305 boothi, 305 leufroyi, 305 purpurea, 305 philippianus, Trophon, 308 philippinarum, Haloginella, 310 philippinavum, Volvarina, 310 Pholadidae, 83 pholadiformis, Petricola, 53, 56, 73, 88 Phos, 303, 327 Photidae, 327 Phyllocoma, 304 Physa, 146, 364, 379-399 gyrina, 380, 395 hildebrandti, 364 integra, 379-399 lamellata, 364 livata, 364 madagascariensis, 364 obtusispiva, 364 parkeri, 379-399 sayi crassa, 380 Physidae, 379 picta, Polystira, 310 Pila, 124, 125, 128, 146, 147, 168, 169, 187-189, 206, 207, 349-351 cecillii, 349-351 globosa, 124, 125, 128, 146, 147, 168, 169, 187-189, 205 virens, 124 Pilidae, 123 pinnulatum, Cerastoderma, 27, 30, 39, 40 Pirena, 356, 357 aspera, 357 debeauxiana, 356, 357 fluminea, 356, 357 gvanulosa, 356 lamarckii, 356 lingulata, 356 madagascariensis, 356, 357 maura, 356 plicata, 356 sinuosa, 356 Spinosa, 356, 357 Pirenella, 361 decollata, 361 Pisidium, 371-373 betafoense, 372 casertanum, 371, 372 edouardi, 371 johnsoni, 371, 372 madagascariensis, 371 pauliani, 372 planatum, 371 reticulatum, 372 Pitar, 22, 26, 21, 29, 39, 40 morrhuana, 22, 26, 27, 29, 39, 40 plana, Crepidula, 24, 26-29, 39, 40 planatum, Pisidium, 371 Planorbidae, 115, 380 Planorbis, 146, 206, 364, 365, 367 alluaudi, 365 apertus, 365 caldwelli, 364 crassilabrum, 364, 365 hildebrandti, 365 madagascariensis, 367 simpliculus, 365 trivialis, 364, 365 plebius, Tagelus, 53, 57, 78, 79, 87, 88, 90 Plesiotriton, 328 cretaceus, 328 plicata, Amblema, 97-113 plicata, Pirena, 356 plicatula, Modiola, 283 plicosus, Lanistes ovum, 349 plicosus, Meladomus ovum, 349 INDEX, VOL. 12 plicosus ovum, Lanistes, 348 Poirieria, 310 zelandica, 310 Polinices, 26, 30, 39, 40 duplicatus, 26, 30, 39, 40 polita, Ampullaria, 124, 147, 186, 188 Polymesoda, 68, 88 caroliniana, 68, 88 polymorpha, Dreissena, 265-281 Polystira, 310 picta, 310 Pomacia, 187, 189 canaliculata, 188, 189 Pomatias, 146, 168, 188 ponderosa, Noetia, 52, 56, 62, 63, 88, 91 Pontiothauma, 305 porcellana, Navicella, 346 Potamides, 361 decollatus, 361 Potamogeton, 383, 385, 395 Prionodontida, 59 prolifera, Microciona, 39, 40 Proneptunea, 310 duplicarinata, 310 Propebela, 320 turricula, 320 Propidiscus, 365 trivialis, 365 Prosobranchia, 146, 169, 206, 297 Protobranchia, 58 Protothaca, 7 proxima, Nucula, 13-46, 58, 88 Pseudanachis, 310 duclosiana, 310 Pseudoliva, 310 crassa, 310 Pseudolivinae, 330 psorica, Nerita, 361 Pteroconchida, 63 Pterygia, 310 crenulata, 310 Pugilina, 310 morio, 310 pulex, Xenostrobus, 269, 276 pullastra, Venerupis, 225-245 pulligera knorri, Clypeolum, 340, 341 pulligera knorri, Neritina, 340 pulligera, Nerita, 341 pulligera, Neritina, 341, 343 Pulmonata, 109, 379 punctulata, Arbacia, 39, 40 purpurea, Philbertina, 305 Purpuridae, 328 Pusia, 310 pygmaeus, Nassarius, 318 Pyrene, 310 gibberula, 310 Pyrenidae, 302-331 Pyrgophysa, 364 bavayi, 364 mariei, 364 pyrum, Turbinella, 319 quoyi quoyi, Paratrophon, 310 Quoyula, 303 Rachiglossa, 295-331 vadiata, Egeria, 4 radiata luteola, Lampsilis, 100 radiata siliquoidea, Lampsilis, 97-113 409 410 MALACOLOGIA Radix, 363, 364 similis, Anachris avara, 13-46 hovarum, 363, 364 simplex, Ampullaria, 349 Rangia, 47, 53, 56, 82, 83, 88, 90 simplex, Anomia, 24, 27, 29, 39, 40, 51, 54, 67, cuneata, 47, 53, 56, 82, 83, 88, 90 68, 88 rangiana, Nerita, 346 simplex, Pachylabra, 349 rangiana, Smaragdia, 348 simpliculus, Planorbis, 365 Rapanidae, 329 simpliculus, Tropidiscus, 365 Rapidae, 329 sinuosa, Pirena, 356 Rapininae, 328, 329 Smaragdia, 346, 348 Ratifusus, 305, 327, 328 rangiana, 348 mestayerae, 305, 327 souverbiana, 348 reticulatus, 305, 327 viridis, 346, 348 recurvum, Ischadium, 283, 284, 285, 289, 291 smithi, Helisoma campanulata, 379-399 recurvus, Brachidontes, 64, 88, 91 smithii, Diplothyra, 84 reticulatum, Parapisidium, 372 Solecurtus, 4 reticulatum, Pisidium, 372 scopula, 4 reticulatus, Nassarius, 301, 313, 318 Solemya, 13-46, 53, 56, 58, 87, 88 reticulatus, Ratifusus, 305, 327 velum, 13-46, 53, 56, 58, 87, 88 Retusa, 22, 24, 30, 39, 40 Solemyidae, 58 obtusa, 22, 24, 30, 39, 40 Solen, 53, 56, 80, 87 rhyssodes, Clithon, 340 viridus, 53, 56, 80, 87 rhyssodes, Neritina, 340 Solenidae, 79 rigida, Atrina, 291 solidissima, Spisula, 27, 30, 47, 48, 53, 57, 80, Rissoacea, 320 81, 88-91, 251, 256, 257 rosea, Phenatoma, 305, 310 souverbiana, Neritina, 348 rubella, Nerita, 341 souverbiana, Smaragdia, 348 rubella, Neritina, 341 sowerbyi, Colubraria, 327 rubiginosa, Austromitra, 309 Speightiidae, 325 Rupia, 48, 90 Sphaerium, 372, 373 Sabellaria, 214, 215, 219 capense, 373 Sanguinolariidae, 78 ferruginea, 373 sayana, Oliva, 309, 310, 313, 318, 319 madagascariense, 373 sayi crassa, Physa, 380 spiniperda, Clithon, 340, 341 Scabricola, 310 spiniperda, Neritina, 340 desetangsii, 310 spinosa, Melanatria, 356, 357 variegata, 310 spinosa, Melanopsis, 356 Scaphella, 310 Spinosa, Pirena, 356, 357 junonia, 310 spiralis, Coluzea, 329 Schistosoma, 115, 119 Spisula, 27, 30, 47, 48, 53, 57, 80, 81, 88-91, mansoni, 115, 119 251, 256, 257 Scissurellidae, 301 solidissima, 27, 30, 47, 48, 53, 57, 80, 81, scopula, Solecurtus, 4 88-91, 251, 256, 257 Scrinium, 305 Splendrillia, 305 neozelanicum, 305 debilis, 305 Scrobicularia, 6 squamata, Amphipholis, 39, 40 secta, Macoma, 6-8 squamosus, Modiola, 284, 291 securis, Xenostrobus, 267, 276 Stagnicola, 379-399 Segmentina, 365 emarginata angulata, 379-399 angusta, 365 Stenoglossa, 295, 322, 323 chevalieri, 365 striata, Iredalula, 310, 327 Segmentorbis, 365, 367 striata, Lanistes ovum, 349 angustus, 365, 367 Striatella, 361 Seila, 27, 30, 39, 40 tuberculata, 361 adamsi, 27, 30, 39, 40 striatula, Venus, 225-245 Semelidae, 77 striatus, Lanistes, 349 Semifusus, 310 Strigatella, 307, 319 morio, 310 paupercula, 319 septangularis, Haedropleura, 319 Strombina, 310 Septaria, 297, 345-347 gibberula, 310 borbonica, 345-347 stumpffi, Neritina, 341 borboniciensis, 346 suborbicularis, Elava, 346 lineata, 346, 347 suborbicularis, Navicella, 345, 346 suborbicularis, 346 suborbicularis, Septaria, 346 tessellata, 346 subscutata, Ampullaria, 349 Septifer, 275 subscutata, Pachylabra, 349 siamensis, Dreissena, 266 subulata, Cerithiopsis, 27, 30, 39, 40 sikorae, Corbicula, 371 Subulitacea, 296, 301 siliquoidea, Lampsilis radiata, 97-113 sudanica tanganyicensis, Biomphalaria, 115-122 INDEX, VOL. 12 411 Tagelus, 1-11, 27, 30, 53, 57, 78, 79, 87, 88, 90 byrum, 319 californianus, 1-11 Turbinellidae, 299-331 divisus, 27, 30, 79 Turbinellinae, 326, 328 plebius, 53, 57, 78, 79, 87, 88, 90 turbinellum, Vasum, 316 tanganyicensis, Biomphalaria sudanica, 115-122 turricula, Lora, 320 Taron, 307, 314, 318 turricula, Propebela, 320 dubius, 314, 318 Turriculinae, 305 tehuelchana, Oliva, 304 Turridae, 300-331 Tellina, 6, 53, 57, 74, 88, 90 Turrinae, 305 agilis, 53, 57, 74, 88, 90 turrita, Nerita, 342 Tellinacea, 1 turrita, Neritina, 342 tenta, Macoma, 13-46, 77, 88, 90 turrita, Vittina, 342 tenuispina, Murex, 310 Typhinae, 328 Terebra, 305 typica, Paradmete, 310 cancellata, 305 umbilicata, Drillia, 310 maculata, 306 undatum, Buccinum, 309, 310, 313 Terebridae, 299-331 unicolor, Cyclostoma, 356 Teredinidae, 85 unicolor, Viviparus, 356, 357 Teredo, 85, 86, 88 Unio, 368 navalis, 85, 86, 88 geayi, 368 tessellata, Navicella, 346 madagascariensis, 368 tessellata, Septaria, 346 malgachensis, 368 Thaididae, 328, 329 Unionidae, 97 Thaidinae, 328, 329 urceus, Ampullaria, 187, 189 Thais, 258, 259, 321 Urosalpinx, 26, 27, 29, 39, 40, 247-263 lapillus, 258, 259 cinerea, 26, 27, 29, 39, 40, 247-263 Theodoxus, 297 cinerea follyensis, 247-249, 253, 256, 257, 259 Thiara, 359, 360 Uttleya, 304 amarula, 359, 360 Vallisneria, 383 thiarella, Melania, 358 variabilis, Donax, 47, 52, 55, 77, 78, 88-90 Thuiaria, 51 variegata, Scabricola, 310 argentea, 51 Vasidae, 326, 328 Tolema, 303 Vasinae, 326, 328 Tonnacea, 296, 297, 327 Vasum, 310, 315, 316, 328 Toxoglossa, 295, 322, 323, 325 ceramicum, 310 trabonjiensis, Paludina, 353 turbinellum, 316 translivata, Anachris, 36, 37 velum, Solemya, 13-46, 53, 56, 58, 87, 88 transversa, Anadara, 13-46, 51, 54, 59, 60, 62, Venericardia, 47, 68 88, 91 tridentata, 47, 68 travelliana, Lora, 316 Veneridae, 70, 225-245 travelliana, Oenopota, 316 Venerupis, 225-245 Treses, 7 aurea, 225-245 tridentata, Venericardia, 47, 68 pullastra, 225-245 Triphoridae, 300 ventricosa, Lampsilis ovata, 99 triseriata, Lunatia, 27, 30 Venus, 225-245 tristis, Pervicacia, 306 fasciata, 225-245 trivialis, Planorbis, 364, 365 striatula, 225-245 trivialis, Propidiscus, 365 verrucosa, 225-245 trivialis, Tropidiscus, 365 verreauxii, Olivella, 310-313 trivittatus, Nassarius, 13-46 verrucosa, Venus, 225-245 Trochidae, 297, 301 Vexilla, 308, 310, 319, 320 Trophon, 308 taeniata, 310 philippianus, 308 Vexillidae, 299-331 Trophoninae, 309, 320, 328 vibex, Nassarius, 24, 30, 39, 40 Tropidiscus, 365 virens, Pila, 124 alluaudi, 365 virginica, Crassostrea, 48, 65, 66, 88, 247-249 simpliculus, 365 viridis, Nerita, 346 trivialis, 365 viridis, Neritina, 346 truncata, Barnea, 51, 54, 83, 84, 88, 90, 91 viridis, Smaragdia, 346, 348 truncata, Neritina, 341 vividus, Solen, 53, 56, 80, 87 trunculus, Murex, 308 Vittina, 342, 343 tuberculata, Melania, 361 gagates, 342, 343 tuberculata, Nerita, 361 turrita, 342 tuberculata, Striatella, 361 Vitularia, 306 tuberculatus, Melanoides, 361 vivens, Comitas onokeana, 305 Tubifex, 109 Viviparus, 124, 146, 356, 357 Turbinella, 305, 310, 319, 321, 328 unicolor, 356, 357 ovoideus, 310 Volemidae, 327 412 MALACOLOGIA Volsella, 266 fortunei, 266 Voluta, 310 musica, 310 Volutacea, 295, 296, 303, 325, 330 Volutidae, 299-331 Volutocorbis, 309, 310, 316 abyssicola, 309, 310 Volutomitridae, 295-331 Volutomitrinae, 330 Volutopsis, 321 norwegicus, 321 Volvarina, 310 philippinarum, 310 watsoni, Biomphalaria alexandrina, 115-122 Xancidae, 328 Xenostrobus, 267, 269, 276 inconstans, 269, 276 pulex, 269, 276 securis, 267, 276 Xymene, 310 ambiguus, 310 Yoldia, 13-47, 59, 88 limatula, 13-47, 59, 88 Zairia, 368 geayi, 368 zelandica, Poirieria, 310 Zeugobranchia, 297 Zostera, 48, 58, 90 marina, 58, 90 Vol. 12, No. 2 # CONTENTS E. S. DEMIAN and F. YOUSIF Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). 2 Ш. Development of the circulatory and renal systems. ..... e SUR E. S. DEMIAN and F. YOUSIF Embryonic development and organogenesis in the snail Marisa cornuarietis (Mesogastropoda: Ampullariidae). IV. Development of the shell gland, mantle and respiratory OrganS ....... A A A cate bo .. J. ‚N. CATHER Regulation of apical cilia development by the polar lobe of imnanassa (Gastropoda,-Nassarüdae)... ору о eee M. L. M. LE PENNEC М. В. CARRIKER and H. H. CHAUNCEY Effect of carbonic anhydrase inhibition on shell penetration fy a by the muricid gastropod Urosalpinx cinerea ...... 1 1040 da 24 ds B. MORTON Some aspects of the biology and functional morphology of the organs of feeding and digestion of Limnoperna fortune = (Dunker) (Bivalvia: Mytllacea); Save ue ala he siete fe AL AA S. K. PIERCE ' 2 The rectum of “Modiolus” demissus (Dillwyn) (Bivalvia: Mytilidae): A clue to solving a troubled taxonomy..... Fisk oes JE 7) М. Е. PONDER Е tr 4 The origin and evolution of the Neogastropoda ............. aire “A E. FISCHER-PIETTE and D. VUKADINOVIC Sur les mollusques fluviatiles de Madagascar....... N o ó AE CLAMPITT | ¿ Substratum as a factor in the distribution of pulmonate AN snails in Douglas Lake, Michigan. .... wa tae TR a sale tee due) US 3 Published at the Museum of Zoology, The University of Michigan, Ann Arbor, п. HAUT Michigan 48104, U.S. A. , by the Institute of Malacology y by à à». ae a e DE $ "4 É ; ñ | ; À TAN 4 CEA Ke mee’ y ‘ ‘ x A AE" nr $ hoes 4 1472. 1 PO vet pS A BOUND SEP 1974 EN 4 072 160 369 E q A nn en 5 a nn nn Een ^ =k Sa nee tone ee eS de men da re wen nn er > ¡ATA ту LR he 0 ann ego лы > » .. x > SSA A ru dr et a > net Poem. ee « rer ern ve SA EEE HEN EEE ee tte ES Oe DRE tae et аня ten wer A do