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VOL. 38, NO. 1-2 1996
MALACOLOGIA
International Journal of Malacolog y Revista Internacional de Malacologia Journal International de Malacologie Международный Журнал Малакологии
Internationale Malakologische Zeitschrift
Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol. Vol.
Publication dates
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19 Jan.
28 Jun. 16 Dec.
1 Aug. 29 Dec.
28 May
30 Nov. 7 Jun. 6 Sep. 9 Sep.
14 Jul.
2 Dec.
8 Jan. 13 Nov 8 Mar
1988 1988 1988 1989 1989 1990 1990 1991 1991 1992 1993 1993 1995 . 1995 . 1996
VOL. 38, NO. 1-2 MALACOLOGIA
CONTENTS
FADWA A. ATTIGA & HAMEED A. AL-HAJJ
Ultrastructural Study of Euspermiogenesis in Clypeomorus Bifasciata and Clypeo-
morus Tuberculatus (Prosobranchia: Cerithiidae) With Emphasis on Acrosome
Éoimationme ee ооо оо оо осо асов особо ove creer RÜDIGER BIELER & RICHARD Е. PETIT
Additional Notes on Nomina First Introduced by Tetsuaki Kira in “Coloured Illustra-
tions of the: ShellSiOf Japan? se soccer ee ce вое о еее M. E. CHASE & R. C. BAILEY
Recruitment of Dreissena Polymorpha: Does the Presence and Density of Conspe-
cifics Determine the Recruitment Density and Pattern in a Population? ........... KENNETH C. EMBERTON
Microsculptures of Convergent and Divergent Polygyrid Land-Snail Shells ........ KENNETH C. EMBERTON, TIMOTHY A. PEARCE & ROGER RANDALANA
Quantitatively Sampling Land-Snail Species Richness in Madagascan Rainforests . MARIA FERNANDA LOPEZ ARMENGOL
Taxonomic Revision of Potamolithus Agapetus Pilsbry, 1911, and Potamolithus
Buschii (Frauenfeld, 1865) (Gastropoda: Hydrobiidae) .......................... MARTIN HAASE & ERHARD WAWRA
The Genital System of Acochlidium fijiense (Opisthobranchia: Acochlidioidea) and its
Inferred\EUNCtiOn Re den Me ire mer ser coca error ve WALTER R. HOEH & MARK E. GORDON
Criteria for the Determination of Taxonomic Boundaries in Freshwater Unionoids
(Bivalvia: Unionoida): Comments on Stiven and Alderman (1992) ................ С. M. KUCHENMEISTER, D. J. PRIOR & I. G. WELSFORD
Quantification of the Development of the Cephalic Sac and Podocyst in the Terres-
tral@astropodilimax Maximus Eos oa во ea an as RICHARD E. PETIT & RÜDIGER BIELER
On The New Names Introduced in the Various Printings of ‘‘Shells of the World in
Colour” [Vol. | by Tadashige Habe and Kiyoshi Ito; Vol. Il by Tadashige Habe and
Sadao: Kosudel za. 0m mais alcala soc dos ea aaa ae en DR. F. D. POR & DR. R. M. POLYMENI
A Call for a New International Congress of Zoology ............................ PETER D. ROOPNARINE
Systematics, Biogeography and Extinction of Chionine Bivalves (Bivalvia: Veneridae)
in Tropical America: Early Oligocene-Recent .................................. LUIZ RICARDO L. SIMONE
Anatomy and Systematics of Buccinanops Gradatus (Deshayes, 1844) and Bucci-
nanops Moniliferus (Kiener, 1834) (Neogastropoda, Muricoidea) From the Southeast-
enn Coast of Brazilian dite oasis iO buste CHRISTINA M. SPOLSKY, GEORGE M. DAVIS & ZHANG YI
Sequencing Methodology and Phylogenetic Analysis: Cytochrome b Gene Sequence
Reveals Significant Diversity in Chinese Populations of Oncomelania (Gastropoda:
POMATOPSIAAE) ола ев ea P. TATTERSFIELD
Local Patterns of Land Snail Diversity in a Kenyan Rain Forest .................. LAURA R. WHITE, BRUCE A. MCPHERON, & JAY R. STAUFFER, JR.
Molecular Genetic Identification Tools for the Unionids of French Creek, Pennsylva-
A ie O E OO SO DAZHONG XU & MICHELE G. WHEATLY
CA Regulation in the Freshwater Bivalve Anodonta Imbecilis: |. Effect of Environmen-
tal CA Concentration and Body Mass on Unidirectional and Net CA Fluxes ......
1996
47
33
143
223
153
35
229
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87
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161
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59
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Copyright © 1996 by the Institute of Malacology
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1996 EDITORIAL BOARD
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W. L. PARAENSE
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J. J. PARODIZ Carnegie Museum Pittsburgh, U.S.A.
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D. G. REID The Natural History Museum London, United Kingdom
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MALACOLOGIA, 1996, 38(1-2): 1-17
TAXONOMIC REVISION OF POTAMOLITHUS AGAPETUS PILSBRY, 1911, AND POTAMOLITHUS BUSCHII (FRAUENFELD, 1865) (GASTROPODA: HYDROBIIDAE)
María Fernanda López Armengol
Instituto de Embriología, Biología e Histología, Facultad de Ciencias Médicas-CONICET,
Universidad Nacional de La Plata, Calle 60 y 120 (1900), La Plata, Argentina
ABSTRACT
Potamolithus agapetus Pilsbry, 1911, and P. buschii (Frauenfeld, 1865) are related species that live sympatrically in Río de la Plata.
Studies carried out on populations of both species from Río de la Plata show that P. agapetus presents a marked secondary sexual dimorphism on shell shape and size.
The female shell is bigger than male shell, and its body whorl shape is subglobose, with a rounded angle at the basal periphery and another angle a short distance below the suture. The male body whorl shape is usually rounded without keels and seldom with a round angle at the basal periphery.
Females of P. agapetus are very similar to the shell of P. buschii, which lacks secondary sexual dimorphism. For that reason, P. agapetus females were excluded from the original description by Pilsbry (1911), and seemingly included in subsequent enlarged descriptions of Р. buschii.
Both species share the same body whorl shape, but both present different degrees between angulose to globular shapes. They can be distinguished by shell color pattern, columella width, body whorl sculpture, head pigment pattern, eyebrow position, nuchal node size in females, gill filament number and range, and in the shape and number of cusps on the central and lateral
radular teeth.
Key words: Potamolithus, Hydrobiidae, taxonomy, sexual dimorphism.
INTRODUCTION
The genus Potamolithus comprises small (up to 7 mm long), thick-shelled gastropods that inhabit rivers and streams (Pilsbry, 1911; López Armengol, 1985).
This genus, exclusively South American and endemic in Ribeira, Itajai-agu and Jacuhy rivers in southern Brazil and Uruguay River, part ofthe Paraná and Río de la Plata drainage systems (López Armengol, 1985).
Controversial aspects of authorship and type species (ICZN Case 2801; López Armen- gol & Manceñido, 1992; Kabat, 1993; Kabat & Hershler, 1993; Manceñido 8 López Armen- gol, 1993) have been cleared up by ICZN ac- tion (ICZN Opinion 1779, 1994) fixing Pilsbry & Rush as the authors of this genus and Pot- amolithus lapidum (d'Orbigny, 1835) as its type species.
In 1911, Pilsbry presented a key to species and subspecies and a description of the known species which were arranged in four groups. Parodiz (1965) gave a description of Potamolithus species and added new char- acters and geographical data. Davis & Pons da Silva (1984) described the anatomy of P.
ribeirensis from Feitoría River, Brazil, and dis- cussed phylogenetic relationships and con- vergence with other hydrobiid and pomatiop- sid genera.
The descriptions of Potamolithus species were based on shell features, and only a few specimens were studied in some cases.
Potamolithus agapetus Pilsbry, 1911, and Potamolithus buschii (Frauenfeld, 1865) are sympatric in Río de la Plata (Pilsbry, 1911; López Armengol, 1985). According to Pilsbry (1911) both species belong to the ‘group of P. buschii”” because they share the same gen- eral shell shape: both equally wide and high with a normal length spire, a simple lip, and a flattened columella. Juveniles of P. buschii are not always readily distinguishable from imma- ture P. agapetus. Potamolithus agapetus was originally described as the smallest Potamo- lithus known and has a globular-conic shell. On the other hand, P. buschii was originally described as having a wide and carinate shell.
Studies carried out on populations of both species from Rio de la Plata show that spec- imens with a shell morphology agreeing with the original description of P. agapetus are all males. On the other hand, a great variability
2 LÓPEZ ARMENGOL
FIG. 1. Scanning electron micrographs of the shell of P. agapetus. A, B, males; C, D, females. Body whorl periphery: A, globose, and C, angular. F, lateral view: note the concave body whorl base. G, enlargement of the shell showing the surface faintly marked with growth-lines and some pits. Scale bar A-E = 1 mm; F
= 50. Lim.
TWO RELATED SPECIES OF POTAMOLITHUS 3
B
==
FIG. 2. Variation in the shape of the shell in P. agapetus. A, females. B, males. Scale bar = 1 mm.
TABLE 1. Whorl number of P. agapetus. Frequency of males and females at each whorl stage present at the localities studied. % = percentage of population.
Anchorena beach
Whorls d Q % g eroded 7 15 3.12 2 2.50 — = — — 3.00 12 1 2.19 5 325 104 ПИ 20.44 7 3:50, 42 68 18.58 1 3375: 7 221 38.51 2 4.00 — 86 14.53 2 4.25 — 12 2.03 ee N = 172 420 19
was observed in P. buschii in such charac- ters as radula, head pigmentation, number of gill filaments, and the size of the female nuchal node.
The aim of this work is to redescribe both P. agapetus and P. buschii.
MATERIALS AND METHODS
Localities studied were: Rio de la Plata, Anchorena beach, Argentina (34°29’S, 58°28’W), col.: López Armengol, 30-IV-1984, Colección Malacológica del Museo de La Plata, MLP 4652; mouth of Rio San Juan where it empties into Rio de la Plata, Uruguay (33°17’S, 57°58’W), col.: Perez Duhalde, 15- VII-1989, МЕР 4986; Rio de la Plata, Isla San Gabriel, Uruguay (34°29’S, 57°52’W),col.: Ló-
Rio San Juan
Isla San Gabriel’s
? % 3 ? % 12 18.92 2 2 4.12 — — a 1 9.19 => 6.76 18 7 25.77 = 9.46 19 1 20.62
1 2.70 й 6 13.40 qt WOW 2 20 22.68 29 41.89 — 8 8.25 2 2:10 — = — 95 92 45
pez Armengol-Casciotta, 17-11-1985, МЕР 4655.
The samples were taken randomly and in- clude all individuals of all size classes at a single site in the river. The sample for the number of individuals and their sex for each whorl number consisted of 592 specimens of P. agapetus and 289 specimens of P. buschii. These samples were drawn from an initial population of 3,404 individuals (MLP 4652).
Specimens were measured by ocular mi- crometer in a Wild M-5 stereoscopic micro- scope. All specimens studied were unpara- sitized. Measurements are those of Hershler 8 Landye (1988). The following ratios were formed using some of this data: shell length/ body whorl length; body whorl length/shell width; shell length/shell width and aperture length/shell length.
TABLE 2. Shell measurements (m to 3.75 whorls of P. agapetus (MLP 4652).
LÓPEZ ARMENGOL
significant difference between sexes, P< .001.
Characters Shell length
Body whorl length
Spire length
Shell width
Aperture length
Aperture width
Columella width
Umbilical area width
Shell length/body whorl length Body whorl length/shell width Shell length/shell width
Aperture length/shell length
m) and ratios for 29 males and 44 females of 3.50 X + standard deviation (range). * =
Number of whorls was counted according to Emberton (1985), but 0.25, 0.5 and 0.75 were the fractions considered. Body whorl and penultimate whorl convexity were calcu- lated following Hershler 8 Landye (1988). Whorl convexity value is directly proportional to whorl convexity.
Shells and radulae were studied and pho- tographed using scanning electron micro- scope (Jeol JSM-T 100). Heads were dried by the critical point method.
The position and distance between the base of penis or nuchal node with respect to the lobes of the eyes and the angle of the base of penis or nuchal node with respect to the mid-line of the neck were calculated on fixed material, following Davis et al. (1986).
Statistical analyses were limited to calcu- lating the means, standard deviations, and standard 't' test for sexual dimorphism in shell measurements and ratios and gill fila- ment number. The significance level ac- cepted was Р < .001. Xi? was performed to evaluate sex ratio = 1:1.
males females SD P < .001 2.32 + 0:25 2.88 + 0.26 5 (1.95 — 3.09) (2.27 — 3.24)
2.08 + 0.24 2.56 + 0.24 5 (1.76 2.77) (1.95 — 2.96)
0.25 + 0.04 0.32 + 0.05 = (0.15 = 0:32) (0.19 — 0.44)
2.28 + 0.26 2:81 ==10.27 . (1.95 — 3.09) (220321)
1.74 + 0.22 2.17 + 0.20 2 (1.45 — 2.39) (1.76 — 2.52)
1.22 + 0.16 510.15 * (ОТ = 1.76) (1.20 — 1.83)
0.24 + 0.04 0.30 + 0.06 És (0.16 — 0.32) (0.19 — 0.44)
0.18 + 0.07 0.22 + 0.08
(0.06 — 0.38) (0.06 — 0.38)
1.12+0.02 1.18 0:02
(1.08 — 1.18) (1.08 — 1.17)
0.91 + 0.03 0.91 + 0.04
(0.84 — 0.99) (0.83 — 0.98)
1.02 + 0.02 1.02 + 0.04
(0.92 — 1.09) (0.96 — 1.07)
0.73 + 0.04 0.75 + 0.04
(0.63 — 0.80) (0.63 — 0.83)
RESULTS
Potamolithus agapetus Pilsbry 1911
Potamolithus agapetus Pilsbry 1911: 578, pl. 40, fig. 10, 10a. Potamolithus agapetus Parodiz 1965: 9
Type material: Academy of Natural Sciences of Philadelphia 69,683.
Type locality: Río de la Plata, at Isla San Gabriel, near Colonia, Colonia Department, Uruguay.
Description
The shell is globose-conic to subglobose (Figs. 1, 2) and solid but not thick. The color is uniform light brown. The surface is rather smooth, faintly marked with growth lines (Fig. 1F). The spire is 11% of the shell length. The number of whorls is most frequently between 3.00 and 4.00 (Table 1), slightly convex (penultimate whorl convexity = 0.20 and body whorl convexity = 0.14) in outline. The
TWO RELATED SPECIES OF POTAMOLITHUS 5
A 475 A A 450 475 AAAA 5 400 А AAAAAA 2 3 © 375 e o. . 0 oAAAAAA, АА © о 5 => o o Фо} оо} 1 { ora A 3.25 e bobrcoojtos A 300 20 3.0 4.0 50 Shell length (mm) B 425 A a is = 700 A 3444444444444 2 3 5 ars POVNET TE NN ET TEEN © pe] Е 2 350
325
Shell length (mm)
FIG. 3. Scatter-diagram for the number of whorls and shell length. A, P. agapetus (82 males and 61 females). B, P. buschii (128 males and 108 females). Note the sexual dimorphism in shell size in P. agapetus. Males (black circles), females (black triangles). One symbol may represents more than one specimen.
6 LÓPEZ ARMENGOL
FIG. 4. Pigment patterns of P. agapetus. A, head-neck, dorsal view. B, penis, right side. Scale bar = 1 mm.
body whorl base is concave in dorsal view (Fig. 1E). The aperture is oblique, inclined about 35° to 42° (X = 39°) towards the coiling axis, rounded-ovate, and angular at the top. The columella is wide and flattened (Fig. 1B, D). Shells with discontinous peristome have a thin outer lip, and the umbilical area can be present or absent. When it present, is narrow and bounded by an angle. In shells with con- tinous peristome (Fig. 1B, D), the inner lip is heavily calloused and the outer lip is simple and thin. There is a rather conspicuous um- bilical area bounded by an angle or an acute ridge. Some specimens have an umbilical opening.
There is sexual dimorphism in shape and shell size. The shape of the body whorl in males is usually globose (Figs. 1A, 2B). How- ever, some males have a shell with a rounded angle below the suture or with two angles, one below the suture and the other at the basal periphery (Fig. 2B). Males have a rounded outer lip (Fig. 1B). The female body whorl shape is usually subglobose, with two rounded angles, one below the suture and the other at the basal periphery (Figs. 1C, 2A); the outer lip is sharp (Fig. 1D).
The females are larger than males with the same number of whorls (Fig. 3A). No sexual dimorphism in umbilical area width and cal- culated ratios were observed. Statistics on shell dimensions for males and females of
3.50 to 3.75 number of whorls are given in Table 2.
There was no significant difference in num- ber of males and females at Anchorena Beach (0.76:1).
The head can be unpigmented or with a band of melanin in the snout, or with two V-shaped bands orientated with the vertex pointing from the snout to the neck. Another band runs dorsally in the middle of each ten- tacle. There is a concentration of white spheric granules above and around the eyes (“eyebrows””) (Fig. 4A), and eye lobes are slight swellings at the base of each tentacle.
The neck of females bears a protuberance called nuchal node (Davis & Pons da Silva, 1984). The position of the nuchal node base is mainly to the right of the mid-line of the head. The nuchal node is X = 0.25 mm + 0.02 (0.24-0.30) high (Fig. 5A, B). The distance be- tween the base of the nuchal node and the eyes is X = 0.31 mm + 0.09 (0.15-0.4). The angle of the base of the nuchal node (with respect to the mid-line of the neck) is X = 52° (34°-72°).
The penis is simple, without appendages; with a black spot at the distal end (Figs. 4B, 5C). The distance between the base of the penis and the lobes of the eyes is X = 0.14 mm + 0.01 (0.12-0.15). The angle of the base of the penis (with respect to the mid-line of the neck) is X = 23° (14°-30°).
There are 19 to 28 gill filaments (Fig. 6),
TWO RELATED SPECIES OF POTAMOLITHUS 7
FIG. 5. Scanning electron micrographs of the head-neck of P. agapetus. A, dorsal view of female head-neck, showing the nuchal node. B, right side of the head-neck of a female. C, left side of the head-neck and fully erect penis of a male. Scale bar = 200 um.
with no indication of sexual dimorphism in- their number (X = 23.00 + 2.30 and 23.87 + 2.64 for males and females respectively). Radula typically taenioglossate (Fig. 7), the statistics and cusp formulae given in Table 3. Distinctive features are: the concave hollow in the middle of the anterior cusp of the cen- tral teeth (Fig. 7C); the external edge of lateral angle of the central teeth is sometimes curved; the innermost pair of basal cusps
arise from the face of the tooth; there is a concave hollow between the basal cusps and basal process, and the basal process is prominent.
There were no differences among the blades of the lateral tooth (Fig. 7A, B, D, E). There is a pronounced posterior projection on the face of the lateral tooth (Fig. 7D).
Potamolithus buschii (Frauenfeld, 1865)
Lithoglyphus Buschii Frauenfeld, 1865, ex Dunker, in litt.: 530, pl. 11
Potamolithus buschii, Pilsbry & Rush 1896: 80
Potamolithus buschii, Pilsbry, 1896: 88
Potamolithus buschii, Pilsbry, 1911: 580, pl. 40, figs. 11-14, pl. 41b, fig. 2
Potamolithus buschii, Parodiz, 1965: 28, figs. 63-72
Type material: Naturhistorisches Museum, Vienna, Austria.
Type locality: ‘“Erst kürzlich von Buenos-Ay- res [sic. Colonia Department, Uruguay] er- halten. Wird gefunden an der Mündung des St. Juan in den La Plata.”
Description
The shell is imperforate, solid, subglobose to globose in shape (Figs. 8-10). The shell is green, with irregular buff zigzag streaks (Fig. 11); some specimens (27% at Anchorena beach) have a dusky-brown band located su- tural and peripheral on the body whorl (Fig. 11). The surface is smooth, although marked with growth-lines (Fig. 8F). The spire length is variable, between 9.60% and 15% of the shell length. The number of whorls is most frequently between 3.75 and 4.00 (Table 4), convex (penultimate whorl convexity = 0.17 and body whorl convexity = 0.21) inoutline. The body whorl can be carinate,strongly an- gular, with a rounded angle, or globose at the basal periphery (Figs. 8A-D, 10). The body whorl is convex above the basal periphery, usually having a low keel or rounded angle at the back and a short distance below the su- ture (Fig. 9A-C). There is also, sometimes, a second spiral ridge below the upper one and a concavity between both called sulcus (Fig. 9D). The base is flattened in dorsal view (Fig. 9A-C). The aperture is oblique, inclined about
8 LÓPEZ ARMENGOL
P agapetus М= 20
Number of individuals
19 20 21 22° 23 24 25 26
27 28 29 Number of gill filaments
P buschii N=18
30, 31 32 33 3403536
FIG. 6. Gill filament number in P. agapetus and Р. buschii. Scatter-diagram between number of gill filaments
and number of individuals.
40° to 54° (X = 46°53’) towards the axis of coiling; basally rounded and angular at the top. Columella narrow and flattened or con- vex (Fig. 8E).
In shells with a discontinous peristome, the outer lip is thin and may or may not have an umbilical area. When the umbilical area is present, it is narrow and bounded by an an- gle. In shells with a continous peristome, the inner lip is heavily calloused and the outer lip is thick (Fig. 8E). Sometimes the peristome is edged with a black line. There is a well-de- veloped concave umbilical area bounded by an angle or an acute ridge. Some specimens have an umbilical opening.
Statistics on shell dimensions for males and females of 3.50 to 3.75 whorls are given in Table 5. No sexual dimorphism in shell size was evident; females and males at the same number of whorls have the same size (Fig. 3B).
There was no significant difference in the number of males and females at Anchorena Beach (0.90:1).
The entire head is black (melanin), and there is a black band in the middle of each tentacle. Next to the eyes there is a hyaline
band with white spheric granules on it (Fig. 12А).
Тре nuchal node is located to the right of the mid-line and is 0.06 mm high (Fig. 13A, B). The distance between the base of nuchal node and the lobes of the eyes is X = 1.01 mm + 0.24 (0.63-1.26). The angle of the base of nuchal node (with respect to the mid-line of the neck) is x = 48° (27°-69°).
The penis is simple, without appendages (Fig. 13C). The penis bears two parallel bands of melanin running on both sides, one dorsal along the distal part and the other ven- tral (Fig. 12B). The distance between the base of penis and the lobes of the eyes is X = 0.59 mm +0.08 (0.45-0.75). The angle of the base of the penis (with respect to the mid-line of the neck) is X = 32° (20-457).
There are 28 to 36 gill filaments (Fig. 6), with no indication of sexual dimorphism in their number (X = 30.14 + 1.57 and 32.45 + 1.69 for males and females respectively).
Radula tipically taenioglossate (Fig. 14). The statistics and cusps formulae given in Table 3. Distinctive features are: that the mid- dle of the anterior cusps of the central tooth is flat; the external edge of lateral angle is
TWO RELATED SPECIES OF POTAMOLITHUS 9
CPE
FIG. 7. Radula of P. agapetus. A, Section of radular ribbon excluding left outer marginals. B, enlargement of central and right lateral teeth. C, central tooth. D, central and left lateral teeth. E, left lateral and marginal teeth. F, right inner and outer marginal teeth. Scale bar A = 50 um; B-F = 10 um.
TABLE 3. Formulae for the most common cusps arrangements for the four radular teeth of P. agapetus and P. buschii.
Tooth N Formula (%) P. agapetus (4 radulae) Central 29 6-1-6 6-1-5 5=1-6 (79.30), (17.24), (3.45) 3-3 3-3 3—3 Lateral 38 4—1—5 (44.74); 5- 1-4 (31.58); 5- 1-5 (23.68) Inner marginal 35 1822 Outer marginal 21 17—23 Р. buschii (2 radulae) Central 51 4-1-4 4-1-4 4-1-5 (33.30); (33.30); (33.30) 2—2 2=3 222 Lateral 46 3—1-3 (80.43); 4-1—3 (10.87); 2-1-2 (8.70) Inner marginal 31 9—11
Outer marginal 24 1215
10 LÓPEZ ARMENGOL
FIG. 8. Scanning electron micrographs of the shell of P. buschii. A-D, frontal view. Body whorl: A, carinated; B, strongly angular; C, rounded angle; D, globose. E, umbilical view. F, enlargement of the shell showing the surface marked with growth-lines and some pits. Scale bar A-E = 1 mm, F=50' um:
TWO RELATED SPECIES OF POTAMOLITHUS 11
FIG. 9. Scanning electron micrographs of the shell of P. buschii. A-C, dorsal view. Note the flat body whorl base and the different degrees of subsutural carination: A, carinated; B, angular; C, globose. D, lateral view: note the sulcus between two ridges. Scale bar = 1 mm.
straight, and the innermost pair of basal cusps arise from the face of the tooth (Fig. 14C). The ventral part of basal cusps is a little concave and the basal process is not prom- inent. The central blade of lateral teeth wid- ened with respect to the other cusps (Fig. 14A, B, D).
DISCUSSION AND CONCLUSIONS
Potamolithus agapetus shows marked secondary sexual dimorphism in shell shape
and size. The shape of the body whorl in males is usually rounded, whereas the female is subglobose, with a rounded angle at short distance below the suture and another angle at the basal periphery. Like other gastropods showing sexual dimorphism, the female shell is larger than the male shell.
Potamolithus agapetus was described by Pilsbry (1911) as the smallest Potamolithus known, with body whorl evenly rounded, without keels or angles but his description did not include subglobose shells. Two
LÓPEZ ARMENGOL
232883 BABA
FIG. 10. Variation in the shape of the shell in P. buschii. Scale bar = 1 mm.
rounded angles are usually present in fe- males.
Potamolithus buschii was described by Frauenfeld (1865) as having a wide, carinate shell, but in subsequent descriptions by Pil-
4mm
FIG. 11. Shell of P. buschii, showing the peripheral band and irregular buff zigzag streaks.
bry (1911) and Parodiz (1965) the concept of this species changed. Pilsbry (1911) included the least angular forms of P. buschii from Isla San Gabriel (type locality of P. agapetus) and Parodiz (1965) stated that carinated shells were not the common form of the species.
Because P. agapetus and P. buschii are related species and sympatric in Rio de la Plata, it is probable that P. agapetus females have been included in the descriptions of P. buschii by Pilsbry (1911) and Parodiz (1965). For example, Pilsbry (1911) showed in his Plate 40, fig. 14, the least angular form of P. buschii, which is very similar to the female form of P. agapetus. This is became both species share the body whorl shape ranging from angulose to globular, and broad um- bilical area circled by an angular or acute ridge. The features that reliably to distinguish both species, as redefined herein are listed in Table 6.
ACKNOWLEDGEMENTS
| wish to express my gratitude to Analia Amor, Instituto de Embriologia, Biologia e
TWO RELATED SPECIES OF POTAMOLITHUS
13
TABLE 4. Whorl number of P. buschii. Frequency of males and females at each whorl stage present at
the localities studied. % = percentage of population.
Whorls
eroded 2.25 3.00 3:25 3.50 3.75 4.00 4.25 N =
Anchorena Beach
3 2 % 3 25 19 15.23 = 1 3 1.38 1 14 el 6.23 == 64 56 41.52 9 29 68 33.56 1 2 4 2.08 5 135 154 16
Rio San Juan
Isla San Gabriel
3 2 20 19 = 3 3 8 15 24 11 19 32 53 21 37 1 4 103 167
TABLE 5. Shell measurements (mm) and ratios for 78 males and 53 females of 3.50 to 3.75 whorls of P. buschii. X + standard deviation (range). There is no significant difference between sexes, P < .001.
Characters Shell length
Body whorl length
Spire length
Shell width
Aperture length
Aperture width
Columella width
Umbilical area width
Shell length/body whorl length Body whorl length/shell width Shell length/shell width
Aperture length/shell length
Histología, and Miguel O. Manceñido, Facul- tad de Ciencias Naturales y Museo, for their valuable help and criticism of the manuscript. | am indebted to G. M. Davis and an anony-
males
3.90 + 0.39 (2.84 — 4.5) 3.49 + 0.35 (2.52 — 4.14) 0.41 + 0.09 (0.18 — 0.63) 3.92 + 0.39 (2.52 — 4.68) 3.03 + 0.29 (2.08 — 3.51) 2.22 + 0.23 (1.39 — 2.61) 0.32 + 0.08 (0.09 — 0.45) 0.24 + 0.12 (0.04 — 0.54) 1.11 + 0.02 (1.06 — 1.20) 0.89 + 0.04 (0.79 — 1.03) 1.01 + 0.05 (0.89 — 1.13) 0.78 + 0.05 (0.67 — 0.92)
females
3.77 + 0.45
(2.34 — 4.68) 3.39 + 0.41 (2.16 — 4.32) 0.39 + 0.08 (0.18 — 0.63) 3.87 + 0.48 (2.61 — 4.86) 2.99 + 0.31 (2.16 — 3.69) 2.17 + 0.26 (1.35 — 2.70) 0.34 + 0.08 (0.18 — 0.54) 0.25+0.13 (0.09 — 0.54) 1.11+#0.02 (1.06 — 1.16) 0.88 + 0.03 (0.82 — 0.97) 1.02 + 0.04 (0.94 — 1.11) 0.79 + 0.04 (0.69 — 0.92)
mous referee for critically reading the тапи- script. | also want to thank Maria |. Braca- monte (CONICET) for the preparation of rad-
ular material.
14
LÓPEZ ARMENGOL
FIG. 12. Pigment patterns of P. buschii. A, head-neck, dorsal view. B, penis, right side. Scale bar = 1 mm.
TABLE 6. Characters distinguishing P. agapetus and P. buschii.
Characters
Shell Irregular buff zigzag streaks Growth-lines Body whorl sculpture
Sulcus in dorsal view Body whorl base in dorsal view
Relationship between shell length
and shell width Aperture inclination Columella Peristome
External Features Head pigment pattern Eyebrows position Nuchal node size Penis pigment pattern
Gill Filaments Gill filaments number range
Radula Central teeth Middle of the anterior cusps External edge of lateral angle Ventral part of basal cusps Basal process prominent Lateral teeth Central blade more developed
Sexual Dimorphism in Shell
P. agapetus P. buschii no yes faintly marked marked
rounded basal angle in females
no concave longer than wider
35° to 42° wide simple and thin
unpigmented above and around the eyes 0.25 mm black spot in distal end
19-28
concave hollow sometimes curved concave yes
no
yes
rounded angle, strongly angular, or carena subsutural and basal in both sexes no/yes flat wider than longer
40° to 54° narrow thicker, sometimes dark-edged
entirely black in hyaline bands 0.06 mm two parallel bands
28-36
flat straight less concave no
yes no
TWO RELATED SPECIES OF POTAMOLITHUS
FIG. 13. Scanning electron micrographs of the head-neck of P. buschii. A, dorsal view of female head-neck, showing the nuchal node (arrow). B, right side of the female head-neck. C, left side of the head-neck and fully erect penis of a male. Scale bar A, B = 200 um; C = 500 um.
15
LÓPEZ ARMENGOL
FIG. 14. Radula of P. buschii. A, section of radular ribbon excluding left outer marginals. B, enlargement of central and lateral teeth. C, central teeth. D, lateral teeth. E, left inner and outer marginal teeth. F, right inner and outer marginal teeth. Scale bar A = 50 um; B-F = 10 um.
LITERATURE CITED
DAVIS, G. M. & M. C. PONS DA SILVA, 1984, Pot- amolithus: morphology, convergence, and rela- tionships among hydrobioid snails. Malacologia, 25: 73-108.
DAVIS, G. M., N. V. SUBBA RAO 4 K. E. HOAG- LAND, 1986, In search of Tricula (Gastropoda: Prosobranchia): Tricula defined, and a new ge- nus described. Proceedings of the Academy of Natural Sciences of Philadelphia, 138: 426- 442.
EMBERTON, K. C., 1985, Seasonal changes in the reproductive gross anatomy of the land snail Tri- odopsis tridentata tridentata (Pulmonata: Po- lygyridae). Malacologia, 26: 225-239.
FRAUENFELD, G. R. VON, 1865, Zoologische Mis- cellen. V. Verhandlungen der K. K. Zoologisch- Botanischen Gesellschaft in Wien, 15: 525-536.
HERSHLER, R. & J. J. LANDYE, 1988, Arizona Hy- drobiidae (Prosobranchia: Rissoacea). Smithso- nian Contributions to Zoology, 459: 63 pp.
ICZN, 1994, Opinion 1779. Potamolithus Pilsbry and Rush, 1896 (Mollusca, Gastropoda): placed
TWO RELATED SPECIES OF POTAMOLITHUS We
on the Official List with Paludina lapidum d’Or- bigny, 1835 as the type species. Bulletin of Zoo- logical Nomenclature, 51: 271-272.
KABAT, A. R., 1993, Comments on the proposed designation of Potamolithus rushii Pilsbry, 1896 as the type species of Potamolithus Pilsbry, 1896 (Mollusca, Gastropoda) (1). Bulletin of Zoo- logical Nomenclature, 50: 52.
KABAT, A. R. & R. HERSHLER, 1993, The proso- branch snail family Hydrobiidae (Gastropoda: Rissooidea): review of classification and su- praspecific taxa. Smithsonian Contributions to Zoology, 547: 94 pp.
LOPEZ ARMENGOL, M. F., 1985, Estudio sistemático y bioecolögico del género Potamo- lithus (Hydrobiidae) utilizando técnicas numéri- cas. Facultad de Ciencias Naturales y Museo, UNLP, Tesis No. 455: 281 pp. unpublished.
LOPEZ ARMENGOL, M. F. & M. O. MANCENIDO, 1992, Potamolithus Pilsbry, 1896 (Mollusca, Gastropoda): proposed confirmation of P. rushii Pilsbry, 1986 as the type species. Bulletin of Zoological Nomenclature, Case 2801, 49: 109- MS
MANCENDO, М. O. 8 M. Е. LÓPEZ ARMENGOL, 1993, Comments on the proposed designation of Potamolithus ruhii Pilsbry, 1896 as the type species of Potamolithus Pilsbry, 1896 (Mollusca, Gastropoda) (2). Bulletin of Zoological Nomen- clature, 50: 53.
PARODIZ, J. J., 1965, The hydrobid snails of the genus Potamolithus (Mesogastropoda-Rissoa- cea). Sterkiana, 20: 1-38.
PILSBRY, H. A., 1896, Notes on new species of Ammicolidae collected by Dr. Rush in Uruguay. The Nautilus, 10: 86-89.
PILSBRY, H. A., 1911, Non-marine Mollusca of Pa- tagonia. In: W.B. SCOTT, ed., Reports of the Princeton University Expeditions to Patagonia, 1896-1899, 3(2)(5): 566-602.
PILSBRY, H. A. & W. H. RUSH, 1896, List, with notes, of land and fresh water shells collected by Dr. Wm. H. Rush in Uruguay and Argentina. The Nautilus, 10: 76-81.
Revised Ms. accepted 1 January 1995
MALACOLOGIA, 1996, 38(1-2): 19-31
RECRUITMENT OF DREISSENA POLYMORPHA: DOES THE PRESENCE
AND DENSITY OF CONSPECIFICS DETERMINE THE RECRUITMENT DENSITY
AND PATTERN IN A POPULATION?
М. E. Chase & В. С. Bailey
Ecology and Evolution Group, Department of Zoology, University of Western Ontario, London, Ontario, Canada N6A 5B7
ABSTRACT
Results of a field experiment conducted to examine the density and spatial pattern of re- cruitment in a population of Dreissena polymorpha in Lake St. Clair were consistent with the hypothesis that recruitment is in response to a chemical cue released by conspecific adults. The number of recruits were significantly higher in treatments in which conspecific adults were present. Analysis of the distribution of adults and recruits in low and high density treatments showed a strong spatial correlation between adults and recruits. However, the distribution of recruits in the low density treatment was more aggregated in comparison to the high density treatment. Comparison of density and size distribution of recruits between low and high density treatments and the adjacent natural population revealed recruits in the natural population were smaller and less dense than recruits in the experimental treatments. This results suggests that although recruitment is in response to conspecific adults, recruitment into a population with lower adult densities, as represented by the experimental treatments, may result in enhanced
growth of the new recruits.
Key words: Dreissena polymorpha, recruitment, spatial, density, conspecific.
INTRODUCTION
Larval settlement and juvenile recruitment are the initial processes determining the structure of populations of many sessile, aquatic species (Rodriguez et al., 1993). Suc- cessful recruitment of a sessile organism de- pends on the behavioral adaptation of early life stages to meet or avoid biological and physical hazards (Schubart et al., 1995). The location of settlement and potential recruit- ment can affect the performance and ultimate survival of a sessile organism. Stimuli neces- sary for settlement involve a combination of factors, including speed of fluids and con- tours of the substratum (e.g., Sebens, 1983; Wethey, 1986; Butman, 1989; Pawlik & Had- field, 1990; Pawlik et al., 1991; Johnson, 1994), luminosity (e.g., Crisp & Ritz, 1973; Young 4 Chia, 1982) and chemical cues (e.g., Morse 8 Morse, 1984, Pawlik, 1986; Rai- mondi, 1988). Perhaps the most widely ex- amined of all settlement stimuli are the exis- tence of chemical inducers associated with conspecific adults. Such cues are of great ecological importance, because the induction of settlement by conspecifics can account for the aggregated distribution of many benthic marine invertebrates (Rodriguez et al., 1993).
19
Aggregated distributions may increase the probability of fertilization in individuals that either release their gametes into the water column (e.g., Pearse & Arch, 1969; Russo, 1979; Pawlik, 1986) or have internal fertiliza- tion (e.g., Raimondi, 1991). Aggregation also acts as an effective defense mechanism (e.g., Garnick, 1978; Bernstein et al., 1981; Pawlik, 1986; Hoffman, 1989), increases filter-feeding efficiency (e.g., Barnes 4 Powell, 1950) and results in decreased juvenile mortality (e.g., Highsmith, 1982). Settlement induced by con- specific adults has been described in several benthic invertebrates, including polychaetes (Jensen & Morse, 1984; Pawlik, 1986), bar- nacles (Knight-Jones, 1953; Rittschof et al., 1984; Raimondi, 1988; Johnson 4 Strath- mann, 1989; Crisp, 1990; Raimondi, 1991), echinoids (Highsmith, 1982; Burke, 1984) and molluscs (Seki & Kan-no, 1981).
The majority of studies of settlement and/ or recruitment, however, have been confined to marine invertebrates. This is a reflection of the common planktonic larval stage charac- teristic of many benthic marine invertebrates. The recent invader Dreissena polymorpha (Pallas), the zebra mussel, is one of the few North American freshwater benthic inverte- brates with a planktonic larval stage. Other
20 CHASE & BAILEY
freshwater bivalves that possess a plank- tonic larval or juvenile stage include such ex- otic species as the quagga mussel, Dreis- sena bugensis, and the asian clam Corbicula fluminea. Most species of North American freshwater bivalves reproduce either via a specialized parasitic larval stage called glochidia (e.g., Unionidae) or through incuba- tion of a small number of embryos that simply crawl away once ready for juvenile existence (e.g., Sphaeriidae) (Mackie, 1991). Dreissena polymorpha larvae may remain in the water column for 5 days to 5 weeks (Sprung, 1993) before settling onto hard substrata, undergo- ing metamorphosis and becoming juveniles. The incorporation of a new cohort or age class into the population is the stage of the larval life cycle referred to as recruitment (Connell, 1985).
Since its introduction into North America, researchers have devoted considerable en- ergy to studying the ecology and the control of D. polymorpha. Extensive research has been conducted to determine the distribution (e.g., Hebert et al., 1991; Schaner et al., 1991; Dermott 8 Munawar, 1993), predict the spread (e.g., Strayer, 1991; Neary & Leach, 1992: Ramcharan et al., 1992) and ultimate impact (e.g., Maclsaac et al., 1992; Bunt et al., 1993) of D. polymorpha on lake ecosys- tems. However, in order to predict the spread or impact of D. polymorpha, we must first understand what factors regulate popula- tions. For a sessile organism, population dis- tribution is determined by dispersal ability and the extent of passive transport at a large spatial scale and suitable settlement sites at a small spatial scale (Minchinton & Scheib- ing, 1991). As a result, a more appropriate predictor of population structure and com- munity patterns may be sought through the study of recruitment.
The results of a 1989 survey of D. polymor- pha in Lake St. Clair (Hebert et al., 1991) re- vealed a marked heterogeneity in size and cohort structure among sites, depending on the density of D. polymorpha. Hebert et al. (1991) suggested that veliger settlement may be cued by a chemical released by conspe- cific individuals that is an attractant at low concentrations and a repellent at high con- centrations. Wainman et al. (1995) also sug- gested that shell induced factor was the ex- planation for the difference in recruitment between experimental substrata with and without mussels present. Their experimental design, however, consisted of racks sus-
pended below the water surface in the metal forbay of a thermal generating station, and therefore their results may not be represen- tative of recruitment in the natural population.
The objectives of this study were twofold. Firstly, we determined whether or not the presence of conspecifics may be a cue to induce recruitment into a population of D. polymorpha at Lake St. Clair. Secondly, we determined whether or not the spatial ar- rangement of recruits was influenced by the presence and density of conspecifics. Re- sults of recruitment in the experimental study were chen compared to recruitment in the natural population in Lake St. Clair.
METHODS Study Site
The study site was approximately 1 km from shore at 42°19’57.0’N, 82°33’19.5’W at 2.5 m depth near Stoney Point, Ontario, on the southeastern shore of Lake St. Clair (Fig. 1). Lake St. Clair is the smallest of the Great Lakes, with a total area of 1,114 km? (Bolsenga & Herdendorf, 1993). The mean depth is only 3 m, with maximum natural depth of 6.4 m and maximum depth along a dredged shipping channel of 8 m (Bolsenga & Herdendorf, 1993). Average annual tempera- ture is 11.9°C. Temperatures range from near freezing for most of the winter to their sum- mer average peak of 24°C in July and Au- gust. Substratum at the site was predomi- nately silt and clay, with some fine sand and approximately 40% hard substrata, consist- ing of mainly rocks and Unionidae shells. Dreissena polymorpha were found on most submerged hard substrata. Densities of D. polymorpha at this site (+ SE) were 15,735 (+ 316)/m? (1992), 15,545 (+ 310)/т? (1993) and 10,264 (+ 109)/m* (1994) (Chase, unpub- lished data). Recruitment occurred in August and October in 1992, August in 1993, and in October in 1994. Population data from previ- ous years showed good recruitment at this site (1992: 5,469 individuals/m?; 1993: 10,393 individuals/m* (Chase, unpublished data).
Experimental Design The experimental substrata consisted of
plexiglass plates (18 x 18 cm). Each plate was attached to a cement block with a stain-
RECRUITMENT OF DREISSENA POLYMORPHA 21
MICHIGAN
LAKE ST. CLAIR
WINDSOR
ONTARIO
LAKE ERIE
STONEY POINT
FIG. 1. Location of study site at Stoney Point, Ontario, Canada.
less steel bolt (Fig. 2b). The plates were im- mersed in lake water 2-3 days before use to remove any manufacturing chemicals that might have been present and which could prevent initial attachment by adult mussels.
On May 15, 1994, adult mussels (6-21 mm in length) were collected from Lake St. Clair using SCUBA, and subsequently returned to the laboratory. Mussels were randomly cho- sen and placed on the plexiglass plates in an aquaria to allow byssal thread attachment. Three experimental treatments were estab- lished:
(1) No adult mussels, (2) Low adult density (average 167 + 30 in- dividuals/m?), and
(3) High adult density (average 4583 + 419 individuals/m?).
Mussels on the plates remained in the lab- oratory for 48 hours, during which time they were fed dried Chlorella sp. (Beta Green, Na- trol) ad lib. It was found that moderate tem- perature (approximately 15°C) and food ad- dition enhanced byssal thread attachment of the adults (M. Chase, personal observation).
Data Collection
On May 17, 1994, the plates were ran- domly arranged in Lake St. Clair using SCUBA in a 6 x 3 configuration, with a 1-m perpendicular distance between blocks (Fig.
22 CHASE & BAILEY
im 7 zu 2 (=) эй
no adult mussels high density treatment № low density treatment
plexiglass plate stainless steel bolt
Be
adult mussel cement block
6 ст
FIG. 2a. Schematic diagram of experimental design, which consisted of three treatments of adult mussel density—no adults, low density and high density—in Lake St. Clair. FIG. 2b. Diagram of one cement block as placed in the field with a plexiglass plate (18 x 18 cm) attached with a stainless steel bolt. FIG. 2c. Diagram of a plexiglass plate from the low density treatment showing division into 324 (1 x 1 cm) squares and subsequent analysis at three spatial scales; 1 x 1 cm, 2 x 2 ст and 6 x 6 cm. Open symbols represent adult mussels, closed symbols represent recruits.
RECRUITMENT OF DREISSENA POLYMORPHA 23
2a). The plates were monitored visually twice monthly for recruitment.
The plates were removed on November 16, 1994, 182 days after deployment, and re- turned to the laboratory for examination. Of the 18 plates deployed, 16 were recovered, including 6 plates from the high density treat- ment, 5 plates of the low density treatment, and 5 plates of the no mussel treatment. In addition to retrieving the plates, 10 rocks were randomly collected from the surround- ing area so that the density and size distribu- tion of recruits from the experimental treat- ments could be compared to the natural population.
In the laboratory, each plate was divided into 324 (1 x 1 cm) squares (Fig. 2c). The number of adults and recruits in each square was recorded under 10x magnification using a Wild-Heerbrug microscope. Recruitment was defined as individuals between 0.8 and 4 mm in shell length. Adults and recruits were then removed from the plates.
Mussels from the natural population were removed from each of the rocks collected and preserved in ethanol. Densities of adults and recruits in the natural population were deter- mined using the method of Bailey et al. (1995). The shell length of the recruits from both the plates and the natural population were mea- sured at 6.4x magnification using a digitizing tablet interfaced with an IBM personal com- puter (Roff & Hopcroft, 1986). Length was measured as the longest distance between the umbo and the ventral margin.
Data Analysis
Counts of the number of recruits per plate in each treatment were Log,, (x + 1) trans- formed, and a one-way ANOVA was per- formed followed by a Tukey-Kramer test to make a posteriori comparisons of means.
Lengths of recruits on the plates were Log,, transformed and then compared within and among treatments by use of one-way ANOVA. Lengths of recruits in each treat- ment were then compared to Log,, trans- formed lengths of recruits in the natural pop- ulation by one-way ANOVA.
To determine the effect of adult density on the spatial arrangement of recruits, the dis- tribution of adults and recruits was examined at three spatial scales; 1 x 1 cm, 2 x 2 cm and 6 x 6 cm (Fig. 2c). A nested analysis of co- variance was applied to determine how adults and recruits covaried at these scales.
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FIG. 3. Number of recruits (Log, (X + 1) trans- formed) (+ SE) in each of the experimental treat- ments; no adult mussels (n = 5 plates), low density (n = 5 plates) and high density (n = 6 plates).
This analysis quantified the strength and na- ture of the covariation of adults and recruits on the plates in the low and high density treatments.
RESULTS Recruit Density
One-way ANOVA on log,, (x + 1) trans- formed number of recruits showed significant (F = 83.82, DF = 2,13, p < 0.001) differences among the treatments (Fig. 3). Pairwise com- parisons of mean number of recruits in each treatment using the Tukey-Kramer test showed that the number of recruits in the no adult mussel treatment was significantly lower than the low density treatment (p < 0.001) and the number of recruits in the low density treatment was significantly lower than the high density treatment (p = 0.036) (Fig. 3). Examination of the relationship be- tween recruit density and adult density within treatments revealed a positive linear relation- ship within the low density treatment (Fig. 4a) but a negative linear relationship within the high density treatment. Neither regression was significant (Low density: DF = 1,3, F = 2.84, г? = 0.49; high density: DF = 1,4, F = 7,814, Г = 0,65),
Size Distribution
One-way ANOVA of length of recruits between the five plates in the low density treatment was not significant (F = 1.26, DF = 4,203, p = 0.286); therefore, lengths of recruits in the low density treatment were pooled. Lengths of recruits from the six
№ >
RECRUIT DENSITY ( INDIVIDUALS / m’)
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ADULT DENSITY ( INDIVIDUALS / m?)
FIG. 4. Regression of recruit density versus adult density for the low density (A) and high density (B) treatments.
plates in the high density treatments were also pooled, because the one-way ANOVA of length of recruits between the high density treatments was not significant (F = 2.12, DF = 5.622. р = 0.062).
One-way ANOVA of length of recruits п the low and high density treatments was signifi- cant (F = 4.39, DF = 1.834, р = 0.027). The mean length of recruits in the low density treatment (1.89 + 0.03 mm) was significantly larger than the mean length of recruits in the high density treatment (1.81 + 0.02 mm), de- spite the small difference in means.
Because the lengths of recruits in the high and low density treatments differed, separate ANOVA’s were performed to compare them to the natural population. One-way ANOVA revealed the length of the recruits in both the low (F = 175.04, DF = 1,353, p< 0.001) and the high (Е = 197-61, DF = 1,773, р. < 0:001) density treatments (Fig. 5) were significantly larger than the mean lengths in the natural population. The mean length of recruits in the natural population was 1.33 + 0.03 mm (Fig. 5), about 500 um less than in both experi- mental treatments.
CHASE & BAILEY
Spatial Arrangement
Across both low and high adult density treatments, and all plates (Fig. 6), correlation between adults and recruits was high (r = 0.90 + 0.07). There was no significant differ- ence between the correlation values at either the 1 x 1, 2 x 2 or 6 x 6 cm Spatial scales in the low adult density treatment, although the mean correlation at the 2 x 2 cm spatial scale was always the highest (2 x 2: r= 1.14 + 0.08; 6 x 67 т = 0:87 + 0.26). Although и Mais mathematically impossible in simple correla- tion analysis, such estimates are possible in nested covariance analysis. They should just be interpreted as high correlations at this scale. One-way ANOVA of correlation at the different spatial scales in the high adult den- sity treatment revealed no significant differ- ence between the 2 x 2 and the 6 x 6 cm spatial scales (F = 2.04, DF = 1, 10, p = 0.183) although the mean correlation at the 6 x 6 cm scale (r = 0.88 + 0.07) was always higher than the mean correlation in the 2 x 2 cm scale (r = 0.74 + 0.08). Correlation at the 1 x 1 cm scale was significantly lower than either the 2 x 2 or the 6 x 6 cm scales in the high density treatment (Е = 17.01, DF = 2, 15, p< 01001}: Correlation at the 1 x 1 cm scale was also low in the low density treatments (mean r = 0.64 + 0.5). Low correlation between adults and recruits at the 1 x 1 cm scale reflects the average length of adult mussels on the plates, which was 1.03 cm.
DISCUSSION Recruitment Density
Results of the experimental study showed that the density of recruitment increased with the density of adults. Little recruitment was observed on plates with no adult mussels present. Several explanations may account for the pattern of recruitment observed in this study, including differential deposition and attachment, post depositional movement, and differential mortality after settlement (Johnson, 1994). Because this study exam- ined only recruitment, it is difficult to deter- mine which of the possible mechanisms may be underlying the settlement of D. polymor- pha at Lake St. Clair. Recruitment is defined as the arrival of the first cohort or age class into the population (Connell, 1985), so it in- cludes any post-settlement movement or
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RECRUITMENT OF DREISSENA POLYMORPHA
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= 631) and low (n =
FIG. 5. Length-frequency histograms of recruit length in the high (n
population (n = 148).
5
1X1
2X2
6X6 1X1
26 CHASE & BAILEY 1.25 PP, ÉD e 1:00 S E 0.75 3 uy 0:50 cc 2 O 0.25 O 0.00 6X6 2X2 HIGH
LOW
FIG. 6. Correlation (+ SE) between adults and recruits in the high and low density treatments at each of the
three spatial scales; 1 x 1 cm, 2 x 2 cm and 6 x 6 cm.
montality that may have occurred. It is possi- ble that settlement did occur on the clean plates but the mussels did not survive to the time of census. Alternatively, another factor may have been acting as a deterrent to pre- vent settlement to the clean plates. Even on plates with adults, recruitment occurred only on or very close to the adults. It was ob- served on several occasions that herbivorous snails were present on the clean plates. While the mussels are at no risk of predation from the snails, their presence may still act as a deterrent to recruitment. Barnacle recruit- ment can be reduced in the presence of lim- pets (Denley 8 Underwood, 1979; Miller, 1986) because of the biological disturbance (i.e., bulldozing) by the limpets. Johnson 4 Strathmann (1989) demonstrated reduced settlement of barnacle larvae as a result of prior occupation of the substratum. Their re- sults indicated that mucus secretions may have been responsible for the reduction in settlement, because they may have affected the adhesion of the larvae or caused an al- teration in the existing cues present on the substratum (Johnson & Strathmann, 1989). The most likely explanation of the recruitment pattern observed in this study, however, is that of differential deposition and attach-
ment, that is, recruitment is in response to a cue released by conspecific adults. Wainman et al. (1995) also observed no settlement on treatments without mussels. In addition to treatments with and without adult mussels, Wainman et al. (1995) included treatments with mussel-sized stones. These treatments served as a control to ascertain whether re- cruitment was in response to a chemical cue released by the adults or simply in response to the heterogeneity of the substrata. Wain- man et al. (1995) found settlement and re- cruitment was significantly lower on mussel- sized stones than on live mussels. This pattern was maintained even after 10-12 days despite reduction in the numbers of re- cruits. This pattern suggests that although there is post settlement mortality, the pattern of settlement with conspecifics was main- tained. A laboratory study on settlement and metamorphosis of larval zebra and quagga mussels (Baldwin, 1995) provides further ev- idence for the presence of a chemical cue associated with conspecific adults. Baldwin (1995) found that in the laboratory D. poly- morpha settled and metamorphosed more readily on natural substrata (adult shells) and in water from adult rearing tanks as opposed to water not exposed to adults. On the basis
RECRUITMENT OF DREISSENA POLYMORPHA 27
of our study and the research described above, it appears that D. polymorpha re- sponds to some chemical cue released by adult conspecifics that enhances settlement and recruitment. The exact nature of the cue, however, was beyond the scope of this study.
Our study also examined the effect of in- creased density of adult mussels on the den- sity and spatial pattern of recruitment. Prox- imity to adults allows for synchronization of spawning and increased fertilization of spawned gametes as well as local introduc- tion of food as a result of adult filtering activ- ity. Large aggregations have a better chance of surviving physical disturbance and conse- quently gain a longer adult life span and over- all increased fecundity (Pawlik, 1986). How- ever, at high population densities, organisms may experience intense intraspecific compe- tition for space (Wu, 1980; Hui & Moyse, 1987) and resources (Russo, 1979) and in- creased rates of both predation (Fairweather, 1988) and parasitization (Blower 8 Roughgar- den, 1989). Therefore, at high population densities there may be selective pressure for individuals to avoid conspecifics at settle- ment (Satchell & Farrell, 1993).
Within this study, recruitment density was highest in the high density treatment. How- ever, variation in the adult densities within each of the high and low density treatments enabled the examination of the relationship between recruit density and adult density within each treatment. This variation is the result of differential attachment of adult mus- sels within the laboratory and subsequent loss of adults during transportation and placement in the field site. Although the data are limited, it was observed that within the high density treatment (n = 6 plates) there is a negative relationship between adult mussel density and the density of recruits, whereas in the low density treatment (n = 5 plates), there is a positive relationship between adult mussel density and recruit density. lt is pos- sible that there is reduced recruitment with higher adult densities, but the adult densities employed in the high density treatments were not large enough to elicit such a re- sponse. When comparison was made be- tween the recruitment densities from the ex- perimental treatments and the natural population, it was observed that the recruit- ment density in the natural population was 1,257 + 178 individuals per m? [which is com- parable to the recruitment density in the low
density treatment (1,198 + 141 individuals per m?)] but much lower than the recruitment density in the high density treatment (3,189 + 637 individuals/m*). Adult densities in the natural population were 8,029 + 506 individ- uals per m? versus only 4,583 + 419 individ- uals per m° for the high density treatments. This suggests that there may be some avoid- ance of the high adult density in the natural population.
Spatial Arrangement
Examination of the spatial arrangement by nested analysis of covariance revealed a strong correlation between adults and re- cruits, confirming the observation that at all scales we tended to find recruits when adults were present. When the spatial arrangement was examined on three spatial scales the low density treatment had the highest correlation at the 2 x 2 cm scale, whereas the high den- sity treatment the highest correlation was at the 6 x 6 cm scale. However, correlation in the 2 x 2 and the 6 x 6 cm scales were not significantly different within treatments. This pattern suggests that while in the low density treatment the recruits are found closer to the adults than in the high density treatment, both treatments show the same conclusion that the recruitment occurs in response to the presence of adult conspecifics.
In a patchy environment (represented by the low density treatment), the recruits must be close to the adults to obtain whatever benefit — protection, enhanced feeding — that such an association would elicit. This is indicative of the higher correlation at the 2 x 2 cm scale. Hoffman (1989) suggested that gregarious settlement reduces stress on the vulnerable meta individual. Clumps of barna- cles may also influence water flow in a way that enhances feeding (Barnes & Powell, 1950). However, in a more homogenous en- vironment (represented by the high density treatment) such a close association may be detrimental because of competition for space and resources and the increased risks of pre- dation of parasitism. In the high density treat- ment, the adults and recruits covaried on a larger scale (6 x 6 cm) than in the low density treatment, indicating a more uniform distribu- tion. In addition, the ratio of recruits to adults was much lower in the high density treatment (0.8 + 0.2) than the low density treatment (7.5 + 0.8). Hebert et al. (1991) observed a marked heterogeneity in size and cohort structure in
28 CHASE & BAILEY
D. polymorpha at different sites in Lake St. Clair in 1989. Members of the 1988 cohort had the smallest shell sizes at sites with the highest density, suggesting that their growth rates were slowed by intraspecific competi- tion.
Natural Population
Comparison of the mean length of recruits revealed that recruits in the natural popula- tion were significantly smaller than recruits in either the low or the high density treatments. The largest mean length of recruits was in the low density treatment (1.89 mm), which may suggest that increased competition for food in the high density environment resulted in reduced growth of recruits. Such a scenario will confer an advantage of recruiting into a low density habitat with either more space to grow or decreased competition for food with larger mussels. This observation may also explain the reduction in growth of mussels at Lake St. Clair since their introduction. Popu- lation densities near Stoney Point were only 0.5 and 4,500 individuals per m° in 1988 and 1989 respectively (Hebert et al., 1991). At that time, Mackie (1991) reported that an overwin- tering young adult between 1-4 mm in shell length will attain a shell length of 15 to 20 mm by the end of the year. Our data have shown that overwintering young adults of similar size (1-4 mm) had shell lengths of only 9 mm (Chase, unpublished data) by the end of the next year. Population densities at Stoney Point now exceed 10,000 individuals per m° (Chase, unpublished data). Similar restriction in growth rates and survival of recent recruits of the barnacle Pollicipes polymerus were determined to be the result of competition between the established adults and the re- cruits for food resources (Page, 1986). When large adults were experimentally removed from an aggregate, the smaller barnacles were able to increase rapidly in size (Page, 1986). Larger barnacles may also have inter- fered with the water flow that brings food to the smaller barnacles (Page, 1986). In the mussel Mytilus edulis, Kautsky (1982) also re- ported that growth was suppressed in small mussels by increased density of large mus- sels. However, differences in size distribution and abundance may also be the result of dif- ferential recruitment between the experimen- tal and natural population. This observation may also be the result of the raised level of the bricks in the water column, which may
enhance growth of recruits. Pontius & Culver (1995) found that D. polymorpha higher in the water column had larger biomass, which may indicate they were better able to obtain food. However, the significant difference between the low and high density treatments suggests an explanation other than height in the water column.
Conclusion
It appears that for D. polymorpha at Lake St. Clair, the presence and density of con- specifics are important determinants of the recruitment density and pattern in the popu- lation. The presence of adult conspecifics may offer some chemical cue that induces recruitment into the population. However, re- cruitment into a low density habitat may be advantageous because it may enhance the growth of young recruits. Therefore, in D. polymorpha there appears to be a tradeoff between adult densities that are high enough to provide an attachment site and protection but low enough to enhance growth and pos- sibly survival. Larger mussels may have a better chance at surviving the winter, and be- cause fecundity is related to size in most benthic invertebrates (Hughes, 1971; Spight & Emlen, 1976; Brousseau, 1978; Sprung, 1987; Chase & Thomas, 1995), recruitment into a low density habitat may also enhance reproductive output, assuming this size dif- ferential is maintained.
The objective of this study was to examine recruitment. As such, the extent of post set- tlement mortality is unknown. It is possible the post settlement mortality was higher in the low density treatments than in either the high density treatment or the natural popula- tion. Thus, although our study suggests that recruitment into low density habitats may be advantageous because of enhanced growth and survival, it may have also suffered from a greater initial mortality. However, in terms of the ultimate survival and population structure of D. polymorpha at Lake St. Clair our results are valid.
ACKNOWLEDGEMENTS
We are grateful to R. Coulas, S. MacPher- son, J. Mitchell and S. Wolfenden for their assistance in the field. Special thanks to M. Topping for reading drafts of this paper and
RECRUITMENT OF DREISSENA POLYMORPHA 29
offering constructive criticism. This research was funded through Natural Science and En- gineering Research Council of Canada, On- tario Ministry of Natural Resources, and the Great Lakes University Research Fund (Lake Erie Trophic Transfer) grants to R. C. Bailey.
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RECRUITMENT OF DREISSENA POLYMORPHA 31
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SPRUNG, M., 1993, The other life: an account of present knowledge of the larval phase of Dreis- sena polymorpha. Pp. 39-53, in: T. F. NALEPA & D. W. SCHLOSSER, eds., Zebra mussels: biology, im- pacts and control. Lewis Publishers, Chelsea, MI.
STRAYER, D. L., 1991, The projected distribution of the zebra mussel, Dreissena polymorpha, in North America. Canadian Journal of Fisheries and Aquatic Sciences, 48: 1389-1395.
WAINMAN, B. C., S. S. HINCKS, N. K. KAUSHINK 8 G. L. MACKIE, 1995, Biofilm and substrate
preference in the dreissenid larvae of Lake Erie. Canadian Journal of Fisheries and Aquatic Sci- ences, In press.
WETHEY, D. S., 1986, Ranking os settlement cues by barnacle larvae: influence of surface contour. Bulletin of Marine Science, 39: 393-400.
WU, R. S. S., 1980, Effects of crowding on the energetics of the barnacle Balanus glandula Dar- win. Canadian Journal of Zoology, 58: 559-566.
YONGE, C. M. 8 F. S. CHIA, 1982, Factors con- trolling spatial distribution of the sea cucumber Psolus chitonoides: settling and post-settling behaviour. Marine Biology, 69: 195-205.
Revised Ms. accepted 28 November 1995
MALACOLOGIA, 1996, 38(1-2): 33-34
ADDITIONAL NOTES ON NOMINA FIRST INTRODUCED BY TETSUAKI KIRA IN “COLOURED ILLUSTRATIONS OF THE SHELLS OF JAPAN”
Rúdiger Bieler' & Richard E. Petit”
The taxa, both available and unavailable, first proposed by Tetsuaki Kira in the numer- ous printings of his ‘‘Coloured Illustrations of the Shells of Japan” and the English edition, “Shells of the Western Pacific in Color, Vol. |’ were recently listed by us (Bieler & Petit, 1990). At the time, we discussed 54 species- group and one genus-group name. Forty names were found to be available from this work, although only five of these had been formally designated as new taxa. The diffi- culty in recognizing some of these unan- nounced introductions is demonstrated by our having to add two new taxa that we over- looked despite extensive searching and comparing the various printings and editions in which some nude names have been intro- duced. There probably remain still others that have eluded us. Also, we add additional data on the previously listed genus-group name.
Laevistrombus Abbott, 1960
Laevistrombus Kira, 1955: 31 (nomen nu- dum).
Laevistrombus Kira. Abbott, 1960: 47-48 (type species designated: Strombus ca- narium Linné, 1758).
This name first appeared in the 3rd printing of the 1st edition of ‘‘Coloured Illustrations of the Shells of Japan” as a subgenus for two nominal species of Strombus: S. (L.) canar- ¡um Linné, 1758, and S. (L.) isabella Lamarck, 1822. No description or statement of differ- entiation was given, as required by ICZN Code Article 13a, nor was a type species designated. Subsequent printings remained unchanged at least through the 6th printing of the 2nd edition (1963). In the 9th printing of the 2nd edition (1964), Laevistrombus is ele- vated to genus-level and L. isabella emended to L. canarium “forma” isabella. The two in- termediate printings have not been seen, but have no effect on this discussion.
When Abbott (1960: 47-48) treated Laevis-
trombus as a subgenus in his monograph of Strombus, he gave a brief description of Laevistrombus and designated S. canarium Linné as its type species. Although Abbott cited Kira as the author of Laevistrombus, the name had not previously been available and must take date and authorship from Abbott, 1960 (ICZN Code Article 50a).
Simplicifusus Kuroda & Habe, 1971
Simplicifusus Kira, 1962: 85 (nomen nudum).
Simplicifusus Kira, 1964: 77 (nomen nudum).
Simplicifusus Kira. Kuroda & Habe, 1971: 282, 184 (type species designated: Fusi- nus simplex Smith [sic; = Fusus simplex Е. A. Smith, 1879].
Simplicifusus first appeared in Kira's “Shells of the Western Pacific in Color” (1962: 85) as a subgenus of Fusinus for two species: F. (S.) hyphalus M. Smith and F. (S.) simplex (Smith) [= Fusinus hyphalus Maxwell Smith, 1940, and Fusus simplex E. A. Smith, 1879]. We cannot determine exactly when this name first appeared in the Japanese ver- sion of this work, ‘‘Coloured Illustrations of the Shells of Japan, Vol. 1.” It was not in the 6th printing (1963) but was in the 9th printing (1964). We have not seen the two intermedi- ate printings. However, Kira (1962, 1964) gave no description or statement of differen- tiating characters as required by ICZN Code Article 13a.
Kuroda & Habe (1971) cited Simplicifus Kira as a genus (Japanese text, p. 282) and as a subgenus of Fusinus (English text, p. 184). A description of the genus is given (Jap- anese text, p. 282), and Fusinus simplex (Smith) is designated as type species (Japa- nese p. 282; English p. 184). Because Sim- plicifusus was not previously an available name, it must take date and authorship from Kuroda & Habe, 1971 (ICZN Code Article 50a).
'Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605, U.S.A. 2P. O. Box 30, North Myrtle Beach, South Carolina 29582, U.S.A.
34 BIELER & PETIT
Pictodentalium Habe, 1963
Pictodentalium Kira, 1959: 105 (and subse- quent years; nomen nudum).
Pictodentalium Habe, 1963: 255 (genus de- scribed; type species designated: Den- talium (Pictodentalium) formosum hirasei Kira, 1959).
In our previous paper (1990: 141), we showed that this genus-group name was a nomen nudum in all editions of Kira's works. lt was treated in a systematic manner by Habe in 1963 (p. 255), who gave a descrip- tion of it as a subgenus. He attributed the name to Kira and gave the type-species as Dentalium (Pictodentalium) formosum hirasei Kira, stating that designation was by mono- typy. He then placed D. (P.) formosum hirasei Kira in the synonymy of D. (P.) formosum (A. Adams & Reeve, 1850). Because Pictoden- talium had not previously been made avail- able, it must take date and authorship from Habe, 1963 (ICZN Code Article 50a).
We thank Dr. Alan R. Kabat for bringing to our attention the omission of Simplicifusus in our earlier paper, and an anonymous re- viewer for additional data on the availability of Pictodentalium.
LITERATURE CITED ABBOTT, R. T., 1960, The genus Strombus in the
Indo-Pacific. Indo-Pacific Mollusca, 1: 33-146. BIELER, R. & R. E. PETIT, 1990, On the various
editions of Tetsuaki Kira’s “Coloured Illustra- tions of the Shells of Japan” and “Shells of the Western Pacific in Color, Vol. |,” with an anno- tated list of new names introduced. Malacologia, 32: 131-145.
HABE, T., 1963, A classification of the scaphopod mollusks found in Japan and its adjacent area. Bulletin of the National Science Museum (Tokyo), 6: 252-281, pls. 37-38.
[ICZN] International Commission on Zoological No- menclature, 1985, International Code of Zoolog- ical Nomenclature, 3rd ed. London, Berkeley, and Los Angeles, xx + 338 pp.
KIRA, T., 1955, Coloured illustrations of the shells of Japan. [viii] + 204 pp., 67 pls.; Hoikusha, Os- aka [for additional printings, see Bieler & Petit, 1990].
KIRA, T., 1959, Coloured illustrations of the shells of Japan. Enlarged & Revised Edition. [1st print- ing of Revised Edition: March 10, 1959]. [6] + vii + [1] + 239 pp., [1] + 71 pls.; Hoikusha, Osaka. [6th printing: February 5, 1963; 9th printing: No- vember 1, 1964; for additional printings, see Bieler & Petit, 1990].
KIRA, T., 1962, Shells of the western Pacific in color. [vii] + 224 pp., 72 pls. Hoikusha, Osaka [for additional printings, see Bieler & Petit, 1990].
KURODA, T. & T. HABE, 1971, [Descriptions of genera and species] in Kuroda, Habe & Oyama, The sea shells of Sagami Bay. Maruzen, Tokyo. xix + 741 pp. [in Japanese], pls. 1-121, 489 pp. [in English], 51 pp. index, map.
Revised Ms. accepted 28 November 1995
MALACOLOGIA, 1996, 38(1-2): 35-46
ON THE NEW NAMES INTRODUCED IN THE VARIOUS PRINTINGS OF “SHELLS OF THE WORLD IN COLOUR” [VOL. | BY TADASHIGE HABE AND KIYOSHI ITO; VOL. Il BY TADASHIGE HABE AND SADAO KOSUGE]
Richard Е. Petit" & Rüdiger Bieler”
ABSTRACT
The two volumes of “Shells of the World in Colour” (Vol. |, “The Northern Pacific” by Habe & Ito; Vol. Il, “The Tropical Pacific’’ by Habe & Kosuge) contain many gastropod and bivalve names denoted as new therein. Some of these are nomina nuda made available only in later publications. However, the volumes also contain new taxa that are made available but not indicated as such. The problem is compounded by the existence of multiple printings of both volumes in which unexplained nomenclatural changes have been made. Forty-four species- group names and two genus-group names date from these works. Twelve genus-group names indicated as new were not made available until later. All pertinent treatments of these taxa are
listed.
INTRODUCTION
In our continuing efforts to determine the status and correct dates of publication of various taxa proposed by Japanese authors, this paper discusses names introduced in the two volumes of ‘‘Shells of the World in Co- lour” (Vol. |, “The Northern Pacific” by Habe 8 Ito; Vol. Il, “The Tropical Pacific” by Habe & Kosuge). Both of these volumes went through numerous printings, with changes being made that are not indicated as such.
Neither book is easy to locate, and few workers have access to more than one print- ing (we have failed to locate any copies of some printings). This paper lists the changes between printings that affect zoological no- menclature. At least 14 genus-group and 44 species-group names are involved, spanning many marine gastropod and bivalve families.
Of particular importance is the determina- tion of when a particular taxon was made available for taxonomic purposes. The de- scriptions of the species and subspecies in the two works under consideration are in Japanese and usually very brief. These spe- cies-group taxa are, however, accepted as being validly proposed. The genus-group taxa present more serious problems because 12 of the new names were introduced with- out fulfilling ICZN Code Article 13 require- ments of providing a fixation of type species, and a differentiating description or indication
to such. They are here regarded as nomina nuda and became available only in later works. Two names, Harpofusus and Mega- crenella, appear to fulfill the minimal require- ments set by the Code and are here ac- cepted as dating from their first appearance.
It is hoped that the following notes will be of value to systematists who must refer to these taxa. We have maintained original or- thography when possible, and have not indi- cated some typographical errors and incor- rect usages in order to avoid using “[sic]” as much as possible. Readers should be aware that in addition to these “new” names there are numerous changes between the editions involving generic or (for subspecies) specific allocations, re-identifications, and adjust- ments in spelling and latinization. The works apparently were newly typeset, at least in part, between printings, sometimes resulting in a compounding of problems. An example of the combination of intended and acciden- tal changes is Habe & Ito’s reference to a species of Neptunea (p. 66, pl. 33, fig. 8); this was initially identified as Neptunea minor and later (1977) corrected to “Neptunea Ruro- sio,’’ a lapsus for N. kuroshio Oyama, 1958.
An example of the taxonomic confusion in these works is the nominal subspecies shi- rogai, first introduced as ‘‘Collisella pelta shi- rogai Habe et Ito (nov.)” in 1965. The 1977 printing of the work, referring to the same illustration, not only still indicated it as being
'P. O. Box 30, North Myrtle Beach, South Carolina 29582, U.S.A. “Field Museum of Natural History, Roosevelt Road at Lake Shore Drive, Chicago, Illinois 60605, U.S.A.
36 PETIT & BIELER
new, but changed the name of the species: “Collisella cassis shirogai Habe et Ito (nov.).” An additional layer of difficulty was intro- duced by printer's errors. For instance, “Buccinum chishimananux Habe et Ito (nov.)” of 1965a was meant to introduce a new subspecies, nux, for the species chishi- manum.
Another example that has perplexed au- thors is Harpa kawamurai Habe, first intro- duced in the 3rd printing of Habe & Kosuge (1972) with no indication that it was new. Harpa kajiyamai Habe, which appeared at the same time, has never before been correctly cited in the literature.
Systematists are urged to cite these works by printing. The date of a particular printing can be easily determined from the colophon (inscription at end of each copy). For details on date determination, see Bieler & Petit (1990: 132).
LISTING OF NEW NAMES
(A) Habe 4 Ito, 1965 (in sequence of occur- rence in volume; the work in which each taxon is considered to have been made available is shown by the usage of 1965a, 1965b, or a later date)
1) Collisella pelta shirogai, 1965a 2) Omphalomargarites, 1965b 3) Cirsotrema kagayai, 1965a 4) Bulbus flavus elongatus, 1965a 5) Trophonopsis scitula emphaticus, 1965a 6) Boreotrophon paucicostatus, 1965a 7) Nodulotrophon, 1965b 8) Mohnia multicostata, 1965a
9) Ancistrolepis trochoidea ovoidea, 1965a 0) Fusipagoda, 1965b
1) Buccinum chishimanum nux, 1965a
2) Buccinum hosoyai, 1965a
3) Висстит opisthoplectum microcon- cha, 1965a
4) Buccinum felis shikamai, 1965a
5) Buccinum kawamurai, 1965a
6) Clinopegma buccinoides, 1965a
7) Neoberingus, 1965b
8) Beringion, 1965b
9) Harpofusus, 1965a
0) Volutopsion, 1965b
1) Buccinum subreticulatum, 1965a
2) Buccinum ferrugineum, 1965a
3) Висстит kinukatsugi Habe 4 Ito, 1968 4) Buccinum midori, 1965a
5) Boreomelon stearnsii ryosukei, 1965a
(26) Fulgoraria (Musashia) kaneko hayashii, 1965a
(27) Decollidrillia, 1965b
(28) Decollidrillia nigra, 1965a
(29) Megacrenella, 1965a
(30) Adula californiensis chosenica, 1965a
(31) Megacardita ferruginosa koreana, 1965a
(B) Habe & Kosuge, 1966 (in sequence of occurrence in volume; the work in which each taxon is considered to have been made available is shown by the usage of 1966a, 1966b, or a later date)
(32) Patelloida (Collisellina) saccharinoides,
1966a
) Astralium yamamurae, 1966a
) Granulittorina, 1966b
) Granulittorina philippiana, 1966a
) Clypeomorus batillariaeformis, 1966a
) Ficadusta, 1966b
) Reticutriton, 1966b
) Spinidrupa, 1966b
) Pyrene testudinaria nigropardalis, 1966a
(41) Pyrene lacteoides, 1966a
(42) Plicarcularia gibbosuloidea, 1966a
(43) Hemifusus carinifer, 1966a
(44) Latirus stenomphalus, 1966a
(45)
(46)
(47)
(33 (34 (35 (36 (37 (38 (39 (40
Vexillum rubrocostatum, 1966a Nebularia yaekoae, 1966a Награ kawamurai Habe, in Habe 4 Kosuge, 1972
(48) Harpa kajiyamai Habe, in Habe 4 Kosuge, 1972
(49) Volutoconus grossi mcmichaeli, 1966a
(50) Brachytoma kurodai, 1966a
(51) Brachytoma kawamurai, 1966a
(52) Brachytoma vexillium, 1966a
(53) Eglisia brunnea, 1966a
(54) Mantellum perfragile, 1966a
(55) Anomiostrea, 1966b
(56) Laevicardium rubropictum, 1966a
(57) Vasticardium nigropunctatum, 1966a
(58) Macrotoma yamamurae, 1966a
DISCUSSION BY VOLUME
“Shells of the World in Colour, Vol. |. The Northern Pacific.” Tadashige Habe and Kiyoshi Ito
The first printing of ““Shells of the World in Colour, Vol. |” is dated June 1, 1965 (Habe 4 Ito, 1965a). A paper by Habe & Ito published in Venus (The Japanese Journal of Malacol- ogy) on July 31, 1965 (1965b) also contains
SHELLS OF THE WORLD IN COLOR 37
descriptions of taxa, indicated as new
therein, which had been shown as new in the
book. In the next few years there were sev-
eral printings of the book; Dr. Kosuge (per-
sonal comm., March 15, 1995) advises that
the 11th printing appeared in March 1991. Printings that we have seen:
Printing 1 June 1, 1965 (1965a) 2 September 1, 1970 4 August 1, 1972
5 January 20, 1974
8 October 1, 1977
The following new species appear (using the original arrangement of families). Impor- tant changes between printings and refer- ences from other sources are also listed.
GASTROPODA
Acmaeidae
(1) Collisella cassis shirogai Habe & Ito, 1965a
Collisella pelta shirogai Habe et Ito (nov.). Habe & Ito, 1965a: 11, pl. 4, fig, 18; 1970, 1972, 1974: ibid.
Collisella pelta shirogai subsp. nov. Habe & Ito, 1965b: 16, 29, pl. 4, fig. 8.
Collisella pelta shirogai Habe et Ito. Habe, 1977: 111 (cited as of 1965a).
Collisella cassis shirogai Habe et Ito (nov.). Habe & Ito, 1977: 11, pl. 4, fig. 18.
Trochidae
(2) Omphalomargarites Habe & Ito, 1965b
Omphalomargarites (nov) vorticifera (Dall, 1873). Habe & Ito, 1965a: 17, pl. 6, figs. 6, 7; 1970, 1972, 1974, 1977: ibid. (ge- nus-group name = nomen nudum).
Omphalomargarites subgen. nov. Habe & Ito, 1965b: 17 (type species Margarites vor- ticifera (Dall, 1873), with no indication of genus in which it was to be placed).
Omphalomargarites gen. nov. Habe & Ito, 1965b: 30 (type species, Margarites vor- ticifera (Dall, 1873).
Omphalomargarites (gen. nov.) vorticifera (Dall). Habe & Ito, 1965b: 45 (plate cap- tion for pl. 2).
Omphalomargarites Habe & Ito. Kuroda & Habe, 1971: 31(21) (with Habe & Ito, 1965b, given precedence over 1965a,
and with type species stated to be by original designation)
Omphalomargarites Habe et Ito. Habe, 1977: 90 (cited as of 1965a, with type as Mar- garites vorticifera (Dall, 1873) by mono- typy; 1965b mentioned only as a “cf.” reference).
Epitoniidae (3) Cirsotrema kagayai Habe & Ito, 1965a
Cirsotrema kagayai Habe et Ito (nov.). Habe & ito, 1965429 pl. 7, fig. 25; 1970, 1972, 1974, 1977: ibid.
Cirsotrema kagayai sp. nov. Habe & Ito, 19656: 17, 30, pl. 2; tig: 9.
Cirsotrema kagayai Habe et Ito. Habe, 1977: 56 (cited as of 1965a).
Naticidae (4) Bulbus flavus elongatus Habe & Ito, 1965a
Bulbus flavus elongatus Habe et Ito (nov). Habe & Ito, 1965a: 31, pl. 8, fig. 8; 1970, 1972, 1974, 1977: ibid.
Bulbus flavus elongatus subsp. nov. Habe & Мо, 19656: 17, 31, pl. 3, fig: 2.
Bulbus flavus elongatus Habe et Ito. Habe, 1977: 38 (cited as of 1965a).
Muricidae
(5) Trophonopsis scitula emphaticus Habe & Ito, 1965a
Trophonopsis scitula emphaticus Habe et Ito (nov.). Habe & Ito, 1965a: 36, pl. 10, fig. 10; 1970, 1972, 1974, 1977: ibid.
Trophonopsis scitula emphaticus subsp. nov. Habe & Ito, 1965b: 18, 31, pl. 2, fig. 1.
Trophonopsis scitulus emphatica Habe et Ito. Habe, 1977: 38 (cited as of 1965a).
(6) Boreotrophon paucicostatus Habe & Ito, 1965a
Boreotrophon paucicostatus Habe et Ito (nov: [sic]). Habe 4 Ito, 1965a: 37, pl. 10, fig. 13; 1970, 1972, 1974, 1977: ibid.
Boreotrophon paucicostatus sp. nov. Habe & Ito, 1965b: 18, 32, pl. 2, fig. 10.
Boreotrophon paucicostatus Habe et Ito. Habe, 1977: 95 (cited as of 1965a).
(7) Nodulotrophon Habe & Ito, 1965b
Nodulotrophon (nov.) аа! (Kobelt, 1878). Habe & Ito, 1965a: 37, pl. 10, fig. 14;
38 PETIT & BIELER
1970, 1972, 1974, 1977: ibid. (genus- group name = nomen nudum).
Nodulotrophon gen. nov. Habe & Ito, 1965b: 19, 32 (with type species as Trophon dalli Kobelt, 1878).
Nodulotrophon Habe et Ito. Habe, 1977: 87 (cited as of 1965a, with type, by mono- typy, Trophon dalli Kobelt, 1878; 1965b not mentioned).
Taxonomic note: This genus-group name must date from 1965b because there was no description in 1965a.
Buccinidae (8) Mohnia multicostata Habe & Ito, 1965a
Mohnia multicostata Habe et Ito (nov.). Habe & Ito, 1965а: 45, pl. 13, fig. 12; 1970, 1972, 1974, 1977: ibid.
Mohnia multicostata sp. nov. Habe & Ito, 1965b: 19, 33, pl. 2, fig: 2.
Mohnia multicostata Habe et Ito. Habe, 1977: 80 (cited as of 1965a).
(9) Ancistrolepis trochoidea ovoidea Habe & Ito, 1965a
Ancistrolepis trochoideus ovoideus Habe et Ito (nov.). Habe & Ito, 1965a: 46, pl. 13, fig. 18; 1970, 1972, 1974, 1977: ibid.
Ancistrolepis trochoideus ovoideus subsp. nov. Habe & Ito, 1965b: 20, 33, pl. 2, fig. 13%
Ancistrolepis trochoidea [Bathyancistrolepis] ovoidea Habe et Ito. Habe, 1977: 92 (cited as of 1965a).
(10) Fusipagoda Habe 4 Ito, 1965b
Fusipagoda (nov.) exquisita Dall, 1913. Habe & Ito, 1965a: 48; Habe & Ito, 1970, 1972, 1974, 1977: ibid. (genus-group name = nomen nudum).
Fusipagoda gen. nov., Habe & Ito, 1965b: 21 (with type species as Mohnia exquisita Dall).
Fusipagoda Habe et Ito. Habe, 1977: 43 (cited as of 1965b with type species as cited, by original designation; 1965a cited as “name only’’).
(11) Buccinum chishimanum nux Habe 4 Ito, 1965a
Buccinum chishimananux [sic] Habe et Ito (nov.). Habe 4 Ito, 1965a: 49, pl. 14, fig. 2.
Buccinum chishimanum nux subsp. nov. Habe & Ito, 1965b: 22, 36, pl. 2, fig. 7.
Buccimum [sic] chishimana nux Habe et Ito (nov.). Habe 4 Ito, 1970: 49, pl. 14, fig. 1; 1972, 1974, 1977: ibid.
Buccinum chishimanum nux Habe et Ito. Habe, 1977: 88 (cited as of 1965).
(12) Buccinum hosoyai Habe & Ito, 1965a
Buccinum hosoyai Habe et Ito (nov.). Habe & Ito, 1965a: 49, pl. 14, fig. 2; Habe & Ito, 1970, 1972, 1974, 1977: ibid.
Buccinum hosoyai sp. nov. Habe & Ito, 1965b::23,:36, pl. 2599-89:
Buccinum hosoyai Habe et Ito. Habe, 1977: 49 (cited as of 1965a).
(13) Buccinum opisthoplectum microconcha Habe & Ito, 1965a
Buccinum opisthoplectum microconcha Habe et Ito (nov.). Habe & Ito, 1965a: 50, pl. 14, fig. 7; 1970, 1972, 1974, 197%
ibid.
Buccinum opisthoplectum microconcha subsp. nov. Habe & Ito, 1965b: 23, 37, pl. 2, fig. 6.
Buccinum opisthoplectum microconcha
Habe et Ito. Habe, 1977: 75 (cited as of 1965a; stated to be a synonym of Buc- cinum japonicum A. Adams, 1861).
(14) Висстит felis shikamai Habe 4 Ito, 1965a
Buccinum felis shikamai Habe et Ito (nov.). Habe 4 Ito, 1965a: 50; 1970, 1972, 1974, 1977: ibid.
Buccinum felis shikamai subsp. nov. Habe & Ко, 19655: 23; 37, pl. 2, fig 5.
Buccinum felis shikamai Habe et Ito. Habe, 1977: 110 (cited as of 1965b).
(15) Buccinum kawamurai Habe 4 Ito, 1965a
Buccinum kawamurai Habe et Ito (nov.). Habe & Ito, 1965a: 52, pl. 15, fig. 1; 1970, 1972, 1974, 1977: ibid.
Висстит kawamurai sp. nov. Habe & Ito, 1965b: 26, 38, ple 2. fig. it.
Buccinum kawamurai Habe et Ito. Habe, 1977: 58 (cited as of 1965a).
(16) Clinopegma buccinoides Habe & Ito, 1965a
Clinopegma buccinoides Habe et Ito (nov.). Habe & Ito, 1965a: 55, pl. 16, fig. 1; 1970, 1972, 1974, 1977: ibid.
Clinopegma buccinoides sp. nov., Habe & Ito, 1965b: 27, 41, pl. 2, fig. 12.
SHELLS OF THE WORLD IN COLOR 39
Clinopegma buccinoides Habe et Ito. Habe, 1977: 28 (cited as of 1965a).
(17) Neoberingius Habe & Ito, 1965b
Neoberingius (nov.) frielei Dall, (1895) [sic]. Habe & Ito, 1965a: 57, pl. 17, fig. 3. (ge- nus-group name = nomen nudum).
Neoberingius gen. nov. Habe & Ito, 1965b: 21, 35, pl. 3, fig. 7. (type species, Ber- ingius frielei Dall, 1894 [sic]).
Neoberingius (nov.) frielei (Dall, 1895). Habe & Ко, 1970: 57, pl 17; fig: 3; 1972, 1974, 1977: ibid.
Neoberingius Habe et Ito. Habe, 1977: 83 (cited as of 1965b, with type species as cited, by original designation; 1965a cited as “name only”).
(18) Beringion Habe 4 Ito, 1965b
Beringion (nov.) marshalli (Dall, 1919). Habe & Ito, 1965a: 58, pl. 17, fig. 4; 1970, 1972, 1974, 1977: ibid. (genus-group name = nomen nudum).
Beringion gen. nov. Habe & Ito, 1965b: 21, 35, pl. 3, fig. 6 (with type species as Ber- ingius marshalli Dall, 1919).
Beringion Habe et Ito. Habe, 1977: 27 (cited as of 1965b, with type species as cited, by original designation; 1965a referred to with comments: “‘f. 4 as Beringion (nov.) marshalli; f. 5, B. beringii, with a notice of ‘the type-species of Beringion’, name only’’).
Taxonomic note: Habe’s statement (1977: 83) is ambiguous as the mention of “type species” in the Japanese text is in the context of ‘‘Beringion type species is figured,’ which appears in discussion of B. beringii (Middendorff). He cited the new genus as of 1965b, which we con- sider to be correct.
(19) Harpofusus Habe & Ito, 1965a
Harpofusus (nov.) melonis (Dall, 1891). Habe & Ito, 1965a: 59, pl. 18, fig. 1; 1970, 1972, 1974: ibid. (with type species, by monotypy, Harpofusus melonis (Dall, 1891)).
Harpofusus gen. nov. Habe & Ito, 1965b: 20, 34 (with type species as Pyrulofusus melonis Dall, 1891 [as Pyrofusus on p. 20)).
Pyrulofusus (Harpofusus) melonis (Dall, 1891). Habe & Ito, 1977: 59, pl. 18, fig. 1.
Harpofusus Habe et lto. Habe, 1977: 46. (listed as a genus of Buccinidae, cited as
of 1965a, with type species, by mono- typy, Pyrulofusus melonis (Dall, 1891) [= Strombella melonis Dall, 1891)).
Taxonomic note: Habe £ lto (1965a: 59) move this species from its previous placement (Volutopsis, name given in Japanese only) into a new genus, based on the yellowish-orange aperture color- ation and the vertical shell folds and spi- ral ribs. Similarity to Pyrulofusus is also mentioned. This fulfills the ICZN Code requirements, and we date this taxon as of 1965a.
(20) Volutopsion Habe & Ito, 1965b
Volutopsion (nov.) castaneus (Mórch, 1858). Habe & Ito, 1965a: 62, pl. 20, fig. 6; 1970, 1972, 1974, 1977: ibid. (genus- group name = nomen nudum).
Volutopsion gen. nov. Habe 4 Ito, 1965b: 21, 35, pl. 2, fig. 15 (with type species as Volutopsius castaneus Dall [sic)).
Volutopsion Habe et Ito. Habe, 1977: 131 (cited as of 1965a with type species, by monotypy, Volutopsion castaneus [-um] (Mórch, 1858); 1965b is mentioned only as a “cf.” reference, with same type species indicated, but by original desig- nation. We consider this genus name to be available from 1965b, with type spe- cies, by original designation, Volutop- sion castaneum (Mörch, 1858) [= Neptu- nea castanea Mórch, 1858].
(21) Buccinum subreticulatum Habe & Ito, 1965a
Buccinum Subreticulatum [sic] Habe et Ito (nov.). Habe & Ito, 1965a: 73, pl. 27, fig. 4.
Buccinum subreticulatum sp. nov. Habe & Ito, 1965b: 24, 39, pl. 2, fig. 14.
Buccinum subreticulatum Habe et Ito (nov.). Habe & Ito, 1970: 73, pl. 27, fig. 4; 1972, 1974, 1977: ibid.
Buccinum subreticulatum Habe et Ito. Habe, 1977: 118 (cited as of 1965a).
(22) Buccinum ferrugineum Habe & Ito, 1965a
(23) Buccinum kinukatsugi Habe & Ito, 1968
Buccinum ferrugineum Habe et Ito (nov.). Habe & Ito, 1965a: 76, pl. 28, fig. 8. Buccinum ferrugineum sp. nov. Habe & Ito,
1965b: 25, 40, pl. 3, fig. 3. Buccinum kinukatsugi nom. nov. Habe & Ito,
40 PETIT & BIELER
1968: 2, 5, pl. 1, fig. 4 (new name for Buccinum ferrugineum Habe & Ito, 1965, non Born, 1780 [sic; = 1778)).
Buccinum kinukatsugi Habe et Ito (nov.). Habe & Ito, 1970: 76, pl. 28, fig. 8; 1972, 1974, 1977: ibid.
Buccinum kinukatsugi Habe et Ito. Habe, 1977: 63 (cited as of 1968).
(24) Buccinum midori Habe & Ito, 1965a
Buccinum midori Habe et Ito (nov.). Habe & Ito, 1965a: 76, pl. 28, fig. 9; 1970, 1972, 1974, 1977: ibid.
Buccinum midori sp. nov. Habe & Ito, 1965b: 25, 405 pl. 2, fig. 16:
Buccinum midori Habe et Ito. Habe, 1977: 75 (cited as of 1965a).
Volutidae
(25) Boreomelon stearnsii ryosukei Habe & Ito, 1965a
Boreomelon stearnsii ryosukei Habe et Ito (nov.). Habe & Ito, 1965a: 77, pl. 29, fig. 2; 1970, 1972, 1974: ibid.
Boreomelon stearnsii ryosukei subsp. nov. Habe & Ito, 1965b: 26, 42, pl. 2, fig. 17.
Boromelon [sic] stearnsii гуозике! Habe et Ito (nov.). Habe & Ito, 1977: 77, pl. 29, fig. 2.
Boreomelon stearnsii ryosukei Habe et Ito. Habe, 1977: 103 (cited as of 1965a).
(26) Fulgoraria (Musashia) kaneko hayashii Habe & Ito, 1965a
Fulgoraria (Musashia) kaneko hayashii Habe et Ito (nov.). Habe & Ito, 1965a: 77, pl. 29, fig. 4; 1970, 1972, 1974, 1977: ibid.
Fulgoraria (Musashia) kaneko hayashii subsp. nov. Habe & Ito, 1965b: 26, 42, pl. 3, fig. oF
Fulgoraria (Musashia) kaneko hayashii Habe et Ito. Habe, 1977: 47 (cited as of 1965a).
Turridae (27) Decollidrillia Habe & Ito, 1965b (28) Decollidrillia nigra Habe & Ito, 1965a
Decollidrillia nigra Hade [sic] et Ito (nov.). Habe & Ito, 1965a: 80, pl. 30, fig. 6. (ge- nus-group name = nomen nudum).
Decollidrillia nigra gen. et sp. nov. Habe & Ito, 1965b: 27, 43, pl. 4, fig. 6.
Decollidrillia nigra Habe et Ito (nov.). Habe & Ito, 1970: 80, pl. 30, fig. 6; 1972, 1974, 1977: ibid.
Decollidrillia Habe et Ito. Habe, 1977: 35 (cited as of 1965b, with type, by original designation, D. nigra; 1965a cited as “name only”).
Decollidrillia nigra Hade [-be] et Ito. Habe, 1977: 83 (species name cited as of 1965a).
Taxonomic note: We agree that this new ge- nus dates from 1965b, but type desig- nation is by monotypy (Articles 13c, 68d).
Bivalvia
Mytilidae (29) Megacrenella Habe & Ito, 1965a
Crenella (Megacrenella nov.) columbiana Dall, 1897. Habe & Ito, 1965a: 109, pl. 35, fig. 11; 1970, 1972, 1974, 1977: ibid.
(with type species, by monotypy, Crenella (Megacrenella) columbiana (Dall, 1897)).
Megacrenella gen. nov. Habe & Ito, 1965b: 28, 44, pl. 3, fig. 4 (with type species as Crenella columbiana Dall, 1897; 1965a listed as a “cf.” reference).
Megacrenella Habe et Ito. Habe, 1977: 74 (cited as of 1965a, with type species, by original designation, Crenella columbi- ana Dall, 1897)
Taxonomic note: We consider the type indi- cation as by monotypy. The two other nominal taxa mentioned in the Japanese text are clearly stated to be synonyms of Crenella columbiana. Habe & Ito (1965a: 100, in Japanese) refer to something that translates to “type species group,” which we cannot accept as original des- ignation. The authors discuss the posi- tion of the group, based on morpholog- ical characters, as standing between Solamen and Crenella (the latter name mentioned only in Japanese characters) and also indicate its relationship to Arvella. This appears to fulfill the ICZN Code requirements, and we date this taxon as of 1965a.
(30) Adula californiensis chosenica Habe & Ito, 1965a
Adula californiensis chosenica (Kuroda MS.) Habe et Ito (nov.). Habe & Ito, 1965a: 11а, pl. 327, fig--4= 1970; 197201974 1977: ibid.
SHELLS OF THE WORLD IN COLOR 41
Adula californiensis chosenica subsp. nov. Habe 4 Ito, 1965b: 28, 43, pl. 3, fig. 1.
Adula californiensis chosenica Habe et Ito. Habe, 1977: 31 (cited as of 1965a and stated to be a synonym of A. schmidti (Schrenck, 1867)).
Carditidae
(31) Megacardita ferruginosa koreana Habe & Ito, 1965a
Megacardita ferruginosa koreana Habe et Ito (nov.). Habe & Ito, 1965a: 128, pl. 43, fig. 8; 1970, 1972, 1974, 1977: ibid.
Megacardita ferruginea [sic] koreana subsp. nov. Habe & Ito, 1965b: 28, 45 (plate caption), pl. 3, fig. 8.
Megacardita ferruginea [sic] koreanica [sic] subsp. nov. Habe & Ito, 1965b: 44. Megacardita ferruginosa koreana Habe et Ito. Habe, 1977: 65 (cited as of 1965a).
“Shells of the World in Colour, Vol. Il. The Tropical Pacific.” Tadashige Habe and Sadao Kosuge
First published January 15, 1966 (1966a), this work preceded an article in Venus by the same authors (1966b) in which new taxa, first appearing in Volume ll, are proposed. There is no indication in Volume II that these taxa are newly introduced therein. The authors stated (1966b) that these “genera and spe- cies were figured and briefly described” in 1966a and that “they are redescribed in de- tail herewith in the nomenclatural value.” Dr. Kosuge (personal comm., March 15, 1995) has confirmed that the genera all must date from the Venus article.
Dr. Kosuge also advises that there are at least ten printings of this work, the 10th ap- pearing in March, 1991.
Printings that we have seen:
Printing 1 January 15, 1966 (1966a) 2 November 1, 1966 (1966c) 3 February 1, 1972
5 November 11, 1974
6
September 1, 1976
The following new species appear (using the original arrangement of families). Impor- tant changes between printings and refer- ences from other sources are also listed.
Gastropoda
Acmaeidae
(32) Patelloida (Collisellina) saccharinoides Habe & Kosuge, 1966a
Patelloida (Collisellina) saccharinoides Habe et Kosuge. Habe & Kosuge, 1966a: 6, pl. 2, fig. 10; 1966c, 1972, 1974, 1976: ibid.
Patelloida (Collisellina) saccharinoides Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 312.
Patelloida (Collisellina) saccharioides [sic] Habe et Kosuge (sp. nov.). Habe & Ko- suge, 1966b: 326, pl. 29, fig. 6 (this spell- ing also on plate caption on same page).
Patelloida (Collisellina) saccharinoides Habe et Kosuge. Habe, 1977: 103 (cited as of 1966a).
Turbinidae
(33) Astralium yamamurae Habe & Kosuge, 1966a
Astralium yamamurai [sic] Habe et Kosuge. Habe & Kosuge, 1966a: 11; 1966c: ibid. (error in spelling corrected on page 121 and in all later usages)
Astralium (Distellifer [sic] yamamurae Habe et Kosuge. Habe & Kosuge, 1966a: 121, pl. 45, fig. 11; 1966c, 1972, 1974, 1976: ibid.
Astralium yamamurae Habe et Kosuge. Habe & Kosuge, 1972: 11; 1974, 1976: ibid.
Astralium (Destellifer) yamamurae Habe et Kosuge (sp. nov.) Habe & Kosuge, 1966b: 313, 327 (with reference to 1966a, pl. 45, fig. 4 [sic; error for fig. 11]).
Astralium (Destellifer) yamamurae Habe et Kosuge. Habe, 1977: 133 (cited as of 1966a; 1966b cited as “name only’).
Littorinidae (34) Granulilittorina Habe & Kosuge, 1966b
(35) Granulilittorina philippiana Habe & Ko- suge, 1966a
Granulilittorina philippiana Habe et Kosuge. Habe & Kosuge, 1966a: 20, pl. 6, fig. 13; 1966c; ibid. (genus-group name = nomen nudum).
Granulilittorina philippiana Habe et Kosuge (gen. et sp. nov.). Habe & Kosuge, 1966b: 313, 328 (with reference to 1966a, pl. 6, fig. 13).
42 PENITT&:BIEEER
Granulilittorina millegrana (Philippi) Habe et Kosuge. Habe & Kosuge, 1972, 1974, 1976: 20, pl. 6, fig: 13:
Granulilittorina Habe et Kosuge. Habe, 1977: 45. (cited as of 1966b, with type, by monotypy, G. philippiana Habe & Ko- suge; 1966a not mentioned).
Granulilittorina philippiana Habe et Kosuge. Habe, 1977: 96 (cited as of 1966a; stated to be a synonym of G. millegrana (Philippi, 1848)).
Taxonomic note: In 1966a no indication was given that this was a newly introduced genus-group name. Rosewater (1970: 491-493) used Granulilittorina as a valid subgenus of Nodilittorina. In treating the genus-group name he cited both 1966a and 1966b. However, under the species name (in the synonymy of N. (G.) mille- grana) he listed as of 1966b with “Tfig- ured in] Habe and Kosuge” 1966a (square brackets in quote are of Rose- water).
Cerithiidae
(36) Clypeomorus batillariaeformis Habe & Kosuge, 1966a
Clypeomrus [sic] batillariaeformis Habe et Kosuge. Habe & Kosuge, 1966a: 23, pl. 7, fig. 14; 1966c: ibid.
Clypeomorus batillariaeformis Habe et Ko- suge (sp. nov.) Habe & Kosuge, 1966b: 314, 328, pl. 29, fig. 13 (with reference to 1966a, pl. 7, fig. 14).
Clypeomorus batillariaeformis Habe et Ko- suge. Habe & Kosuge, 1972, 1974, 1976: 23, pl. 7, fig. 14.
Clypeomorus batillariaeformis Habe et Ko- suge. Habe, 1977: 26 (cited as of 1966a; original misspelling of genus shown and corrected).
Taxonomic note: Houbrick (1985: 51) treated this species in detail and attributed it to Habe & Kosuge, 1966b, without any mention of 1966a.
Cypraeidae
(37) Ficadusta Habe 8 Kosuge, 1966b
Ficadusta pulchella (Swainson, 1823). Habe 8 Kosuge, 1966a: 40, pl. 14, figs. 15, 16; 1966c: ibid. (genus-group name = nomen nudum).
Ficadusta Habe et Kosuge (gen. nov.). Habe 8 Kosuge, 1966b: 314, 329 (with refer-
ence to 1966a; type species: Cypraea pulchella Swainson).
Ficadusta pulchella (Swainson). Habe 8 Ko- suge, 1966b: 326 (plate expl.), pl. 29, figs: 11,112:
Ficadusta pulchella (Swainson, 1923 [sic]). Habe 8 Kosuge, 1972: 40, pl. 14, figs. 15, 16; 1974, 1976: ibid. (type reset in 1972 to correct English common name).
Ficadusta Habe et Kosuge, 1966. Habe, 1977: 40 (cited as of 1966b, but with type by “monotypy,” whereas in 1966b it was designated; 1966a listed as “name only”).
Cymatiidae (38) Reticutriton Habe & Kosuge, 1966b
Reticutriton pfeifferianum (Reeve, 1844). Habe & Kosuge, 1966a: 43, pl. 15, fig. 14; 1966c: ibid. (genus-group name = nomen nudum).
Reticutriton Habe et Kosuge (gen. nov.). Habe & Kosuge, 1966b: 315, 330 (with reference to 1966a; type species: Triton pfeifferianus Reeve).
Reticutriton pfeifferianus (Reeve, 1844). Habe & Kosuge, 1972: 43, pl. 15, fig. 14; 1974, 1976: ibid.
Reticutriton Habe et Kosuge. Habe, 1977: 102 (cited as of 1966b; 1966a not men- tioned).
Muricidae
(39) Spinidrupa Habe & Kosuge, 1966b
Spinidrupa eurantha [sic] (A. Adams). Habe & Kosuge, 1966a: 54, pl. 20, fig. 4; 1966c, 1972, 1974, 1976: ibid. (genus-group name = nomen nudum).
Spinidrupa Habe et Kosuge (gen. nov.). Habe & Kosuge, 1966b: 315, 330 (with refer- ence to 1966a; type species: Murex eurantha [sic] A. Adams [p. 315; as eu- racantha on p. 330; = Murex euracanthus A. Adams, 1851].
Spinidrupa Habe et Kosuge. Habe, 1977: 115 (cited as of 1966b; 1966a listed as “name only”).
Pyrenidae (Columbellidae)
(40) Pyrene testudinaria nigropardalis Habe & Kosuge, 1966a
Pyrene testudinalia [sic] nigropardalis Habe et
SHELLS OF THE WORLD IN COLOR 43
Kosuge. Habe & Kosuge, 1966a: 57, pl. 21, fig. 3; 1966c: ibid.
Pyrene testudinaria nigropardalis Habe et Ko- suge (sp. nov.). Habe & Kosuge, 1966b: 316, 331, pl. 29, fig. 7 (with reference to 1966a).
Pyrene testudinaria nigropardalis Habe et Ko- suge. Habe 8 Kosuge, 1972, 1974, 1976: 57, Pl 21, 19: 3.
Pyrene testudinalia [sic] nigropardalis Habe et Kosuge. Habe, 1977: 83 (cited as of 1966a).
(41) Pyrene lacteoides Habe & Kosuge, 1966a
Ругепе lacteoides Habe et Kosuge. Habe 8 Kosuge, 1966a: 57, pl. 21, fig. 8; 1966c, 1972, 1974, 1976: ibid.
Pyrene lacteoides Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 316, 330, pl. 29, fig. 8 (with reference to 1966a).
Pyrene lacteoides Habe et Kosuge. Habe, 1977: 68 (cited as of 1966a).
Nassariidae
(42) Plicarcularia gibbosuloidea Habe & Ko- suge, 1966a
Pliarcularia [sic] gibbosuloidea Habe et Ko- suge. Habe & Kosuge, 1966a: 60, pl. 22, figs. 5, 6; 1966c, 1972, 1974, 1976: ibid.
Pliarcularia [sic] gibbosuloidea Habe et Ko- suge (sp. nov.). Habe & Kosuge, 1966b: 317,
Plicarcularia gibbosuloidea Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 326 [pl. explanation], 331, pl. 29, figs. 2, 3 (with reference to 1966a).
Plicarcularia gibbosuloidea Habe & Kosuge. Habe, 1977: 44 (cited as of 1966a; orig- inal misspelling of genus shown and cor- rected).
Galeoidae (Galeolidae in 1966a: 64 and 1966c: 64; correct on p. 65 and in later printings)
(43) Hemifusus carinifer Habe & Kosuge, 1966a
Hemifusus carinifera [sic] Habe et Kosuge. Habe & Kosuge, 1966a: 64, pl. 23, fig. 2; 1966c, 1972, 1974, 1976: ibid.
Hemifusus cariniferus Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 317, 332, pl. 29, fig. 17 (with reference to 1966a).
Hemifusus cariniferus Habe et Kosuge. Habe, 1977: 29 (cited as of 1966a).
Note: Originally introduced as an adjective in the female form, the ending has to be adjusted to the masculine -fer (-fer, -fera, -ferum, meaning “bearing””; as opposed to -ferus-a-um, meaning ‘‘wild’’).
Fasciolariidae
(44) Latirus stenomphalus Habe 8 Kosuge, 1966a
Latirus stenomphalus Habe et Kosuge. Habe 8 Kosuge, 1966a: 68, 122, pl. 45, fig. 16 (with reference to Kira, [1954]: pl. 30, fig. 16, which is the species Kira figured as Latirus recurvirostrum Schubert 8 Wag- ner); 1966a, 1972, 1974, 1976: ibid.
Latirus stenomphalus Habe et Kosuge (sp. nov.). Habe 8 Kosuge, 1966b: 318, 334, (with reference to Latirus recurvirostrum Kira, 1954: pl. 30, fig. 16 [on p. 318] and to 1966a [p. 334]; misspelled sttnom- phalus on p. 318). This reference to Kira is to the species he figured as Latirus recurvirostrum Schubert & Wagner.
Latirus stenomphalus Habe et Kosuge. Habe, 1977: 116 (cited as of 1966a).
Mitridae
(45) Vexillum rubrocostatum Habe & Kosuge, 1966a
Vexillum rubrocostatum Habe et Kosuge. Habe & Kosuge, 1966a: 73, pl. 28, fig. 9; 1966c, 1972, 1974, 1976: ibid.
Vexillum rubrocostatum Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 319, 333, pl. 29, fig. 4 (with reference to 1966a).
Vexillum rubrocostatum Habe et Kosuge. Habe, 1977: 102 (cited as of 1966a).
(46) Nebularia yaekoae Habe & Kosuge, 1966a
Nebularia yaekoae Habe et Kosuge. Habe & Kosuge, 1966a: 76, pl. 28, fig. 34; 1966c, 1972, 1974, 1976: ibid.
Nebularia yaekoae Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 319, 333, pl. 29, fig. 10 (with reference to 1966a).
Nebularia yaekoae Habe et Kosuge. Habe, 1977: 131 (cited as of 1966a).
Harpidae
(47) Harpa kawamurai Habe, in Habe & Ko- suge, 1972
Harpa striata (Lamarck, 1816). Habe & Ko-
44 PETIT & BIELER
suge, 1966a: 79, pl. 30, fig. 2; supple- mental pl. 1, fig. 2; 1966c: ibid.
Harpa kawamurai Habe. Habe, in Habe & Ko- suge, 1972: 79, pl. 30, fig. 2; supplemen- tal pl. 1, fig. 2; 1974, 1976 (no indication that name is new).
Harpa kawamurai Habe & Kosuge, 1973 [sic]. Habe, 1975b: 10 (listed as “invalid” and as ‘= Harpa major Röding, 1798”).
Harpa kawamurai Habe & Kosuge, 1973 [sic]. Matsukuma & Okutani, 1986: 6.
Taxonomic note: The 3rd printing of Habe & Kosuge, where this species first ap- pears, is rare, and we have located only one copy. Not listed by Habe (1977). The Japanese text of Habe (1975b: 10) states that, according to personal com- munication with Dr. Rehder, this nominal species is a form of Harpa major Róding, 1798.
(48
—
Harpa kajiyamai Habe, in Habe & Ko- suge, 1972
Награ cancellata (Roding, 1798). Habe & Kuroda, 1966a: 79, pl. 30, fig. 3; supple- mental pl. 1, fig. 3; 1966c: ibid.
Harpa kajiyamai Habe. Habe & Kosuge, 1972: 79, pl. 30, fig. 3; supplemental pl. 1, fig. 3
Harpa kajiyamai Rehder, 1973: 244, pl. 188, figs. 3, 4 (described from specimens re- ceived from Habe, who was stated to have recognized the species as new and given it a provisional name, and re- quested that it be named for the collec- tor).
Harpa kajiyamai Rehder. Habe & Kosuge, 1974: 79, pl. 30, fig. 3; supplemental pl. 1, fig. 3; 1976: ibid.
Taxonomic note: Walls (1980: 191) in his list of Harpa species includes both H. kajiy- amai Habe, 1970 [sic], and H. kajiyamai Rehder, 1973, indicating that both are ‘‘= [Harpa] harpa,” a synonymy we do not endorse. This species name must be at- tributed to Habe (1972). Not listed by Habe (1977).
Volutidae
(49) Volutoconus grossi mcmichaeli Habe & Kosuge, 1966a
Volutoconus grossi mcmichaeli Habe & Ko- suge. Habe & Kosuge, 1966a: 86, pl. 33, fig. 1; 1966c, 1972, 1974, 1976: ibid.
Volutoconus grossi mcmichaeli Habe et Ko-
suge (sp. nov.). Habe & Kosuge, 1966b: 320, 335, pl. 29, fig. 19 (with reference to 1966a).
Volutoconus grossi mcmichaeli Habe et Ko- suge. Habe, 1977: 74 (cited as of 1966a).
Turridae
(50) Brachytoma kurodai Habe & Kosuge, 1966a
Brachytoma kurodai Habe et Kosuge. Habe & Kosuge, 1966a: 96, pl. 38, fig. 13; 1966c, 1972, 1974, 1976: ibid.
Brachytoma kurodai Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 320, 335, pl. 29, fig. 14 (with reference to 1966a)
Brachytoma kurodai Habe et Kosuge. Habe, 1977: 66 (cited as of 1966a).
(51) Brachytoma kawamurai Habe & Kosuge, 1966a
Brachytoma kawamurai Habe et Kosuge. Habe & Kosuge, 1966a: 96, pl. 38, fig. 14; 1966c, 1972, 1974, 1976: ibid.
Brachytoma kawamurai Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 321, 336, pl. 29, fig. 9 (with reference to 1966a)
Brachytoma kawamurai Habe et Kosuge. Habe, 1977: 58 (cited as of 1966a).
(52) Brachytoma vexillium Habe & Kosuge, 1966a
Brachytoma vexillium Habe et Kosuge. Habe & Kosuge, 1966a: 96, pl. 38, fig. 15; 1966c, 1972, 1974, 1976: ibid.
Brachytoma vexillum Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 321, 336, pl. 29, fig. 5 (with reference to 1966a).
Brachytoma vexillum Habe et Kosuge. Habe, 1977: 130 (cited as of 1966a; original spelling not mentioned).
Taxonomic note: The original spelling of the specific name, although obviously a mis- spelling or typographical error, must be retained in accordance with ICZN Code Article 32.
Epitoniidae (53) Eglisia brunnea Habe & Kosuge, 1966a
Eglisia brunnea Habe et Kosuge. Habe & Ko- suge, 1966a: 103, pl. 40, fig. 16; 1966c: ibid.
Eglisia brunnea Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 322, 337, pl. 29, fig. 18 (with reference to 1966a).
SHELLS OF THE WORLD IN COLOR 45
Eglisia lanceolata brunnea Habe et Kosuge. Habe & Kosuge, 1972: 103, pl. 40, fig. 16; 1974, 1976: ibid.
Eglisia brunnea Habe et Kosuge. Habe, 1977: 28 (cited as of 1966a).
Bivalvia Limidae
(54) Mantellum perfragile Habe 8 Kosuge, 1966a
Mantellum perfragile Habe et Kosuge. Habe 8 Kosuge, 1966a: 144, 177, pl. 68, fig. 6; 1966c, 1972, 1974, 1976: 144.
Mantellum perfragile Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 323, 338. (not figured; 1966a not referred to)
Limaria perfragile Habe et Kosuge. Habe 4 Kosuge, 1972, 1974, 1976: 177, pl. 68, fig. 6 (as Mantellum on p. 144).
Mantellum perfragile Habe et Kosuge. Habe, 1977: 95 (cited as of 1966a and placed in Limaria (Platilimaria)).
Ostreidae (55) Anomiostrea Habe & Kosuge, 1966b
Anomiostrea pyxidata (Adams et Reeve, 1850). Habe & Kosuge, 1966a: 144, pl. 55, fig. 9; 1966c, 1972, 1974, 1976: ibid. (genus-group name = nomen nudum).
Anomiostrea Habe et Kosuge (gen. nov.). 1966b: 323, 338, with type designated as Ostrea pyxidata Adams et Reeve (with reference to 1966a).
Anomiostrea Habe et Kosuge. Habe, 1977: 23 (cited as of 1966b; 1966a not men- tioned).
Taxonomic note: Listed under “nomina du- bia” by Stenzel (1971: N1167, figs. J140a-c), who also showed the name of the type species to be preoccupied. Type species renamed Anomiostrea cor- alliophila Habe, 1975a (new name for O. pyxidata Adams & Reeve, 1848 [sic; = 1850] non Born, 1780 [sic; = 1778].
Cardiidae
(56) Laevicardium rubropictum Habe & Ko- suge, 1966a
Laevicardium rubropictum Habe et Kosuge. 1966a: 153, pl. 59, fig. 2; 1966c, 1972, 1974, 1976: ibid.
Laevicardium rubropictum Habe et Kosuge (sp. nov.). 1966b: 324, 339, pl. 29, fig. 20 (with reference to 1966a)
Laevicardium rubropictum Habe et Kosuge. Habe, 1977: 102 (cited as of 1966a).
(57) Vasticardium nigropunctatum Habe & Kosuge, 1966a
Vasticardium nigropunctatum Habe et Ko- suge. Habe & Kosuge, 1966a: 154, pl. 59, fig. 9; 1966c, 1972, 1974, 1976: ibid.
Vasticardium nigropunctatum Habe et Ko- suge (sp. nov.). Habe & Kosuge, 1966b: 324, 340, pl. 29, fig. 16 (with reference to 1966a).
Vasticardium nigropunctatum Habe et Ko- suge. Habe, 1977: 84 (cited as of 1966a).
Mactridae
(58) Macrotoma yamamurae Habe & Kosuge, 1966a
Mictrotoma [sic] yamamurae Habe et Ko- suge. Habe & Kosuge, 1966a: 166, pl. 65, fig. 8; 1966c: ibid.
Mactrotoma yamamurae Habe et Kosuge (sp. nov.). Habe & Kosuge, 1966b: 325, 340, pl. 29, fig. 15 (with reference to 1966a; original misspelling of genus noted).
Mactrotoma yamamurae Habe et Kosuge. Habe & Kosuge, 1972: 166, pl. 65, fig. 8.
Heterocardia gibbosula Philippi [sic; = De- shayes]. Habe & Kosuge, 1974: 166, pl. 65, fig. 8; 1976: ibid.
Mactrotoma yamamurae Habe et Kosuge. Habe, 1977: 133 (cited as of 1966a; stated to be a synonym of Heterocardia gibbosula Deshayes, 1855).
ACKNOWLEDGEMENTS
The following made copies of publications available or otherwise responded to our re- quests for data: Dr. E. V. Coan, Dr. В. М. Kilburn, Dr. H. G. Lee, Dr. J. H. McLean, Mr. Thomas C. Rice, Dr. Gary Rosenberg, Mr. Walter Sage, and Dr. Emily H. Vokes. Dr. Sadao Kosuge corresponded with us con- cerning later printings of both volumes and the availability of the taxa. Dr. H. D. Cameron, University of Michigan, provided etymologi- cal advice. We are especially indebted to Dr. Takahiro Asami, Tachikawa College of To- kyo, whose translations from the Japanese helped us in deciding on the validity of taxon
46 PETIT & BIELER
descriptions, and to Dr. M. G. Harasewych who, while in Japan, searched for and ob- tained for us a copy of the elusive 3rd printing of Habe & Kosuge. We also wish to thank two anonymous reviewers for their comments.
LITERATURE CITED
BIELER, R. & R. E. PETIT, 1990, On the various editions of Tetsuaki Kira’s “Coloured illustra- tions of the shells of Japan” and “Shells of the western Pacific in color Vol. 1,” with an anno- tated list of new names introduced. Malacologia 32: 131-145.
HABE, T., 1975a, New name for Anomiostrea pyx- idata (Adams & Reeve) (Ostreidae). Venus 33: 184 (April).
HABE, T., ed., 1975b, Publication for commemo- rate 77th anniversary of the birth of Mr. Ryosuke Kawamura. Illustration of shells described by and dedicated to Mr. R. Kawamura. 20 pp., incl. 5 pls. Tokyo (December).
HABE, T., 1977, Catalogue of molluscan taxa de- scribed by Tadashige Habe during 1939-1975, with illustrations of hitherto unfigured species (for commemoration of his sixtieth birthday). 185 pp. incl. 7 pls.; Tokyo. [compiled by T. Inaba and K. Oyama, but authorship credited to Habe on page 2]
HABE, T. & K. ITO, 1965a, Shells of the world in colour, Vol. |. The northern Pacific. viii, [2 pp. map], 176 pp., 56 pls.; Hoikusha, Osaka [addi- tional printings listed in this paper].
HABE, T. & K. ITO, 1965b, New genera and spe- cies of shells chiefly collected from the North Pacific. Venus 24: 16-45, pls. 2-4 (July 31).
HABE, T. & K. ITO, 1968, Buccinid species from
Rausu, Hokkaido. Venus 27: 1-8, pl. 1 (August 31).
HABE, T. 4 S. KOSUGE, 1966a, Shells of the world in colour, Vol. |. The tropical Pacific. vii, [2 pp. map], 193 pp., pls. 1-68, supplemental pls. 1-2; Hoikusha, Osaka (January 15; additional print- ings listed in this paper).
HABE, T. & S. KOSUGE, 1966b, New genera and species of the tropical and subtropical Pacific molluscs. Venus 24: 312-341, pl. 29 (May 17).
HOUBRICK, R.S., 1985. Genus Clypeomorus Jousseaume (Cerithiidae: Prosobranchia). Smithsonian Contributions to Zoology 403: 1-131.
KIRA, T., 1954. [Coloured illustrations of the shells of Japan]. [viii] + 172 + 24 pp., 67 pls; Hoikusha, Osaka (additional printings listed in Bieler 8 Petit, 1990).
KURODA, T., T. HABE & K. OYAMA, 1971. The sea shells of Sagami Bay. Maruzen, Tokyo. xix + 741 pp. [in Japanese], pls. 1-121, 489 pp. [in En- glish], 51 pp. index, map.
MATSUKUMA, A. & T. OKUTANI, 1986. Studies on the Kawamura collection (Mollusca) in the Na- tional Science Museum, Tokyo-ll. Catalogue of type specimens, with description of Pinna cello- phana n. sp. (Bivalvia). Venus 45: 1-10
REHDER, H. A., 1973, The family Harpidae of the world. Indo-Pacific Mollusca 3: 207-274.
ROSEWATER, J., 1970, The family Littorinidae in the Indo-Pacific. Part I. The subfamily Littorini- nae. Indo-Pacific Mollusca 2: 417-528.
STENZEL, H. B., 1971, Oysters. Treatise on Inver- tebrate Paleontology, Part N, Volume 3, Mol- lusca 6, Bivalvia. Pp. N953-N1224.
WALLS, J. G., 1980, Conchs, tibias and harps. T.H.F. Publications Inc. Ltd., Neptune, New Jer- sey. 191 pp.
Revised Ms. accepted 28 November 1995
MALACOLOGIA, 1996, 38(1-2): 47-58
ULTRASTRUCTURAL STUDY OF EUSPERMIOGENESIS IN CLYPEOMORUS BIFASCIATA AND CLYPEOMORUS TUBERCULATUS (PROSOBRANCHIA: CERITHIIDAE) WITH EMPHASIS ON ACROSOME FORMATION
Fadwa A. Attiga' & Hameed A. Al-Hajj
Department of Biological Sciences, University of Jordan, Amman, Jordan
ABSTRACT
The ultrastructure of euspermiogenesis and euspermatozoa of Clypeomorus bifasciata and C. tuberculatus are almost identical. Early spermatids have oval to spherical nuclei, sparse endoplasmic reticulum, few mitochondria, and a well-developed Golgi complex with many vesicles in its vicinity. Acrosome differentiation occurs anywhere within the cytoplasm, and begins with a proacrosomal vesicle, which becomes cup-shaped and plugged at its edges with a dense interstitial granule. Microtubules are embedded in the matrix between the outer and inner acrosomal membranes. The acrosomal vesicle becomes aligned parallel to the antero- posterior nuclear axis, and changes into an inverted flask shape, with two external supporting structures at its basal margins. The interstitial granule becomes hat-shaped, separating the acrosome from the nucleus. The mature acrosome consists of a flat cone with microtubules in its core, an acrosomal rod-like material, and a basal plate. Nuclear shape changes from spher- ical to hammer-head to club-shape, with a posterior invagination enclosing the initial axonemal portion. The fine chromatin material of early spermatids changes to fibrillar, lamellar, and finally very compact material. The euspermatozoan midpiece originates from fusion of spermatid mitochondria into four large spheres, which are later organized into four non-helical mitochon- drial elements, two of which are large and the other two are extremely small. A dense ring structure marks the junction between the midpiece and the glycogen piece. The latter consists of nine tracts of glycogen granules surrounding nine axonemal doublets. The results of this study suggest that acrosomal ultrastructure could be used to establish phylogenetic relation-
ships in Cerithiacea at the generic level.
INTRODUCTION
Morphological diversity of spermatozoa in prosobranchs, as in other animal groups, has been considered as a tool that can be used to ascertain evolutionary paths, through building up phylogenetic and taxonomic. affinities among species (Franzen, 1955, 1956, 1970; Nishiwaki, 1964; Healy, 1983a, 1988a; Koike, 1985). Based on ultrastructural studies of spermiogenesis and sperm morphology, me- sogastropods as a part of caenogastropods (mesogastropods and neogastropods) are classified into two groups. Members of the first group have short nuclei with shallow basal invaginations, associated with conical or flattened acrosomes. The midpiece may show modification of cristae into parallel cri- stal plates, and it is separated from the gly- cogen piece by a dense ring structure. The glycogen piece consists of axonemal micro-
tubules and nine tracts of glycogen granules, whereas the short end piece is composed of an axoneme surrounded only by a plasma membrane. This group of caenogastropods includes superfamilies Cerithiacea (Healy, 1982a, b, 1983a; Afzelius & Dallai, 1983; Koike, 1985), Viviparacea (Griffond, 1980; Koike, 1985), and Cyclophoracea (Selmi & Giusti, 1980; Healy, 1984; Kohnert & Storch, 1984a, b, Koike, 1985). All other superfamilies in Caenogastropoda are classified into the second group, which shares with the first group similar glycogen pieces, dense ring structures and end pieces. On the other hand, members of this group have apical acrosomal vesicles and accessory acrosomal mem- branes, whereas their short or long tubular nuclei may be completely invaginated by the axoneme (Healy, 1988a). The midpiece ele- ments are helically coiled, with usually un- modified cristae (Healy, 1983a, 1986b; Max-
“This work was conducted as part of Fadwa Attiga’s Master thesis. The George Washington University, Columbian College and Graduate School of Arts and Sciences, Department of Biological Sciences, Ph.D. Program. Author to whom all correspondence should be mailed. Address: 2301 E St. NW, Apt # A406, Washington, DC 20037, U.S.A.
48 ATTIGA & AL-HAJJ
well, 1983; Kohnert & Storch, 1984a; Koike, 1985; Jaramillo et al., 1986). Furthermore, comparative sperm ultrastructure has been useful in establishing the affinities of many cerithiacean superfamilies of the Caenogas- tropoda (Healy, 1982a, b, 1983a, 1986a, b, 1988a, b, 1990a, b, 1993; Houbrick, 1988). The present work deals with the ultrastruc- ture of euspermiogenesis and mature eu- sperm (typical sperm) in two species of the superfamily Cerithiacea (family Cerithiidae) that inhabit the rocky shore of the Gulf of Aqaba (Houbrick, 1985; Hulings, 1986). These are: Clypeomorus bifasciata (Sowerby, 1855) [= С. moniliferum (Kiener, 1841), auett.], and C. tuberculatus (Linnaeus, 1758) [= C. petrosa gennesi (Fisher & Vignal, 1901)]. Comparative study of spermiogenesis and sperm morphology of the two cerithiid spe- cies as well as other reported cerithiids aims to emphasize species-specific characters between cerithiids from different geographi- cal regions, and to establish the phylogenetic status of cerithiaceans among prosobranchs.
MATERIALS AND METHODS
Specimens were collected monthly for a year in the intertidal zone opposite to the Ma- rine Science Station of the Gulf of Aqaba. The shell was gently broken, and the testis, re- moved by dissection, was immediately im- mersed in 2.5% glutaraldehyde in filtered sea water for 2 hours at room temperature. The tissue was rinsed thoroughly in filtered sea water, post fixed in 1% OsO, solution in fil- tered sea water, dehydrated in acetone and embedded in Spurr's (1969) medium. Blocks were cut with Sorval MT 2B ultramicrotome using glass knives, and ultrathin sections (50-60 nm) were stained with uranyl acetate and lead citrate. Electron microscopic exam- inations were done with a Zeiss EM 10B transmission electron microscope operated at 60 KV.
RESULTS
The various stages of euspermiogenesis in Clypeomorus bifasciata and C. tuberculatus are almost identical. Therefore, the following description applies for both species unless otherwise mentioned.
Early spermatids are spherical to ovoidal,
with eccentric nuclei. The chromatin material is granular, with some local aggregations of no specific pattern. The granular cytoplasm contains few cisternae of endoplasmic retic- ulum, few mitochondria, and a well-devel- oped Golgi complex with many vesicles at the extremities of its cisternae, indicating ac- tivity (Fig. 1). Nutritive cells can be seen in the intercellular space with many elongated pseudopodia (Fig. 1).
Acrosome development can be divided into two major phases; the pre-attachment acrosome and the post-attachment one, in reference to its attachment to the nucleus. Acrosomal genesis during the first phase be- gins with a single proacrosomal vesicle as- sociated with Golgi complex, in addition to many nearby dense vesicles that are likely to be utilized in the production of the acrosomal elements (Fig. 2). Later, this vesicle attains an inverted U-shape due to posterior indenta- tion, and a dense interstitial granule plugs the prospective subacrosomal space (Figs. 3, 4). The dispersion of dense material from this granule and its deposition on the inner and outer acrosomal membranes assist in the ac- centuation of the acrosome (Figs. 4, 9). Two dense internal supporting structures appear within the acrosomal body, and microtubules constitute the skeleton of the acrosomal cone between the inner and outer acrosomal membranes (Figs. 4, 8, 9).
The second phase of acrosomal develop- ment is demarcated by the attachment of the basal interstitial granule to a depression on the anterior pole of the fibrous nucleus, op- posite to the site of axoneme development (Fig. 10). The acrosome rotates 90” to be- come aligned parallel to the antero-posterior axis of the developing spermatid (Figs. 10, 11). Following its attachment, the acrosome looks like an inverted flask due to a constric- tion at its posterior part (Figs. 11, 12). Two crescent-shaped external supporting struc- tures can be seen at the basal margins of the acrosome near its attachment point to the nucleus. The post-attachment acrosome is further elongated, while the dense interstitial granule gives rise to a basal plate between the acrosome and the nucleus (Figs. 11, 12).
The acrosome of the mature euspermato- zoon in C. bifasciata and C. tuberculatus con- sists of three structures; acrosomal cone, ac- rosomal rod-like material, and basal plate (Figs. 16 inset, 17). The tapering cone may occasionally show parallel plate-like sub- structures, and it is characterized by basal
ULTRASTRUCTURAL STUDY OF EUSPERMIOGENESIS 49
e
FIG. 1. Clypeomorus bifasciata. Early spermatid showing nucleus (N), mitochondrion (M), Golgi complex (GC) and associated vesicles (V). Notice pseudopodia (PP) of the nutritive cell (NC). x11,500
FIG. 2. C. bifasciata. Early spermatid showing peripheral chromatin lining the nucleus (N), Golgi complex (GC), and interstitial granule (IG). x31,250
50 ATTIGA & AL-HAJJ
FIG. 3. C. bifasciata. Early spermatid showing nucleus (N), two mitochondrial (M) spheres at nuclear base, Golgi complex (GC), vesicles (V), and differentiating proacrosomal vesicle (PAV). Notice cytoplasmic bridge (asterisk). x16,000
FIG. 4. C. bifasciata early spermatid. Section showing a differentiating acrosome with microtubules (MT) in its cone, internal supporting structures (arrows) subacrosomal space (SAS), and interstitial granule (IG). x36,000
FIG. 5. C. tuberculatus early spermatid. Section showing nucleus (N), with sites of the attachment of mitochondrial (M) spheres (arrows). x15,200
FIG. 6. C. tuberculatus early spermatid. Section showing nuclear (N) base with mitochondrial (M) spheres, implantation fossa (IF), centriolar derivative (CD), and axoneme (AX). x56,700
FIG. 7. C. bifasciata early spermatid. Section showing four mitochondrial (M) spheres surrounding the axoneme (AX) as the first stage of midpiece development. x15,000
ULTRASTRUCTURAL STUDY OF EUSPERMIOGENESIS 51
bulges in the cone wall that cause a constric- tion in the subacrosomal space. The latter, which extends the whole length of the ac- rosomal cone, contains an acrosomal rod- like material (Figs. 16 inset, 17). À dense basal plate linking the acrosome and the nu- cleus can be seen as a straight dense layer between the two structures. Cross sections in the mature acrosome indicate its flatness, and microtubules assume a zipper-like struc- ture in the matrix between the inner and outer acrosomal membranes (Fig. 18).
Chromatin condensation starts with the formation of a uniformly thick layer at the pe- riphery of the nucleus (Figs. 2, 3). As spermi- ogenesis proceeds, the granular chromatin accumulates at the posterior nuclear pole, and the nucleus undergoes antero-posterior compression, leading to gradual increase in the nuclear width at the expense of its length (Fig. 8). In addition, the axoneme extends backwards from a centriolar derivative in the implantation fossa, so that vertical sections through a developing euspermatozoon at this stage present hammer-head and handle con- figurations (Fig. 10).
A second phase of chromatin condensa- tion is evident in middle spermatids as the mid-anterior portion of the nucleus, opposite to the axoneme, begins a forward movement. During this phase, fibrils are arranged longi- tudinally parallel to the nuclear antero-poste- rior axis (Fig. 11). As fibrils increase in thick- ness, they stan to fuse into fibers and subsequently into lamellae representing thereby the lamellar phase of chromatin con- densation (Figs. 13-15). Chromatin conden- sation culminates in a homogenous, com- pact club-like nucleus with no distinct ultrastructure (Fig. 19).
Concomitant with nuclear condensation, a growing axoneme pushes the nucleus for- ward to increase its length, while the nuclear width is reduced under a force of lateral com- pression. This leads to progressive lengthen- ing of the antero-posterior nuclear axis, thus reversing its trend in the previous stages (Figs. 10, 11). The mature nucleus in C. bifas- ciata and C. tuberculatus has a short poste- rior invagination accommodating the proxi- mal portion of the axoneme (Figs. 16, 19).
The euspermatozoan tail in C. bifasciata and C. tuberculatus is composed of a middle piece, a glycogen piece and an end piece. The posterior nuclear envelope becomes in- dented at its center defining thereby the im- plantation fossa, which represents the point
of axoneme development (Fig. 6). The gene- sis of the axoneme appears to be associated with a single dense structure (centriolar de- rivative), which does not seem to possess the common pattern of centriolar arrangement (Fig. 6). As nuclear condensation com- mences, mitochondrial fusion gives rise to four large spherical mitochondria at the pos- terior nuclear pole (Fig. 7). The association of these spheres with the nucleus is achieved by their attachment to four posterior nuclear depressions, and it represents the first step in midpiece development, which is concom- itant with the granular phase of nuclear con- densation. The mitochondrial cristae are modified into parallel cristal plates that have undergone considerable reorganization as mitochondria form a sheath around the typi- cal 9 + 2 axoneme (Figs. 10, 11). Transverse sections through the midpiece reveal four non-helically arranged mitochondrial ele- ments, two of which are semicircular large elements that are arranged perpendicular to the central pair of axonemal microtubules, and each reveals multiple cristal plates. The other two mitochondrial elements are ex- tremely small and are aligned with this central pair, showing at most one cristal plate (Fig. 21). In addition, a ring of microtubules is ob- served surrounding the midpiece at late stages of its development (Fig. 21). Glycogen granules in the glycogen piece are organized in nine tracts; one per microtubular doublet (Fig. 24), and the transition zone between the midpiece and the glycogen piece is marked by a dense ring structure that is attached to the euspermatozoan plasma membrane (Fig. 22). The latter continues to encircle the ax- onemal microtubules, forming the end piece of the tail (Fig. 25), without a distinct transi- tion structure between the glycogen piece and the end piece (Fig. 23). Cytoplasmic bridges connect adjacent developing sper- matids throughout various stages of eusper- miogenesis (Figs. 3, 11).
DISCUSSION
Euspermiogenesis as seen in Clypeomorus bifasciata and C. tuberculatus includes many common features that were reported in all other cerithiaceans (Giusti, 1971; Healy, 1982a, 1984; Koike, 1985; Afzelius et al., 1989, Hodgson & Heller, 1990; Minniti 1993) as well as other mesogastropods and neo- gastropods (Giusti, 1969; Buckland-Nicks &
ATTIGA & AL-HAJJ
52
FIGS. 8-15.
ULTRASTRUCTURAL STUDY OF EUSPERMIOGENESIS 53
Chia, 1976; West, 1978; Griffond, 1980; Kohnert, 1980; Healy 1983b; Koike 1985). In general, acrosome formation is associated with Golgi complex and involves the produc- tion of a proacrosomal vesicle, which occurs anywhere in the cytoplasm, because there is no definite route of acrosome migration from the posterior to the anterior pole of the de- veloping spermatid. This situation was re- ported in other cerithiaceans (Healy, 1982a, 1986a; Minniti, 1993), in contrast to many other mesogastropods and neogastropods, in which such a route is marked and linked to various stages of nuclear shaping (Buckland- Nicks & Chia, 1976; West, 1978; Jong-Brink et al., 1977; Buckland-Nicks et al., 1983; Jaramillo et al., 1986, Gallardo & Garrido, 1989). Cerithiids, including those used in this study, are characterized by a high degree of development of the pre-attachment ac- rosome. Prior to its attachment to the nu- cleus, the acrosome bears an acrosomal cone, an acrosomal rod-like material and an interstitial granule, which gives rise to the basal plate; these constitute the elements of the mature acrosome.
Because spermiogenesis involves several complex processes of cellular shaping and remodeling, microtubules and microfilaments are expected to play a crucial rule in these processes. In contrast to other reported cer- ithiids, microtubules were seen within the de- veloping acrosomal cones of Clypeomorus bifasciata and C. tuberculatus. This was
strongly suggested by the longitudinal sec- tions cutting through the developing ac- rosomes (Figs. 4, 9) as well as the hollow round structures seen in transverse sections (Fig. 18). Such an arrangement of microtu- bules within the cone is thought to provide it with a degree of rigidity, and aid in its elon- gation after it attaches to the nucleus, as was suggested in some non-cerithiacean meso- gastropods and neogastropods (Walker & MacGregor, 1968; Buckland-Nicks & Chia, 1976; Giusti & Mazzini, 1973). Other cerithiids as well as other mesogastropods and neo- gastropods have a ring of microtubules surrounding developing acrosomes (Buck- land-Nicks & Chia, 1976; Huaquin & Bustos- Obergon, 1981; Buckland-Nicks et al., 1983; Healy, 1983b). In addition, microtubules were seen around midpieces of Clypeomorus bi- fasciata and C. tuberculatus at late stages of development. Their appearance at such late stages in these two cerithiids as well as other mesogastropods (Jong-Brink et al., 1977; Kohnert, 1980; Griffond, 1980; Healy, 1982a, 1983a, b, 1988b; Buckland-Nicks et al., 1983; Afzelius et al., 1989; Al-Hajj & Attiga, 1995) strengthens the idea that they are im- portant in sloughing the excess cytoplasm around midpieces as well as other parts of the euspermatozoon (Fawcett et al., 1971). Furthermore, the ornamentation of the ma- ture acrosomal cone with parallel plate-like substructures seen in Clypeomorus bifasci- ata and C. tuberculatus was also reported in
FIG. 8. C. tuberculatus. Early spermatid showing basal chromatin accumulation in nucleus (N), sites of mitochondrial (M) association with the nucleus (arrow heads), acrosomal cone (AC), interstitial granule (IG), and internal supporting structures (arrow) in acrosomal cone. 27,200
FIG. 9. C. tuberculatus early spermatid. Section showing acrosomal cone with microtubules (arrow) and internal supporting structures (arrows), subacrosomal space (SAS), and interstitial granule (IG). «50,000
FIG. 10. C. bifasciata. Middle spermatid showing interstitial granule (IG), hammer-like nucleus (N), and midpiece (MP). x22,400
FIG. 11. C. tuberculatus. Middle spermatid with a cytoplasmic bridge (asterisk) Showing acrosomal cone (AC), external supporting structure (ES), basal plate (BP), nucleus (N), and midpiece (MP). «15,000
FIG. 12. C. tuberculatus middle spermatid. Section showing acrosomal cone (AC), internal supporting structure (arrow heads), external supporting structure (ES), basal plate (BP), and fibrillar nucleus (N). x44 ,000
FIG. 13. С. bifasciata middle-late spermatid. Cross section in fibrillar nucleus. «23,750
FIG. 14. C. bifasciata late spermatid. Cross section in nucleus showing islands of lamellae. x35,000
FIG. 15. C. tuberculatus late spermatid. Cross section in nucleus with semi-fully condensed chromatin. х31,500
ATTIGA & AL-HAJJ
54
oe
A A À
RO = A At RU nn TE NS D
A Я
es us si,
LT, 53. ATA + nn in
Ly
Pr
FIGS. 16-25.
ULTRASTRUCTURAL STUDY OF EUSPERMIOGENESIS 55
other mesogastropods and neogastropods (Giusti & Mazzini, 1973; Healy, 1983a, 1986b; Jaramillo et al., 1986; Afzelius et al., 1989; Al-Hajj & Attiga, 1995). Acrosomal mem- branes in Chorus giganteus (Jaramillo et al., 1986), Truncatella subcylindrica (Giusti & Mazzini, 1973), and Melanopsis (Afzelius et al., 1989) were reported to have a scalloped appearance with regular periodicity. This or- namentation of the growing acrosome that is later hidden by electron-dense material seems to be of scarce occurrence. Giusti & Mazzini (1973) interpreted this periodicity as microtubular palisade, whereas Jaramillo et al. (1986) thought that it is due to the pres- ence of actin crests, which may play a role in acrosome reaction and egg penetration. However, the lack of Knowledge about ac- rosome reaction and fertilization in gastro- pods makes it difficult to conclude the nature or function of these structures, pending fur- ther investigation.
Chromatin condensation and nuclear shap- ing are two highly linked processes in sper-
miogenesis of mesogastropods and neo- gastropods. Chromatin condensation passes through granular, fibrillar and lamellar phases, culminating in a homogeneous compact nu- cleus with no ultrastructure (Walker & Mac- Gregor, 1968; Buckland-Nicks & Chia, 1976; Feral, 1977; West, 1978; Huaquin & Bustos- Obergon, 1981; Healy, 1982a, b, 1983b, 1988b; Buckland-Nicks et al., 1983; Jaramillo et al., 1986; Gallardo & Garrido, 1989). The mature nucleus in the two cerithiids investi- gated in this study has a short basal invagi- nation accommodating the proximal portion of the axoneme, which is a common nuclear shape seen in many other mesogastropods and neogastropods (Giusti, 1969, 1971; Giusti & Mazzini, 1973; Reader, 1973, Griffond, 1980; Kohnert, 1980; Koike & Nishiwaki, 1980; Healy, 1982a, b, 1983a, 1986b). On the other hand, some mesogastropods and many neo- gastropods have intranuclear canals that in- vaginate the nucleus completely up to its apex (Walker & MacGregor, 1968; Buckland-Nicks, 1973; Buckland-Nicks & Chia, 1976; West,
FIG. 16. С. tuberculatus mature euspermatozoon, with acrosome (A) and nucleus (N). x48,000 Inset: Section showing acrosomal cone (AC) with plate-like substructure (arrow head), acrosomal rod-like material (AR), and basal plate (BP). x57,500
FIG. 17. C. bifasciata semi-mature acrosome. Section showing acrosomal cone (AC) with plate-like sub- structure (arrow head), acrosomal rod-like material (AR), and basal plate (BP). x63,000
FIG. 18. C. bifasciata semi-mature euspermatozoon. Section in acrosome showing acrosomal rod-like material (AR), microtubules (MT) in acrosomal cone, and surrounding pseudopodium (PP) of nutritive cell. x40,000
FIG. 19. C. tuberculatus semi-mature euspermatozoa showing nucleus (N), centriolar derivative (CD) in nuclear basal invagination and midpiece with mitochondrial sheath (M) surrounding the axoneme (AX). x60,000
FIG. 20. C. tuberculatus semi-mature euspermatozoon. Cross section in nucleus (N) showing the proximal portion of the axoneme (arrows) within nuclear basal invagination. Notice pseudopodia (PP) of nutritive cells. x40,000
FIG. 21. С. bifasciata late euspermatozoon. Cross section in midpiece showing two large and two extremely small mitochondrial (M) elements surrounded by microtubules (arrows). x48,000
FIG. 22. C. tuberculatus mature euspermatozoon. Section showing dense ring structure (DRS) at the junction between midpiece with mitochondrial sheath (M) around axoneme (AX), and glycogen piece (GP). x38,000
FIG. 23. C. bifasciata mature euspermatozoa. Sections showing the junction between glycogen piece (GP) and end piece (EP). x52,000
FIG. 24. C. bifasciata mature euspermatozoa. Cross section in glycogen piece showing nine tracts of glycogen granules associated with axonemal microtubular doublets. x37,500
FIG. 25. С. bifasciata mature euspermatozoa. Cross section in end piece showing 9 + 2 pattern of micro- tubular arrangement surrounded by plasma membrane. x128,000
56 ATTIGA 8 AL-HAJJ
1978; Huaquin & Bustos-Obergon, 1981; Buckland-Nicks et al, 1983; Healy, 1984; Jaramillo et al., 1986; Hodgson, 1993). Healy (1983a) interpreted this extreme structural di- versity in the extent of nuclear invagination to factors in the reproductive environment, es- pecially because some superfamilies include both types of nuclei among their species (Buckland-Nicks, 1973; Healy, 1988a).
Centrioles were not seen in developing eu- spermatids in C. bifasciata and C. tubercula- tus, and the proximal portion of the axoneme was attached to the posterior nuclear invagi- nation through a single dense structure that has no apparent microtubules. This centriolar derivative was reported in other caeno- gastropods (Buckland-Nicks, 1973; Healy, 1982a, 1983a, 1986a, b, 1988b).
The midpiece in euspermatozoa of C. bi- fasciata and C. tuberculatus is consistent with those of other cerithiids and members of sub- group 1(i) of Healy’s (1983a) classification of mesogastropods as a group of caenogastro- pods. Midpieces in these animals are char- acterized by four non-helically arranged ele- ments, two of which are extremely small, whereas the other two are large showing mul- tiple cristal plates. The non-helical arrange- ment of mitochondria around the axoneme in Cerithiacea is considered a primitive charac- ter compared to the helical mitochondrial sheath seen in other mesogastropods and neogastropods (Walker & MacGregor, 1968; Giusti, 1969, 1971; Anderson & Personne, 1970; Buckland-Nicks, 1973; Giusti & Maz- zini, 1973; West, 1978; Koike & Nishiwaki, 1980; Kohnert, 1980; Griffond, 1980). This feature supports Healy's (1982a) proposi- tion that cerithiaceans represent ancestral mesogastropods, acting as a linkage group between primitive spermatozoa of Archaeo- gastropoda on one hand and modified sper- matozoa of higher mesogastropods and neo- gastropods on the other. Such a position makes it an interesting group to study sper- matozoan evolution.
In cerithiids, including those investigated in this study, the glycogen piece consists of nine tracts of glycogen granules associated with the nine doublets of the axonemal mi- crotubules. This arrangement, which is seen also in other mesogastropods and neogas- tropods (Giusti, 1969, 1971; Buckland-Nicks, 1973; Reader, 1973; West, 1978; Koike & Nishiwaki, 1980; Kohnert, 1980; Huaquin & Bustos-Obergon, 1981; Healy, 1982a, 1986a, b, 1988a, c; Jaramillo et al., 1986; Gallardo 8
Garrido, 1989; Al-Hajj & Attiga, 1995), is thought to be linked to the euspermatozoan motility, because the nine glycogen tracts in the mature euspermatozoa obscures nine ra- dial links between the axonemal doublets and the plasma membrane in the immature spermatid (Healy, 1983a).
Many investigators have suggested that acrosomal ultrastructure of gastropods could provide useful taxonomic data by being spe- cies-specific. In Cerithiacea, such a species- specific acrosome ultrastructure is not well presented. Species-specific features were seen when comparing acrosomes of Cerith- ¡um vulgatum (Giusti, 1971), C. nodulosum (Koike, 1985), C. rupestre (Minniti, 1993), C. caeruleum (Al-Hajj & Attiga, 1995), whereas Clypeomorus bifasciata, C. tuberculatus (this study), C. moniliferus (bifasciata), and C. breviculus (Healy, 1983a) have almost identi- cal acrosomes. In addition, differences in the ultrastructure of the acrosome were estab- lished at the generic level between Cerithium, Rhinoclavis, Australaba (Healy, 1983a), and Clypeomorus (Healy, 1983a; this study), but were not seen between euspermatozoa of Conomurex and Lambis, which possess very similar acrosomes (Koike & Nishiwaki, 1980).
In conclusion, comparative studies of sperm ultrastructure have proved to act as an acceptable guide for determining the affini- ties between major groups in gastropods as well as in many other animal groups.
ACKNOWLEDGMENTS
The authors are thankful to Dr. Saleem Al- Mograby from the Marine Science Station of the Gulf of Aqaba for help in providing access to collect the specimens from the station’s rocky beach.
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HEALY, J., 1988b, The ultrastructure of spermato- zoa and spermiogenesis in pyramidellid gastro- pods, and its systematic importance. Helgolán- der Wissenschaftriche Meeresuntersuchungen, 42: 303-318.
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(Bruxelles), 92: 259-274.
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KOHNERT, В. 8 V. STORCH, 1984 a, Vergleichend- ultrasrtukturelle untersuchungen zur morpholo- gie eupyrener spermien der Monotocardia (Prosobranchia). Zoologische Jahrbucher, 11: 51-93.
KOHNERT, R. & V. STORCH, 1984b, Elektronen- mikroskopische Untersuchungen zur Spermio- genese der eupyrenen Spermien der Monotocar- dia (Prosobranchia). Zoologischer Jahrbucher, 112: 1-32.
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NISHIWAKI, S., 1964, Phylogenetical study on the type of the dimorphic spermatozoa in Proso- branchia. The Science Report of the Tokyo Ky- oiku Daigaku, Sec. B, 2: 237-275.
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Revised Ms. accepted 28 November 1995
MALACOLOGIA, 1996, 38(1-2): 59-65
CA REGULATION IN THE FRESHWATER BIVALVE ANODONTA IMBECILIS: I. EFFECT OF ENVIRONMENTAL CA CONCENTRATION AND BODY MASS ON UNIDIRECTIONAL AND NET CA FLUXES
Dazhong Xu' & Michele С. Wheatly'
Department of Zoology, University of Florida, Gainesville, Florida 32611, USA
ABSTRACT
The present paper reports unidirectional and net Ca fluxes of a freshwater bivalve, Anodonta imbecilis, as a function of external Ca concentration and body mass. Larger animals were better able to maintain Ca balance than smaller animals, which experienced net loss of Ca. External Ca concentration had no significant effect on net Ca flux. Unidirectional Ca influx decreased with body mass and increased with external Ca concentration. The relationship between ex- ternal Ca concentration and unidirectional Ca influx follows the Michaelis-Menten equation. The estimated half saturation Ca concentration for unidirectional Ca influx and the maximum uni- directional influx were 0.213 mM and 4.329 ито! g dry mass 'h ', respectively. External Са concentration did not affect unidirectional Ca efflux of the animals. Unidirectional Ca efflux
decreased with body mass.
Key words: Calcium flux, calcium concentration, body mass, bivalve.
INTRODUCTION
While calcification has been relatively well studied in molluscs (reviewed by Watabe, 1983), the contribution made by whole body unidirectional Ca flux to Ca regulation in bi- valves has not been well established.
In molluscs, various epithelia can take up external Ca (Van der Borght, 1963; Van der Borght & Van Puymbroeck, 1964; Green- away, 1971; Thomas et al., 1974), especially the mantle surface facing the mantle cavity (Jodrey, 1953; Horiguchi, 1958) and the gill (Horiguchi, 1958). The active transport of Ca was demonstrated in the freshwater gastro- pods Lymnaea stagnalis (Van der Borght & Van Puymbroeck, 1964; Greenaway, 1971) and Biomphalaria glabrata (Thomas et al., 1974). Based on models for active Ca uptake into other freshwater species (for example te- leost fish, Flik et al., 1985), the epithelial up- take occurs in two stages: diffusion down an electrochemical gradient across the apical membrane into the cytosol, and active trans- port across the basolateral membrane into the haemolymph. If, as in other freshwater species, the Ca pump in molluscan epithelia is Ca-activated ATPase (Watabe, 1983), the rate of Ca uptake should be correlated with the Ca concentration in the ambient water.
Previous studies showed that this is true for some molluscs (Greenaway, 1971; Thomas et al., 1974; Russell-Hunter, 1978; Pynnonen, 1991) but not others (Hunter, 1975; Russell- Hunter et al., 1981).
Allometry refers to the scaling of physio- logical function/morphological parameters to body mass. Interspecific allometry of captive aquatic molluscs described scaling of water flux to body mass (Nagy & Peterson, 1988). Significant relationships between dry body mass and shell length, shell height, gut-pas- sage time, gut content or metabolic fecal loss have also been reported (Hawkins et al., 1990). The relationship between dry mass and oxygen consumption had a negative cor- relation (Dietz, 1974).
The present study uses radiotracer tech- niques to determine the unidirectional Ca fluxes in a freshwater bivalve, Anodonta im- becilis, as a function of external Ca concen- tration and body mass.
MATERIALS AND METHODS
Experimental Animals and General Holding Conditions
The freshwater bivalves Anodonta imbeci- lis (6-58 g) were collected 60 km from Gainesville, Florida, from a canal along the
‘Present Address: Department of Biological Sciences, Wright State University, Dayton, OH 45435, USA.
59
60 XU & WHEATLY
TABLE 1. Wet and dry mass of animals used to determine the effect of body mass on unidirectional
and net Ca flux.
group 1 group 2 group 3 group 4 wet mass (g) 15 == 0:89 15.88 + 0.56 25.98 + 1.40 44.02 + 2.03 dry mass (9) 0.362 + 0.041 0.511 + 0.064 1.061 + 0.076 1.929 + 0.171
Mean + SEM. М (groups 2, 3, 4) = 10. М (group 1) = 9.
Suwannee River at Fanning Springs. The ап- imals collected were kept in aquaria with aged and well-aerated 21°C Gainesville tap water with the following cationic composition (in mM): Nat, 0.55; К*, 0.04; Са?*, 0.60; Mg?*, 0.42; and СГ, 0.73. The pH was 7.7. Food was withheld for the holding period (up to two months), and animals were used within two months of collection. Animals were acclimated in aquaria for at least 10 days before measurements were made. Only healthy animals (indicated by relatively heavy weight, active ventilation and powerful water ejection upon disturbance) were used in the experiments. All experiments were con- ducted at 21°C.
Unidirectional and Net Ca Fluxes—Effect of External Ca Concentration
Four groups of animals were used in the experiment. The Ca concentrations of the ex- perimental media were 0.27, 0.60, 1.00 and 2.00 mM, respectively. The outer surface of the shell of the experimental animals was covered with wax to prevent direct Ca loss from the shell/water interface. Animals were acclimated in the experimental water for 3 days before conducting the experiment. Me- dia with Ca concentration of 1.00 and 2.00 mM were made by adding CaCl. to Gaines- ville tap water (0.6 mM Ca). The medium with Ca concentration of 0.27 mM was made us- ing the following recipe (in mM): NaCl, 0.4; CaCl,, 0.27; NaHCO,, 0.2; and KCI, 0.04. An- imals were placed individually in experimen- tal flux chambers containing 300 ml medium and acclimated for more than 12 hours. At the beginning of a flux measurement, the wa- ter was drained from the chamber and 200 ml fresh medium were added. An initial water sample was taken from each chamber and then 1 uCi of *°Ca (CaCl, in water, 10 mCi ml *, Du Pont) was added to each chamber. Water samples were taken from each cham- ber at t= 0h and t = 6 В for determination of radioactivity and Ca concentration. These samples were used to estimate net and uni-
directional Ca fluxes. At the end of the exper- iment, animals were sacrificed by cutting the adductor muscles using a dissecting knife. Soft tissues of each animal were then dis- sected out and dried to constant weight to determine dry mass. In a parallel experiment, empty shells (the valves sealed together and covered with wax on the outer surface) were bathed in an identical chamber to estimate the possible accumulation of *°Ca by the shell surface. Throughout the paper, dry mass means the dried mass of the soft tis- sues (excluding shells), wet mass refers to the whole wet mass of the animals (including shells).
Unidirectional and Net Ca Flux—Effect of Body Mass
Bivalves with wet mass of 6-58 g (N = 39) and dry mass of 0.2-2.7 g were used in the experiment. Animals were divided into four groups according to wet mass (Table 1). Groups were numbered 1 to 4 (small to large). For each group, the flux volume and isotope addition were as follows: group 1, 100 ml and 0.5 uCi *°Ca; group 2 and 3, 150 ml and 0.8 uCi “Ca; group 4, 200 ml and 1 uCi *°Ca. The experimental method was the same as described above. The Ca concen- tration of the media was 1 mM.
Analytical Methods
Water samples (3 ml) were mixed with ScintiVerse fluor (3 ml) and then radioactivity was measured using a liquid scintillation counter (LSC, Beckman LS5801). The Ca concentration of experimental water or extra- pallial fluid (EPF) was measured after appro- priate dilution (0.2 ml sample + 2 ml 2% LaCl, + 1.8 ml distilled water) using an atomic ab- sorption spectrophotometer (Perkin Elmer 2100).
Calculation
The flux equation described by Wheatly (1989) was used to calculate unidirectional Ca influx:
Ca REGULATION IN THE FRESHWATER BIVALVE ANODONTA IMBECILIS 61
Jin = =——— (1)
where Jin is unidirectional Ca influx (umol g dry mass 'h '), Ri and Rf are the initial and final radioactivity (cpm ml ') of respective water samples, V is the flux volume (ml), SA is the medium mean specific radioactivity (cpm umol ') calculated as the mean radioactivity divided by the mean Ca concentration, t is the elapsed time (h), and W is the dry mass of the animal (9). Net flux was calculated as:
(EL—IEHV Hehe? (2) tW where Jnet is Ca net flux (umol g dry mass h '), Ci and Cf are the initial and final me- dium Ca concentrations (mM), V is the flux volume (ml), t is the elapsed time (h), and W is the dry mass of the animal (g). A positive value for net flux indicates net Ca influx while a negative value indicates net Ca efflux. Unidirectional efflux was calculated using the conservation equation:
1
Jout = Jin — Jnet (3) Statistical Analysis
Data were expressed as mean and stan- dard error (+ SEM). The statistical analysis was performed using StatView 4.01 and Su- per ANOVA computer packages. Correlation analysis was performed by calculating corre- lation coefficients (r values) and using Fish- er's rto z method to test the significance of correlation. One-factor ANOVA was used to analyze differences between groups and then Fisher's PLSD test was used when nec- essary to compare the means. ANCOVA was used to compare the slopes and intercepts of different linear relationships. The significance level for all statistical analyses was set at 0.05.
RESULTS
Empty shells showed no significant accu- mulation of “Са on the waxed outer shell surface. Ca net flux was affected by the Ca concentration in the medium (Fig. 1). Animals in medium containing 0.27 mM Ca showed a significant net Ca efflux of — 1.63 + 0.24 umol g dry mass 'h ' (М = 9) compared to those
D Ori © M NO vw» y
Ca flux (umol g dry mass hl do
A
0 0.5 1 1.9 2
Ca concentration in the medium (mmol I!)
FIG. 1. Unidirectional and net fluxes of Anodonta imbecilis in media of different Ca concentrations. Points represent mean and standard errors. The wet mass of animals used were as follows: group 1 (Ca = 0.27 mM), 41.59 + 2.30 g (N = 9); group 2 (Ca = 0.6 mM), 40.14 + 2.41 g (N = 10); group 3 (Ca = 1.0 mM), 44.02 + 2.03 g (N = 10); group 4 (Ca = 2.0 mM), 43.59 + 2.07 g (N = 8). The equation of the curve fitting the influx data is: influx 4.329C/(0.213 + C), where C is the Ca concentration of the me- dium; r = 0.996.
of the animals in media containing 0.60 mM (Fisher’s PLSD, p = 0.0036), 1.00 mM (Fish- er's PLSD, p = 0.0007) and 2.00 mM Ca (Fisher’s PLSD, p = 0.0001). There were no significant differences in Ca net flux in Ca concentrations of 0.60, 1.00, 2.00 mM (Fish- er’s PLSD, p = 0.1500 for the largest differ- ence).
There was a nonlinear relationship be- tween the unidirectional Ca influx and the ex- ternal Ca concentration (Fig. 1). The unidirec- tional influxes for animals in media containing 0.27, 0.60, 1.00 and 2.00 mM Ca were sig- nificantly different (one-factor ANOVA, p = 0.0132). The mean unidirectional influx in- creased as external Ca concentration in- creased, was partially saturable and could be approximately described by the Michaelis- Menten equation:
Influx = К (4)
m+C
where K is the maximum rate of unidirec- tional Ca influx, Km is the Ca concentration in the medium at which half saturation is at- tained, and C is the Ca concentration in the
62 XU & WHEATLY
dry mass = 0.047(wet mass) -0.184 e
Dry mass (g)
Wet mass (g)
FIG. 2. Relationship between dry mass and wet mass of Anodonta imbecilis. Points represent the mass of individual animals; r = 0.909 for regression. Fisher’s r to z, p < 0.0001, N = 39.
medium. The calculated half saturation Ca concentration for unidirectional Ca_ influx (Km) was 0.213 mM. The maximum unidirec- tional influx (K) was 4.329 umol g dry mass
'h '. Thus, the following equation can be used to describe the relationship between unidirectional influx and external Ca concen- tration:
C ntux=4:329 == (5) 0.213+C
Unidirectional Ca effluxes showed no sig- nificant difference among animals in media with different Ca concentration (one factor ANOVA, p = 0.7807; Fig. 1).
The dry mass of bivalves (excluding shell) was positively correlated with wet mass (r = 0.909, Fisher's r to z, p < 0.0001, Fig. 2). Larger animals generally maintained Ca bal- ance as indicated by the negligible net flux (Fig. 3). However, animals smaller than 0.5 g tended to exhibit a negative Ca balance as indicated by a net efflux (Fig. 3). Both the unidirectional Ca influx and efflux decreased with increase in dry body mass. Negative lin- ear relationships were derived between log unidirectional Ca influx and log dry mass (r = — 0.800, Fisher's r to z, p < 0.0001), and log unidirectional efflux and log dry mass (r = — 0.862, Fisher's r to z, p < 0.0001; Fig. 4). The slopes and intercepts respectively were as follows: —4.03, 6.52 (unidirectional influx) and —8.34, 7.54 (unidirectional efflux). The
slope and intercept for unidirectional efflux were both significantly higher than those for unidirectional influx (ANCOVA, p = 0.0001).
DISCUSSION
Active unidirectional Ca influx that follows enzyme saturation kinetics has been previ- ously demonstrated in freshwater snails. Greenaway (1971) found in the snail Lymnaea stagnalis that active uptake of Ca was nec- essary below external levels of 0.5 mM. The uptake mechanism was half-saturated and near-saturated in external media containing 0.3 and 1.0-1.5 mM Ca, respectively, and snails showed a positive Ca balance in media containing more than 0.062 mM Ca. For the snail Biomphalaria glabrata, the half and near saturated Ca concentration for Ca uptake were 0.267 and 1.0-2.0 mM, respectively, and the minimum equilibrium concentrations were 0.012-0.025 mM for a closed system and 0.25 mM for an open system (Thomas et al., 1974). Both animals exhibited a high af- finity Ca uptake mechanism. In the present study, the unidirectional Ca influx of A. imbe- cilis seems to display the same kinetics as a function of external Ca concentration. The half saturation Ca concentration in the me- dium was 0.213 mM, lower than the value estimated for the freshwater snail L. stagnalis (0.3 mM; Greenaway, 1971) and the value es-
Ca REGULATION IN THE FRESHWATER BIVALVE ANODONTA IMBECILIS 63
m 5 я 0 a 3 SN a = -10 FE a -15 O E -20 3 -25
do =
0 р
Dry mass (2)
FIG. 3. Relationship between Ca net flux and body dry mass of Anodonta imbecilis. Points represent Ca net flux of individual animals. The Ca concentration of the medium is 1 mM. N = 36.
— o o
Ca flux (umol g dry mass Ih’)
0.1
log (influx) = -0.4028log (dry mass) + 0.6520 log (efflux) = -0.8342log (dry mass) + 0.7548
—e—influx
+ efflux
Dry mass (g)
FIG. 4. Relationship between log unidirectional Ca influx and log dry mass (r = 0.800, Fisher's r to z, p < 0.0001), and between log unidirectional Ca efflux and log dry mass (r = 0.862, Fisher's r to z, p < 0.0001) of Anodonta imbecilis. Points represent the unidirectional influx or efflux of individual animals. The slopes for log unidirectional influx and log unidirectional efflux are significantly different (ANCOVA, p = 0.0001). N
= 36.
timated for the freshwater snail Biomphalaria glabrata (0.267 mM; Thomas et al., 1974).
If the unidirectional Ca efflux is purely by passive diffusion, one would expect unidirec- tional efflux to decrease as the external con- centration is raised. Because unidirectional Ca efflux was unaffected by change in exter-
nal Ca concentration, other mechanisms may be involved. Greenaway (1971) suggested that part of the unidirectional Ca influx in L. stagnalis is due to exchange diffusion and that this component increases when external Ca concentration increases following en- zyme-saturation kinetics. If the unidirectional
64 XU & WHEATLY
Ca efflux in A. imbecilis is attributable to ex- change diffusion, then unidirectional efflux would increase as external Ca rises. Any por- tion of unidirectional Ca efflux not attributed to exchange diffusion (‘routine loss””) would decrease with the increase in external Ca concentration because of the reduction in concentration gradient. The combined effect might be that unidirectional Ca efflux is un- changed. The net Ca flux of animals in media of different Ca concentration mirrored the change in unidirectional Ca influx because unidirectional Ca efflux remained constant. This pattern of Ca net flux is similar to the Ca net uptake pattern of L. stagnalis in media of different Ca concentration (Greenaway, 1971). The difference between these two an- imals is that in A. imbecilis Ca net flux was negative as opposed to the net uptake exhib- ited by L. stagnalis.
The relationship between wet and dry mass of A. imbecilis is linear, indicating the proportional increase of soft body tissue with shell and water content. A similar relationship was found between shell weight and fresh tissue weight in the freshwater snail L. stag- nalis (Greenaway, 1971).
Few animals in this study exhibited a sig- nificant net uptake of Ca from the medium, suggesting that considerable Ca is obtained from dietary sources. The freshwater snail Lymnaea stagnalis was found to obtain 20% of its calcium from food (Van der Borght & Van Puymbroeck, 1966). This is also consis- tent with previous work, which demonstrated that freshwater bivalves obtain part of their Ca from food (Pynnonen, 1991).
Larger animals are better able to maintain their Ca balance with the environment than smaller animals, which tend to lose Ca to the medium. This was due to the fact that unidi- rectional Ca efflux is larger than Ca influx in small animals and decreases at a greater rate with increase in body mass. This implies that smaller animals depend more on dietary Ca than larger animals, possibly since they cal- cify their shell more rapidly.
Allometric regression showed that unidi- rectional Ca fluxes decreased with dry body mass of A. imbecilis. Thus, smaller animals exchange Ca with their environment more rapidly commensurate with an increased sur- face area to volume ratio. This result is similar to a recent study on crayfish, which revealed that the diffusional and active ¡on flux rates are both greater in small crayfish (Wheatly et al., 1991). An allometric study of Na fluxes in
amphibia (Pruett et al., 1991) showed that re- gression lines for unidirectional Na influx and efflux had the same slope and intercept con- firming Na balance in animals of all size. In the present study, efflux decreased more than influx with increase of body dry mass resulting in significantly greater net efflux of Ca in smaller animals.
ACKNOWLEDGMENTS
This research was supported by NSF grant DCB 89 16412 to MGW. We thank Drs. Karen Bjorndal, David Evans and Frank Nordlie for their suggestions on the research and for use of experimental equipment. We thank Dr. Jim Williams, Ms. Jane Brimbox and Mr. Ricardo Lattimore in the U.S. Fish and Wildlife service for their help in collecting experimental ani- mals.
LITERATURE CITED
DIETZ, T. H., 1974, Body fluid composition and aerial oxygen consumption in the freshwater mussel, Ligumia subrostrata (Say): effects of de- hydration and anoxic stress. Biological Bulletin, 147: 560-572.
FLIK, G. R., J. Н. VANRIJS & S. E. WENDELAAR ВОМСА, 1985, Evidence for high-affinity Са?*- ATPase activity and ATP-driven Ca”*-transport in membrane preparations of the gill epithelium of the cichlid fish Oreochromis mossambicus. Journal of Experimental Biology, 119: 335-347.
GREENAWAY, P., 1971, Calcium regulation in freshwater mollusc Limnaea stagnalis (L.) (Gas- tropoda: Pulmonata). |. The effect of internal and external calcium concentration. Journal of Ex- perimental Biology, 54: 199-214.
HAWKINS, А. J. S., E. NAVARROL & J. I. P. IGLE- SIAS, 1990, Comparative allometries of gut-pas- sage time, gut content and metabolic faecal loss in Mytilus edulis and Cerastoderma edule. Ma- rine Biology, 105: 197-204.
HORIGUCHI, Y., 1958, Biochemical studies on Pteria (Pinctada) martensii (Dunker) and Hyriop- sis schlegeli (Martens) IV. Absorption and trans- ference of *°Ca in Hyriopsis schlegeli (Marterns). Bulletin, Japanese Society of Scientific Fisheries, 23: 710-715.
HUNTER, R. D., 1975, Variation in population of Lymnaea palustris in upstate New York. Ameri- can Midland Naturalist, 94: 401-420.
JODREY, L. H., 1953, Studies on shell formation. Ill. Measurement of calcium deposition in shell and calcium turnover in mantle tissue using the mantle-shell preparation and *°Ca. Biological Bulletin, 104: 398-407.
Ca REGULATION IN THE FRESHWATER BIVALVE ANODONTA IMBECILIS 65
NAGY, K. A. & C. C. PETERSON, 1988, Scaling of water flux rate in animals. University of California Press, Berkeley.
BRUERS 5. 4., О. Е. HOYT & В. Е. STEFLER, 1991, The allometry of osmotic and ionic regu- lation in amphibia with emphasis on intraspecific scaling in larval Ambystoma tigrinum. Physiolog- ical Zoology, 64: 1173-1199.
PYNNONEN, K., 1991, Accumulation of *°Ca in the freshwater Unionids Anodonta anatina and Unio tumidus, as influenced by water hardness, pro- tons, and aluminum. Journal of Experimental Zo- ology, 260: 18-27.
RUSSELL-HUNTER W. D., 1978, Ecology of fresh- water pulmonates. Pp. 335-383, in: V. FRETTER & J. PEAKE, eds., Pulmonates 2A, Academic Press, London.
RUSSELL-HUNTER, W. D., A. J. BURKY & R. D. HUNTER, 1981, Interpopulation variation in cal- careous and proteinaceous shell components in the stream limpet, Ferrissia rivularis. Malacolo- gia, 20: 255-266.
THOMAS, J. D., M. BENJAMIN, A. LOUGH & В. H. ARAM, 1974, The effects of calcium in the ex- ternal environment on the growth and natality rates of Biomphalaria glabrata. Journal of Animal Ecology, 43: 839-860.
VAN DER BORGHT, O., 1963, In- and outflux of
Ca-ion in freshwater gastropods. Archives Inter- nationales de Physiologie et de Biochimie, 71: 46-50.
VAN DER BORGHT, O. & S. VAN PUYMBROECK, 1964, Active transport of alkaline earth ions as physiological base of the accumulation of some radio-nuclides in freshwater molluscs. Nature, 204: 533-535.
VAN DER BORGHT, O. & S. VAN PUYMBROECK, 1966, Calcium metabolism in a freshwater mol- lusc: quantitative importance of water and food as supply for calcium during growth. Nature, 210: 791-793.
WATABE, N., 1983, Shell formation. Pp. 236-287, in: K. M. WILBUR 8 A. S. M. SALEUDDIN eds., The Mollusca Vol. 4. Physiology, Academic Press, New York.
WHEATLY, M. G., 1989, Physiological responses of the crayfish Pacifastacus leniusculus to envi- ronmental hyperoxia. Journal of Experimental Bi- ology, 143: 33-51.
WHEATLY, M. G., F. P. ZANOTTO & A. T. GAN- NON, 1991, Allometry of postmolt calcification and associated ¡on fluxes in crayfish. American Zoologist, 31: 119A.
Revised Ms. accepted 1 January 1996
MALACOLOGIA, 1996, 38(1-2): 67-85
MICROSCULPTURES OF CONVERGENT AND DIVERGENT POLYGYRID LAND-SNAIL SHELLS
Kenneth C. Emberton
Department of Malacology, Academy of Natural Sciences of Philadelphia, 1900 Benjamin
Franklin Parkway, Philadelphia, Pennsylvania 19103-1195, U.S.A.
ABSTRACT
Polygyrid evolution has produced five pairs of closely convergent shell forms, four of which occur in sympatry. Scanning electron microscopy of the apertural parietal and basal denticles (or regions) (at about 500x) in those ten species, and of the body whorl (at about 100x) in those and eleven more polygyrid species, reveals possible new microsculptural characters, homol- ogies, and radiations. Twelve informative new character states are tentatively proposed, of which half support, without homoplasy, previous shell-free phylogenetic hypotheses based on anatomy and allozymes. Two of the homoplastic characters actually enhance shell-form con- vergences, which are nonetheless distinguishable using other microsculptural features. Further SEM studies are warranted to test these proposed characters, to add others, and to test the hypothesis that shell micromorphology is much more informative than shell macromorphology
for land-snail phylogenetics.
Key words: Gastropoda: Stylommatophora, morphology, systematics, phylogenetics, cla-
distics, SEM.
INTRODUCTION
Polygyrid shell-form evolution is unique for its multiple close convergences in sympatry and is also noteworthy for its sudden diver- gences; shell-sculpture evolution in polygy- rids is also of great interest for its repeated convergences on periostracal hairs and its divergences among sister taxa (Pilsbry, 1940; Solem, 1976; Emberton, 1988, 1991a, 1994a, 1995a, 1995b; Asami, 1988, 1993). These combinations of close convergences and rapid divergences make it virtually impossi- ble to reconstruct polygyrid phylogeny from gross shell morphology, even when develop- mental characters are viewed by x-ray (Em- berton, 1995b). Polygyrid shell convergences and divergences, however, have so far been compared only macroscopically, at magnifi- cations no greater than 50x.
The purpose of this paper is a preliminary assessment of the the microsculptures of se- lected polygyrid shell convergences and di- vergences, using scanning electron micros- copy (SEM).
Four species of polygyrids have previously been examined under SEM for microsculp- tural features of the apertural lip: Stenotrema barbatum (Clapp) (Solem, 1972: figs. 23, 24 = Solem, 1974: fig. 5), as well as Daedalochila
67
auriformis (Bland), Millerelix mooreana (Bin- ney), and M. doerfeuilliana sampsoni (Weth- erby) (Solem & Lebryck, 1976: figs. 33-46). All four species had fields of hexagonal to rounded crystalline plates, uplifted on one side, and those plates varied in size and dis- tributional pattern among species. Intraspe- cific variation was studied in D. auriformis, with the important discoveries that the pari- etal and the palatal apertural denticles dif- fered in microsculpture, and that a gerontic shell had more strongly developed micro- sculpture than a younger adult shell (Solem & Lebryck, 1976).
Only a single polygyrid specimen has pre- viously been examined under SEM for shell periostracal microsculpture. Stenotrema bar- batum exhibited at 195x and 360x a regular array of gradually tapered, sharp-pointed hairs, seemingly round in cross-section and projecting perpendicularly from a surface field of subparallel, slightly anastomosing ridges (Solem, 1974: fig. 6).
The present study is a preliminary survey, based on only one shell per species (al- though including several pairs of sister spe- cies), so the microsculptural characters dis- covered herein must be considered tentative. In order to minimize the known sources of intraspecific variation (Solem & Lebryck,
68 EMBERTON
1976), only gerontic shells were used and both parietal and palatal apertural denticles (or regions) were examined.
MATERIALS AND METHODS
Twenty-one polygyrid species were cho- sen for examination; Figure 1 presents their phylogenetic relationships as hypothesized from anatomical and biochemical data (Em- berton, 1988, 1991a, 1994a, 1995b). The species include North America's four most extreme cases of shell-form convergence in sympatry (Emberton, 1995b: fig. 1): globose Neohelix major and Mesodon normalis, um- bilicate Allogona profunda and Appalachina sayana, flat Xolotrema fosteri and Patera lae- vior, and tridentate Triodopsis fallax and In- flectarius inflectus. A fifth shell-form conver- gence (Emberton, 1991b) was also included: “lipped” Neohelix dentifera and Inflectarius ferrissi.
Additional polygyrid species were included for their periostracal-microsculpture diver- gences and convergences. Xolotrema deno- tata and X. obstricta are sister species (Em- berton, 1988) that can hybridize in the field (Vagvolgyi, 1968) and in the laboratory (Webb, 1980), but their differences in shell- whorl shape and sculpture are extreme. Xo- lotrema obstricta has a strongly keeled pe- riphery and is sculpted with large, strongly raised ribs, whereas X. denotata has a rounded periphery and is sculpted with hair- like processes (Pilsbry, 1940; Emberton, 1988). The keeled, ribbed shell of X. obstricta is closely paralleled by that of Patera sargen- tiana (Pilsbry, 1940; Emberton, 1991a), with which it is sympatric in northern Alabama. Species of the Patera radiation (Emberton, 1991a) have diverged primarily in their shell surface sculpture: P. laevior is smooth, P. sargentiana is ribbed, P. perigrapta bears in- cised spiral grooves, and P. appressa sculp- tior is pustulose (Pilsbry, 1940).
Hair-like periostracal processes on the shell surface have arisen independently and convergently (Emberton, 1995b) in Xolotrema denotata, in some Vespericola such as V. co- lumbiana pilosa, in the Stenotrema clade, and in the /nflectarius clade (Pilsbry, 1940). Stenotrema's radiation is marked by extreme divergence in shell hairs, the variation of which includes short and dense (e.g. S. max- illatum), and long and sparsely distributed (e.g. S. barbigerum) (Pilsbry, 1940). To a
much smaller degree, the general shapes of shell hairs also seem (at 50x) to differ among species of /nflectarius: broad-based and sharp-tipped in I. inflectarius and I. magazin- ensis, acutely triangular in /. smithi, obtusely triangular in /. subpalliatus, and lost in I. fer- rissi, the sister species of I. subpalliatus (Em- berton, 1991a).
All studied shells are in the collection ofthe Academy of Natural Sciences of Philadelphia (ANSP). Species authors